American Journal of Primatology 37:103-125 (1995)

Temperament in Nonhuman Primates

A. SUSAN CLARKE' AND SUE BOINSKI'
'Asher Center for the Study and Treatment of Depressive Disorders, Northwestern University
Medical School, Chicago and Harlow Primate Laboratory, University of Wisconsin, Madison;
Department of Anthropology, and Division of Comparative Medicine, University of Florida,
Gainesville and Laboratory of Comparative Ethology, NZCHD, National Znstitutes of
Health-A nimal Center Poolesuille, Maryland

Formerly applied to studies of responsivity in children, in more recent

years the concept of temperament has been applied to nonhuman primates
at the individual, species, and now population levels. While the concepts of
temperament and personality have been less distinguished in nonhuman
primate studies than in the human literature, temperamental and person-
ality differences have now been identified among individual primates and
among primate species in a number of studies. At the individual level,
certain temperamental characteristics have been associated with age, sex,
and most frequently rank. At the species level, temperamental profiles
have been linked to intraspecific differences in social systems, sociodemo-
graphics, and features of life history and ecology. In this report we discuss
the application of the temperament concept to nonhuman primates and
review findings from studies of primate temperament at the individual,
population, and species level. We also cite evidence for genetic and expe-
riential influences on temperament in primates, outline concepts related
t o possible evolutionary influences on temperament, and discuss the pos-
sible relation of temperamental characteristics to social behavior and ecol-
ogy in selected species. o 1995 Wiley-Liss, Inc.

Key words: temperament, personality, behavioral traits, reactivity,

individual differences, species differences

INTRODUCTION: THE CONCEPT OF TEMPERAMENT

The concept of temperament originated from studies of infants and young
children, in which consistent response styles in novel situations could be identified
in a certain proportion of children at an early age. Such terms as bold vs. shy,
inhibited vs. uninhibited, highly reactive vs. unreactive, highly fearful vs. unfearful,
and emotional vs. unemotional have been used to characterize the behavioral styles
of young children in response to novel and/or challenging situations. The similar-
ity among terms indicates the primary dimension by which children are charac-
terized-that is, whether they tend t o approach or avoid novel stimuli and to what
extent they show negative emotional and heightened physiological responses to

Received for publication June 14, 1993; revision accepted February 2, 1994.
Address reprint requests t o A S . Clarke, Harlow Primate Laboratory, University of Wisconsin, 22 N.
Charter St., Madison, WI 53711.

0 1995 Wiley-Liss, Inc.

104 I Clarke and Boinski
novelty. While the precise definitions vary in the literature, the term temperament
refers to behavioral styles or tendencies (rather than discrete behavioral acts) that
show continuity over time and can be identified in early infancy. Such character-
istic styles are reflected in the degree and nature (i.e., approach vs. avoidance
[Kagan et al., 19921) of responsivity to novel or stressful stimuli, and nearly all
temperamental frameworks include a dimension of intensity, distress, or emotion-
ality [Lewis et al., 19891.
In addition to behavioral responsivity, physiological reactivity to challenge is
considered an important component of temperament, since it is believed that tem-
peramental response styles are based on biological underpinnings that are re-
flected in physiological responsiveness [Fox, 1989; Goldsmith et al., 1987; Gunnar,
1988; Healy, 1989; Kagan, 1989; Kagan & Snidman, 1991; Rothbart & Derryberry,
19811. Indeed, it has been argued that distinct and opposing temperamental styles
are based on constitutional variations in physiological organization that bias the
organism toward a certain temperamental response style from birth, although its
manifestation may require a particular environment [Kagan et al., 19921. The
primary physiological component of temperamental responsivity is the sensitivity
of the sympathetic nervous system (SNS) to stimuli. In human investigations,
measures of SNS activity in studies of temperament have included cardiac activity,
pupil dilation, norepinephrine and cortisol secretion, and facial cooling [Fox, 1989;
Gunnar, 1994; Gunnar et al., 1992; Kagan et al., 19921.
In children, the most widely used paradigm to measure temperamental char-
acteristics is response to the unfamiliar, a paradigm in which the child is typically
exposed to an unfamiliar adult, novel surroundings, stimulating objects, or a com-
bination of these. Fifteen percent of Caucasian American children can be assigned
to one of two extreme categories on the basis of behavioral and physiological
response to novelty. When confronted with a wide variety of challenges, such as the
presence of an unfamiliar adult or automated and colorful toys, some children are
shy and restrained, while others are outgoing and spontaneous. Children falling at
these extremes of the spectrum are classified as inhibited vs. uninhibited andlor
reactive vs. nonreactive, respectively, based on composite responsivity measures
obtained in these situations and tendencies to distinctly avoid or approach novel
stimuli [Kagan et al., 1988; Kagan & Snidman, 19911. There also exists an inter-
mediate majority that cannot be classified reliably along these dimensions. In a
longitudinal study of 400 children from age 2-7, the temperaments of the ex-
tremely shy and the extremely outgoing minority remained stable, whereas the
developmental trajectory of the intermediate majority could not be predicted. In
addition, several indices of physiological reactivity were correlated with behav-
ioral temperament. Inhibited, highly reactive children exhibited high and mini-
mally variable heart rates, exacerbated pupillary dilation, and high norepineph-
rine and cortisol concentrations in response to novelty [Kagan et al., 1988, 19901.
POTENTIAL INFLUENCES ON THE EXPRESSION OF
TEMPERAMENTAL TRAITS
Influence of Heredity
It is commonly believed that temperament is constitutional factor that is
present a t birth and has a biological basis [Goldsmith et al., 19871, based on the
ability of researchers to identify temperamental differences among human infants
shortly after birth and the fact that biological correlates of temperamental respon-
sivity have been identified in infants and young children [Fox, 1989; Healy, 1989;
Kagan et al., Snidman, 1987, 1988; Kagan & Snidman, 19911. These findings
suggest that certain temperamental qualities may be heritable. There have thus
 Temperament in Primates / 105
been several attempts t o assess genetic influences on temperamental characteris-
tics in children, and these have varied in both methodology and the characteristics
measured. In spite of problems with twin studies [reviewed in Emde et al., 19921
and the existence of contrasting results between some studies, the evidence overall
suggests that there is at least a moderate genetic influence on some aspects of
temperament in children [Emde et al., 1992; Braungart et al., 1992; Matheny,
1983; Saudino & Eaton, 1991; Wilson & Matheny, 19831.
While there have been few studies attempting to assess heritable influences on
temperament in nonhuman primates, breeding studies with rhesus (Macaca mu-
latta) show that some behavioral and physiological response traits have some de-
gree of genetic component [Suomi, 19811. Rhesus that were identified as either
high reactive or low reactive in psychophysiological and behavioral responsivity to
novelty were more similar in these measures to siblings or half-siblings than to
unrelated monkeys. Individual differences in these temperamental traits can first
be detected in 1-month-old rhesus infants and remain consistent into adulthood
[Higley & Suomi, 1989; Suomi, 19871.
Prenatal Factors
Another source of constitutional variation in temperamental characteristics is
prenatal experience. Evidence from human studies indicates that offspring of
mothers reporting stress during pregnancy show heightened emotionality and re-
activity [Minde et al., 1968; Field et al., 1985; Clements, 19921. However, the
human studies suffer from numerous inherent methodological problems [Istvan,
19861. Enhanced reactivity and emotionality have also been observed in the off-
spring of gestationally stressed rodent mothers [see Joffe, 1978; Weinstock et al.,
19881. Evidence from nonhuman primates indicates that prenatally stressed mon-
keys show enhanced behavioral and physiological reactivity to novelty and stress-
ful stimuli [Clarke & Schneider, 1992,1993; Schneider, 1992a,bl. Further, human
studies have found a consistent association between prenatal maternal anxiety
and a “difficult” (reactive) temperament in the infants of anxious mothers [Led-
erman et al, 1981; Meijer, 19851. This finding has been replicated across several
different designs and maternal samples and has been suggested to be mediated by
elevated levels of stress hormones (ACTH and cortisol) in the stressed mothers
[Vaughn et al., 19871. Thus, there is evidence that prenatal factors can influence
temperamental responsivity. This is an area open to further investigation in more
controlled studies in nonhuman primates.
Environmental Influences
The behavior-genetic studies illustrating some heritable influence on infant
temperamental characteristics in young children have also demonstrated some
environmental influences on temperamental qualities [Braungart et al., 1992;
Thomas & Chess, 1986; Wilson & Metheny, 19831,although specific features of the
nonparental aspects of the environment have generally not been studied. As re-
viewed below, a number of nonhuman primate studies have demonstrated signif-
icant effects of variations in the early rearing environment on reactivity in pri-
mates [Clarke, 1993; Hill et al., 1973; Kraemer, 1992; Kraemer et al., 1989; Novak
& Harlow, 1975; Mason, 1979a,b; Mason et al., 19911. However, there has been
little prospective research on the possible interaction of infant temperament and
features of the early rearing environment in human or nonhuman primate studies.
Exceptions are longitudinal studies of children by Emmy Werner, whose results
indicated the independent effects of temperament, environment, and tempera-
ment-environment interactions on later adolescent behavior [Werner, 1989a,b]. In
106 I Clarke and Boinski
addition, several human studies have examined the role of the interaction of ma-
ternal style and infant temperament in influencing outcomes such as the quality
of mother-infant attachment [Calkins & Fox, 1992; Grossman & Grossman, 1991;
Izard et al., 19911. In this context, it is of considerable interest that a recent study
of vervet monkeys has found evidence of a maternal behavioral influence on the
component of temperament most frequently measured in humans, response to the
unfamiliar [Fairbanks & McGuire, 19931.
In nonhuman primates, cross-fostering of rhesus infants with both exception-
ally nurturant vs. average rhesus mothers demonstrated that maternal style can
significantly affect the behavioral development of infants with predispositions for
high vs. low reactivity. High-reactive infants cross-fostered to nurturant mothers
exhibited more rapid behavioral development, while low-reactive infants were
unaffected by the style of mothering to which they had been exposed (Suomi, 1987).
An earlier study also found a n interaction between maternal and infant temper-
ament in rhesus. Offspring of excitable mothers were rated as less confident than
offspring of less excitable mothers, and this effect was greater for males [Steven-
son-Hinde & Simpson, 19881.
APPLYING THE TEMPERAMENT CONCEPT TO
NONHUMAN PRIMATES
Clearly, many researchers have observed individual differences among their
nonhuman primate study subjects. Field workers have long been cognizant of
individual differences in the personality, behavioral style, or temperaments of
their subjects and that such trait-like characteristics may influence the individu-
als’ social, ecological, andlor reproductive success. Only recently has this become a
topic of interest rather than regarded as “noise” in the data.
While the terms temperament and personality have been used more loosely and
sometimes interchangeably in the nonhuman primate literature, it is in fact clear
from the literature that a distinction between these concepts can be made similarly
to that usually applied in human studies. Temperament may be considered a char-
acteristic response style to novel stimuli or challenging situations that is largely
independent of immediate social or volitional influences and that is observable
primarily in novel situations. As in the human literature, personality refers more
to specific social characteristics of the individual-for example, the degree to which
a n animal is gregarious, aggressive, confident, playful, etc. [Buirski et al., 1978;
Caine et al., 1983; McGuire et al., 1994; Stevenson-Hinde & Simpson, 1981;
Stevenson-Hinde & Zunz, 19781. Thus, personality traits are relatively easy to
identify from repeated observations of group-living animals but more difficult to
ascertain in nonsocial test situations. Conversely, behavioral reactivity is more
readily observed in novel situations in which the single animal subject is exposed
to some sort of novelty challenge [Higley & Suomi, 1989; Suomi, 1985; Vochteloo
et al., 19911 (including social challenges, such a s exposure to a stranger [see An-
zenberger et al., 1986; Mendoza & Mason, 19861).Reactivity is thus generally more
difficult to assess in a group-living situation, except in very delimited and perhaps
infrequent circumstances, such as responses to another’s aggression.
Similarly to the human literature, some proportion of individual primates are
said to be classified as reactive and fearful or as unreactive or unfearful [Suomi,
19851. Like children labeled as reactive or shy, reactive monkeys avoid novel
stimuli and show heightened psychophysiological responsivity to stress. Also in
parallel with the human studies, laboratory studies indicate that, at least in
rhesus monkeys, high or low reactivity can be identified in young animals and that
these profiles are stable across time and situations [Higley & Suomi, 19891.
 Temperament in Primates / 107
While characterizing stable behavioral traits based on human temperament
theory in nonhuman primates might in some sense be considered anthropomor-
phic, at least several temperamental traits assessed subjectively in animals have
been found to correlate with objective measures of behavior [Feaver et al., 1986;
Mondragon-Ceballos et al., 19911. Further, certain temperamental dimensions,
such as the shy-boldlreactive-unreactive continuum, have now been found to be
appropriate for characterizing individual differences in a taxonomically diverse
array of species [e.g., see Feaver et al., 1986; Francis, 1990; Lyons et al., 1988;
Mather & Anderson, 19931. Applying the concept of temperament to nonhuman
primates may inform us about the proximal bases of interspecific and intraspecific
variation in social behavior. At the species level, temperamental differences
among related species may give rise to variations in social structure. For example,
several investigators have suggested that primate interspecific differences in so-
cial tolerance, aggression, and affiliation may be proximally related to group com-
position (male to female ratios) and dispersal patterns [Caldecott, 1986; Moore,
1992; Shiveley et al., 19821.
Ecological specializations have also been associated with temperament differ-
ences. Species that depend on manipulative and explorative foraging techniques
tend to be highly inquisitive and less reactive to novelty than other species [Clarke
& Lindburg, 1993; Vitale et al., 19911. Just as aggression is often deprecated in
human societies but may be extremely adaptive among wild primate populations
[de Waal, 19921, high reactivity profiles for species and individuals may be advan-
tageous in a natural context. A highly reactive, cautious, and vigilant primate
species might, for example, be less susceptible to predation. A timid and diffedent
male might not provoke ejection from a troop as quickly as a more boisterous,
aggressive male. Similarly, Clark and Ehlinger [ 19871 have pointed out that
among humans a shy and timid child could be quite functional in a small, buffered,
and predictable society, whereas the same child would likely have difficulty coping
in a high-paced, confrontational society where outgoing personalities are es-
teemed.
TEMPERAMENT STUDIES IN NONHUMAN PRIMATES
The earliest studies of temperament and personality in a nonhuman primate
species were designed by Stevenson-Hinde and colleagues [Stevenson-Hinde &
Zunz, 1978; Stevenson-Hinde et al., Barnes, 19801. These researchers developed a
rating scale for measuring personality traits and temperamental characteristics of
socially housed rhesus monkeys. Thirty-three traits were identified that could be
reliably scored among multiple observers. The rating scales were loosely based on
the Emotions Profile Index (EPI) of Plutchik [19701 developed for personality stud-
ies in humans. Using principal component analysis, three dimensions of temper-
amental variation were derived from the traits, labeled as confident-fearful,
active-slow, and sociable-solitary [Stevenson-Hinde & Zunz, 19781. These re-
searchers found numeric ratings on these dimensions to be reliable and consistent
among observers and that some social traits were predictive of behavior in nonso-
cial test situations [Stevenson-Hinde et al., 19801.Adaptations of this method have
now been found to be valid for other studies of rhesus and several other nonhuman
primate species [e.g., Bolig et al., 1992; M. nemestrina: Caine et al., 1983; Papio
hamadryas, M . fuscata, Saimiri boliuiensis, S . sciureus: Martau et al., 1985; Cer-
copithecus aethiops: McGuire et al., P. cynocephalus: Sapolsky, 1988; Sapolsky &
Ray, 1989; Ray & Sapolsky, 19921. Further, there has been a recent acute interest
in the personality traits of primates in free-ranging situations and the subsequent
adaptation of temperament scales similar to those used by Stevenson-Hinde et al.
108 I Clarke and Boinski
[1980] for use in more naturalistic settings [Higley et al., 1992; Rasmussen &
Suomi, 1989; Sapolsky & Ray, 19891.
Another method of assessing temperament in infant nonhuman primates uses
a n adaptation of the widely used human neonatal test, Brazelton’s Newborn Be-
havioral Assessment Scale [Schneider & Suomi, 19921. This primate scale uses a
priori cluster scores based on factor analysis that parallel those clusters used with
human neonates (i.e., orientation, motor maturity, state control, and activity)
[Schneider et al., 19911. Longitudinal studies have demonstrated behavioral sta-
bility in these measures from day 12 postpartum in rhesus monkey neonates.
Further, differential postnatal rearing conditions influenced state control, in that
rhesus monkey infants reared with early exposure to peers and toys were rated as
superior in self-quieting and lower in fearfulness compared to infants reared with-
out toys or peers [Schneider & Suomi, 19923. Finally, recent evidence suggests that
even prenatal events can impact the manifestation of state control in rhesus mon-
key neonates. Infants born to females exposed to a 2 week period of adrenocorti-
cotropic hormone treatment during midgestation demonstrated increased irrita-
bility and were strikingly difficult to console during the neonatal period [Schneider
et al., 19921.
In parallel with the human work, recent studies have begun to explore bio-
logical correlates of behavioral characteristics in nonhuman primates. For exam-
ple, Sapolsky and Ray [1989; Ray & Sapolsky, 19921 found that styles of interac-
tion in wild baboons were related to several physiological indicators of stress
(changes in androgens and glucocorticoids). In another recent study, McGuire et al.
[19941 have developed a rating system to assess temperamental traits of socially
housed vervet monkeys and have found some traits to be related to measures of
CNS aminergic activity [HVA and 5-HIAA: Dillon et al., 19921.

Variation Among Individuals

The early studies of Stevenson-Hinde and others sought to establish whether
behavioral traits in socially living monkeys could be reliably identified among
individuals and to what extent they were stable over time. Since these early in-
vestigations, other studies have sought to investigate how temperamental traits
might be related to other variables such as social behavior or dominance ranking.
Caine et al. [19831 found that pigtailed macaques rated highly on the dimensions
of confident-effective and opportunistic were more likely to be high ranking,
whereas those rated as insecure and dependent were likely to be low ranking.
Monkeys that had experienced a brief maternal separation were rated as less
social. An analogous result was reported by Stevenson-Hinde and Zunz [19781, who
found that group-living rhesus monkeys rated as the least fearful were also rated
the most social.
Similar studies were conducted by Buirski and colleagues in wild baboons and
chimpanzees. In a study of free-ranging baboons, troop members were rated by
multiple observers on eight personality dimensions using a version of Plutchik’s
[ 19701EPI adapted for baboons. Animals rated lowest on fearfulness were groomed
the most often, and these were the most dominant animals, who were also rated as
less social and more aggressive relative to low-ranking animals. Low-ranking
animals were rated as both more social and more fearful [Buirski et al., 19731. An
analogous scheme was used in a study of the Gombe chimpanzees. Dominant an-
imals were again rated as more aggressive than subordinates and also a s more
gregarious and controlled, whereas low-ranking animals were characterized as
timid and impulsive. Males were rated as more aggressive and gregarious than
 Temperament in Primates / 109
females, while females were more timid and controlled than males [Buirski et al.,
19781.
A recent large study (n = 97) of personality traits in group-living vervet
monkeys utilized 17 rating items which were factor-analyzed to yield three factors:
socially competent, playful/curious, and opportunistic. Results of three separate
assessments of the animals by multiple observers showed that ratings on these
dimensions were related to sex, age, and dominance status. Dominant animals
were rated as higher on the socially competent and lower on the opportunistic
factor as compared to subordinates. Females were rated as more opportunistic than
males. Ratings on the dimensions changed with age, with juvenile and subadult
animals rated as more opportunistic and playful relative to adults [McGuire et al.,
19941. Interestingly, individual differences in factor ratings were more consis-
tent over time and changing social groupings than a number of measures of overt
behavior (e.g., grooming).
A complex study by Bolig et al. [1992] sought to distinguish temperamental
reactivity from personality characteristics in rhesus monkeys. Individuals were
rated as low, moderate, or high on reactivity based on their tendencies to approach
new stimuli and to attempt challenges and to be anxious and socially inhibited. In
addition, four components of personality similar to those identified by Stevenson-
Hinde and Zunz [1978] were identified. The components were derived from 20
personality descriptors found to be reliable across observers. Relationships were
found between the temperament ratings and personality components, and person-
ality components were differentially related to age, rank, and sex. High reactors
were rated as low on confident-popular and high on tense-insecure, whereas the
opposite result was found for low reactors. High reactors were also rated as less
solitary and more aggressive-irritable than low reactors. High-ranking animals
were rated as more confident-popular and less tense-insecure than low-ranking
animals. Consistent with the findings noted above for vervets, younger animals
were more likely to be rated as playful-active [Bolig et al., 19921.
At the level of individual primates, robust and developmentally stable differ-
ences are also present in the physiological response patterns of the hypothalamic-
pituitary-adrenal axis and the sympathetic nervous system t o environmental
changes and disturbances. About 20% of individual rhesus are easily disrupted and
stressed [Suomi, 19911, a distribution similar to that reported for children [Kagan,
19891. Such individuals are much more likely to have higher baseline levels of
catecholamine turnover, particularly norepinephrine, and higher heart rates than
the other 80%. In contrast, the remaining 80% of individuals exhibit rapid adap-
tation to environmental perturbations like social separation [Suomi, 19911. Juve-
nile rhesus with high reactivity to experimentally induced stressors were less
likely to attain high dominance status as adults than low-reactivejuveniles [Golub
et al., 19791.
Provisioned, free-ranging rhesus also exhibit marked differences in individual
reactivity. In a population of juvenile male rhesus on the island of Cay0 Santiago,
Puerto Rico, heart rate patterns covaried with several endocrine measures subse-
quent to the stress of capture [Rasmussen and Suomi, 19891. Juvenile males with
low cortisol levels had relatively low and variable heart rates and higher prolactin,
testosterone, and growth hormone concentrations than individuals with higher
cortisol levels. The former, low-reactive set of males was suggested to have a
physiological profile that would facilitate success in competitive interactions. An-
other study of juvenile male rhesus on Morgan Island off the coast of South Caro-
lina focused on the interrelationships of stress hormones, serotonin metabolites in
cerebrospinal fluid, and levels of aggressive behavior [Higley et al., 19921. As in
110 / Clarke and Boinski
the Cay0 Santiago study, individual hormone levels varied dramatically. Levels of
aggression, as evaluated by behavioral observations and quantification of wounds
and scars received in fights, were negatively related with titers of the serotonin
metabolite. In other words, the lower the titer of the serotonin metabolite, the more
prone the individual was to engage in aggressive behavior. Higher levels of ag-
gressive behavior were also associated with greater concentrations of cortisol, cor-
ticotrophin, and norepinephrine, hormones indicative of higher levels of stress.
Dominance status, behavioral style, and the turmoil of disruptions in a troop’s
social structure add a n additional level of complexity to any discussion of individ-
ual variation in reactivity to novelty or stress [Sapolsky, 1990; Alberts et al.,
19921. Sapolsky’s long-term field studies of the relationship between dominance
and the physiology of stress in savannah baboons (P. cynocephalus) determined
that the testosterone responses of subordinate and dominant males differed sub-
sequent to encounters with the same psychological stressor, capture stress. Tes-
tosterone titers of dominant males quickly elevated and remained elevated for
about a n hour, whereas testosterone titers of subordinate males dropped precipi-
tously [Sapolsky, 1990; Sapolsky & Ray, 19891. Further, among dominant male
baboons, there were those distinguished by a low-reactive vs. a high-reactive style
[Sapolsky, 1990; Sapolsky & Ray, 19891. Those dominant males who consistently
exhibited a low-key behavioral response to psychological stressors and were also
able to calibrate their response to different intensities of stress (such as distin-
guishing between the mere presence of another adult male vs. being threatened
by that male) also had low basal concentrations of cortisol. In contrast, dominant
males who were highly reactive to identical stressors had basal cortisol levels
comparable to those of subordinate adult males. As Rasmussen and Suomi
[19891 suggested for low-reactive male rhesus, Sapolsky [19901 argued that a non-
reactive style may facilitate attainment and/or maintenance of high rank in
baboons.
Sapolsky’s [19901 observations of different behavioral styles among dominant
male baboons suggest that in some cases particular behavioral characteristics may
be only relative contributors to social success within populations. As pointed out by
Clark in discussing primate individual differences within a social context [ 1991, p.
1041, “Looking for the advantages or disadvantages of particular types of physio-
logical/behavioral responsiveness may be taking the wrong approach. Especially
in a highly social species, where an individual’s relative fitness is a result of both
what i t does and what others are doing, the important factor in success may be the
differences between it and other individuals, rather than its exact physiological
make-up or its absolute level of response to a given amount of change.”
Variation Among Rearing Groups
Since the early work of Harlow and colleagues, a large literature has accumu-
lated documenting the effects of variations in early social experience on a number
of behavioral domains in rhesus monkeys. The largest portion of this literature
concerns comparisons between isolate- or inanimate surrogate-reared animals
and animals reared in various social conditions. These studies have found alter-
ations from the norm in a diverse array of behavioral measures [for reviews see
Capitanio, 1986; Kraemer, 1992; Ruppenthal et al., 1976; Sackett, 1970; Suomi,
19821. Later studies established that variations among different types of social
rearing conditions also produced differential behavioral outcomes in the young
monkeys [Champoux et al., 1991; Chamove et al., 1973; Coehlo & Bramblett, 1981,
1982, 1984; Kraemer et al., 1984; Novak & Harlow, 19751.
 Temperament in Primates / 111
As noted earlier, conspecific primate infants reared in contrasting early
rearing environments also show differential temperamental characteristics. A
number of nonhuman primate studies have demonstrated effects of variations
in the early rearing environment on reactivity in primates [Clarke, 1993; Hill et
al., 1973; Kraemer et al., 1989; Mason et al., 19911. The results of these are
complex. In general, negative behavioral responsivity (fearful and disturbance
behavior) to novelty challenge appears to be enhanced in primates reared in
atypical social environments (isolate-, surrogate-, or peer-reared), while physio-
logical responsivity in the same situations appears to be reduced [see Clarke,
1993; Kraemer, 1992; Novak & Harlow, 1975; Mason, 1979a,b]. Primate infants
reared in artificial environments providing relatively more stimulation or in those
that more closely approximate the species-typical norm appear to have less
inhibited behavioral responses to novelty challenges (e.g., show more exploration
and less inhibition) and appear to approach novel situations in a more bold and
instrumental manner [Mason, 1979a,b; Suomi, 1985; Voctheloo et al., 19911.
Further, one recent study directly addressing the effects of early environmental
stimulation on measures of temperament in nonhuman primate infants found that
infants showing disparate temperamental traits were differentially responsive to
environmental stimulation [Schneider et al., 19911. This interesting finding
suggests the possibility of future studies of the interaction of early environmental
experience with temperamental characteristics in nonhuman primates, such as
rearing infants with contrasting early temperamental traits in different social
environments.
An example of the effects of early social experience on one aspect of sympa-
thetic responsivity known to be highly sensitive to novelty and stress in both
human and nonhuman primates, the hypothalamic-pituitary-adrenal (HPA) axis,
comes from studies of rhesus monkeys. The HPA axis system has been used as an
index of temperamental responsivity in nonhuman primate studies at both the
individual and species levels [Clarke et al., 1988a; Mendoza & Mason, 1986,1989;
Sapolsky, 19901. In a recent study, HPA axis activity was assessed via measure-
ment of ACTH and cortisol values over the first 6 months of life and in response to
two stressful housing transitions in 48 infant rhesus monkeys that were either
mother- or peer-reared. Peer-reared monkeys showed lower levels of ACTH over
the first 6 months of life than mother-reared, but the rearing groups did not differ
in basal cortisol values over this period. Mother-reared animals showed increases
in ACTH and cortisol in response to the mild stress of being moved to a new cage,
whereas the peer-reared group showed virtually no HPA axis response to this
transition. The mother-reared group also showed higher values of ACTH and cor-
tisol in response to the more severe stress of separation from their rearing partners
and housing with unfamiliar age-mates; in fact, ACTH values were unchanged
following this transition in the peer-reared group. Thus, peer-reared infants
showed reduced ACTH and cortisol responses to stressors as compared to mother-
reared infants. This finding was interpreted as reflecting a lack of maternal in-
fluence on the organization of the HPA axis in the peer-reared animals, resulting
in their failure to show an appropriate HPA axis response to stress [Clarke, 19931,
in keeping with the presumed influence of the mother on the organization of
psychobiological systems in the infant [Hofer, 1978, 1987; Kraemer, 19921. These
results add to the growing evidence that early social experience can influence
basal physiological activity and responsivity to stress in primates [see also Cham-
poux et al., 1989; Coe et al., 1989; Higley et al., 1991; Kraemer et al., 1984, 1989,
Mason, 1979a,bl.
112 / Clarke and Boinski
Variation Among Species

Over 50 years ago three ape species were described as differing in personality.
Yerkes and Yerkes (19291 found gorillas (Gorilla gorilla) to be diffident and shy
and chimpanzees (Pan troglodytes) outgoing, expressive, and impulsive, while
orangutans (Pongopygmaeus) were withdrawn and brooding. Since then, the num-
ber of studies addressing the diverse reactivity patterns and personalities of pri-
mates, as well as their physiological concomitants, has increased in number and
sophistication.
Thus, a number of studies have sought to characterize differences among pri-
mates in responsiveness toward novel stimuli. The most common of these have
involved responses to novel inanimate objects. In the largest study, Torigoe [19851
compared responses to novel objects among 74 primate species. He found a large
range of interspecific variation in degree of object responsiveness, with the apes,
Cebus species, and macaques the most actively responsive to the objects. Similarly,
Parker [ 19741 compared ten primate species in degree of object manipulation and
found that great apes showed the most frequent approaches and instrumental
responses to the objects.
In another large study, Glickman and Sroges [19661 examined the reactivity of
several hundred zoo animals, including 46 primate species, to the presence of novel
objects. They were able to rank broad taxonomic groups in regard to reactivity
(reptiles had the lowest rank, while primates and carnivores were most reactive),
and variation was also shown among the primate species tested. The folivorous
langurs (Colobus spp.) were much less reactive than the aggressive and inquisitive
macaques (Macaca spp.) and baboons (Papio spp.). The baboons and macaques were
characterized as highly reactive, aggressive, and vigorous in their approach to-
ward the objects. Other comparative studies during this period addressing reac-
tivity differences in primates employed fewer species but more extensive behav-
ioral tests. Singh and Manocha [19661 found contrasts between langurs (Presbytis
entellus) and rhesus monkeys (M. mulatta) in their responses to a variety of objects.
Langurs were more bold and less fearful than rhesus, approached and contacted
the objects more often, and showed less abnormal behavior. Rhesus were also found
to differ from gibbons (Hylobates lar and H . pileatus) in response to novel stimuli.
Gibbons were more active, manipulative, and bold in their approach toward un-
familiar objects, animals, and environments, while rhesus showed more distur-
bance behavior [Bernstein et al., 19631. Individuals comprising six monkey and
one prosimian species (Cebus apella, S . sciureus, Lemur catta, Lagothrix hum-
boldti, M. mulatta, M. nemestrina, and M. speciosa) exhibited unique profiles with
regard to time allocated to self-directed behaviors, object manipulation, vigilance,
and high energy expenditure locomotion [Davis et al., 19681. The species differ-
ences in reactivity, even among the three closely related macaques, were so
marked and consistent that Davis et al. [1968] suggested that there was a strong
genetic basis to these behavioral differences and th a t selection had occurred to
cause rapid evolutionary divergence in responsivity among these species.
William Mason and his colleagues and students have focused much of their
research on the proximate sources of differences in reactivity across primate spe-
cies [Clarke & Mason, 1988; Clarke et al., 1988a,b, 1994; Mason, 1976, 1978;
Mendoza & Mason, 19891. Underlying differences in physiological responsiveness,
as determined at least in part by hypothalamic-pituitary-adrenal (HPA) and sym-
pathetic-adrenomedullary systems, are explicitly recognized as a major source of
temperamental differences among species. Furthermore, species differences in rep-
resentative or modal social organization have been characterized as emergent
 Temperament in Primates / 113
phenomena resulting from interactions among individuals with disparate reactiv-
ity patterns or stress-response characteristics [Mason, 1976, 19781. Evolution of
the phenotypic expression of social organization thus could result from selection on
the physiological systems underlying behavioral reactivity to stress.
An example comes from Mason and colleagues’ studies of titi monkeys (Cal-
licebus moloch) and squirrel monkeys (Saimiri sciureus), two neotropical primates
of relatively distant phylogenetic affinity. These studies provide the most detailed
example of the association between temperament, physiological characteristics of
the stress response, and social and ecological specializations between species. Titis
form close, monogamous pair bonds, are territorial, and have a significant folivo-
rous component to their diet [Kinzey, 19811. In contrast, squirrel monkeys live in
large, nonterritorial, multimale and multifemale groups, and are largely insectiv-
orous [Janson & Boinski, 19921. In other words, the titis can be regarded as
adapted to a niche less demanding of rapid and sustained vigorous activity than
are squirrel monkeys. Concomitantly, titis have a lower heart rate and plasma
cortisol response to experimentally imposed stressors than do squirrel monkeys.
Even in baseline conditions, squirrel monkeys have a higher heart rate and higher
cortisol levels than titis; stress-inducing situations increase this disparity [Men-
doza & Mason, 1989; Cubicciotti et al., 19861. In comparisons of the two species in
response to various novelty and stress challenges, Saimiri were characterized as
more active, more opportunistic, impulsive, and bolder than Callicebus [Mendoza
& Mason, 1984, 19861.
Another recent report comparing responses of a New and an Old World species
(Cebus apella and M. fascicularis) to a highly provocative artificial stimulus (a
snake model) also illustrates intraspecific temperamental differences. The capu-
chin monkeys engaged in more approaches, exploratory behavior, and contact with
the snake model than the macaques, whose behavior toward the model was de-
scribed as avoidant and fearful [Vitale et al., 19911. The authors suggested that
these differences were based on contrasts in predator defense and foraging strat-
egies in the wild, which were in turn related to the contrasting temperaments of
the two species. The bold and instrumental Cebus have an omnivorous diet and
actively defend against predators, whereas the more frugivorous Cynomolgus
sureptiously avoid predators [Vitale et al., 19911.
In all of the studies described above, comparisons have been made primarily
across genera. A more fine-grained analysis motivated by the lure of possible
phyletic insights into interspecific variations in temperamental responsivity
would logically begin with comparisons of more closely related (i.e., congeneric)
species. The Old World monkey genus Macaca presents a tantalizing but too rarely
realized opportunity for comparative studies, with a t least 12 species distributed
across Asia and having diverse habitat and dietary adaptations [Melnick & Pearl,
19871. Among the genus, only a few species are well studied, and the number of
directly comparative studies is very limited. While superficially similar in social
structure, these congeneric species do exhibit differences in sociodemographicsand
aspects of social and sexual behavior [reviewed in Caldecott, 1986; Lindburg, 1991;
Melnick & Pearl, 1987; Shively et al., 19821. There is also great interspecific
variation in habitat use and foraging and ranging behavior [Melnick & Pearl,
19873. Several workers have commented on the consistent species differences in
temperament and reactivity within this genus and suggested that disparate diet
and habitat specializations might be the ultimate explanation [Caldecott, 1986;
Richard et al., 19891. Macaque species such as the rhesus (M. mulatta),that flour-
ish in commensal relationships with humans, are described by Richard et al. [1989:
5771 as possessing the traits of “curiosity, behavioral adaptability,” and “an ag-
114 I Clarke and Boinski
gressive and gregarious temperament.” In an analogous comparison, de Waal
[19891 contrasts the “hot headed, belligerent” personality of rhesus monkeys with
the intelligent, mild-tempered, exuberant, and complex personality of stumptailed
macaques (M. arctoides). Rhesus were also found to be more exploratory and less
socially passive than pigtail macaques (M.nemestrina) [Sackett et al., 19761. In a
detailed comparison of three species of macaques (rhesus, Tonkean [ M . tonkeana],
and cynomolgus [M. fascicularisl), Thierry [19851 showed that they could be dis-
tinguished by the intensity of aggression and the proclivity to reconcile subsequent
to aggression. Rhesus showed the most aggression and were the least conciliatory,
while Tonkean macaques showed the least aggression and were the most likely to
reconcile, with cynomolgus intermediate in both measures [Thierry, 19851.
A series of experiments involving four macaque species (rhesus, cynomolgus,
bonnet ( M . radiata), and lion-tailed [M. silenusl) quantified species differences in
tendencies to approach and to interact with or to manipulate novel objects and
features of the environment [Clarke & Mason, 1988; Clarke et al., 1988a,b; Clarke
& Lindburg, 19931. Clarke and Lindburg [19931compared responsivity to environ-
mental stimulation and a novel training task in male cynomolgus and lion-tailed
macaques. Compared to the passive and diffident cynomolgus macaques, lion-tails
were characterized as bold, adaptable, vigilant, manipulative, and exploratory. It
was suggested that the greater environmental curiosity of lion-tails is consistent
with their diverse, omnivorous diet relative to the frugivorous cynomolgus and to
the extractive foraging techniques that are more prevalent in the former species.
In laboratory studies, females of three macaque species (rhesus, bonnets, and cy-
nomolgus) were compared in their behavioral and physiological responses to sev-
eral novel situations. The species showed striking contrasts in behavioral and
physiological responses to a novel environment [Clarke et al., 1988al and to a
simple operant training task [Clarke et al., 1988bl. In both situations, rhesus were
characterized as the most active and instrumental in their approach toward the
situations, bonnets as the most passive and least disturbed, and cynomolgus as
most disturbed. Across all test conditions the cynomolgus exhibited the highest
adrenocortical and heart rate response and rhesus the lowest. Rhesus also had the
lowest indices of depression and highest levels of motor activity [Clarke et al.,
1988a,bl. All three species had distinctive and consistent behavioral and physio-
logical responses to environmental stimuli. These differences were interpreted as
based on temperamental factors that contrasted between the species. Cynomolgus
were best described as highly aroused and emotional relative to the other two
species, especially the brazen rhesus [Clarke & Mason, 1988; Clarke et al.,
1988a,b, 19941.
Together these studies clearly demonstrate that primate species may vary
widely in behavioral and physiological response patterns to an extensive array of
stimuli encompassing both social and nonsocial situations, including new social
partners, individuals of other species, and novel or stressful situations. These
species differences have thus been characterized as response dispositions or tem-
peraments by several authors [Higley & Suomi, 1989; Kagan, 1989; Mason et al.,
1993; Mendoza & Mason, 19891 that may be described in relation to stimuli as
attributes such as “habituation, persistence, boldness and distractibility” [Cubic-
ciotti et al., 19861. In particular, the shy-boldkeactive-unreactive dimension is
apparently the dimension that is most applicable to cross-species comparisons, in
parallel with findings for contrasting individual differences. While data on more
species are needed to draw broad generalizations, comparisons thus far suggest
that species that are relatively bold and unreactive in their approach to novel
situations tend to have an omnivorous diet andfor utilize instrumental foraging
 Temperament in Primates / 115
techniques. These findings support the hypothesis that species-typical interrela-
tionships exist between temperament, the physiological systems affecting the ex-
pression of temperament, and ecological and social adaptations.
Variation Among Populations
In contrast to comparisons among species, there are very few data clearly
demonstrating within-species population variations in temperament. This, in part,
follows from the fact that a great deal of within-species variation in behavior has
usually been explained as nongenetic responses to local conditions. Behavioral
variation among conspecific populations has been attributed to habitat and tem-
poral differences in food distribution and availability [Whitten, 1983; Barrett et
al., 19921, population density [Chivers, 19691, sex ratio and group composition
[Datta 1989; van Schaik & van Noordwijk, 19851, susceptibility to predation [Boin-
ski, 19871, and the formation of mixed-species groups [Gautier-Hion et al., 19831.
A species for which there are relatively good data for geographic differences in
behavioral traits is the squirrel monkey (Sairniri sciureus) [for recent taxonomic
revisions see Costello et al., 1993; and Silva et al., 19931. There has been a series
of studies on social behavior and physiological reactivity in captive Gothic (North-
ern South America and Central America) vs. Roman (Peruvian and Bolivian)
morphotypes. Roman squirrel monkeys have a sexually segregated social organi-
zation in which males and females remain spatially separated outside of the breed-
ing season [Mendoza et al., 1978; Gonzalez et al., 19811. Male and female domi-
nance hierarchies are also segregated; all females are dominant to all males.
Aggression by females toward males underlies the spatial segregation. Among
Gothic squirrel monkeys, in contrast, social groups are integrated throughout the
year, and a single linear dominance hierarchy includes both males and females.
Overall, Roman females are much more frequently aggressive than Gothic fe-
males. In both populations individual differences in temperament are documented
for both males and females, but population differences exceed individual differ-
ences [Martau et al., 19851.
These behavioral patterns are concordant with population-level data on phys-
iological reactivity. The more aggressive Roman squirrel monkeys have higher
baseline cortisol levels and a more pronounced cortisol response to stress-inducing
situations. Although they are larger than Gothic squirrel monkeys, and lower
cortisol levels might therefore be expected [Coe et al., 19921, Roman squirrel mon-
keys have higher basal cortisol levels than Gothic squirrel monkeys [Coe et al.,
19851. Further, following formation of new social groups in captivity, plasma cor-
tisol levels of females in Gothic groups were unchanged from baseline levels, but
those of Roman females were elevated for up to 9 weeks, only gradually decreasing
over that period [Gonzalez et al., 19811. Males also exhibit a notable geographic
variation in the interaction between dominance and stress response. Among
Gothic males, cortisol levels following group formation were greater in subordinate
than in dominant males, but in Roman groups the relationship was reversed:
dominant males had higher cortisol levels than subordinates [Coe et al., 19831.
Further evidence of intraspecific population differences in temperamental
characteristics comes from a study of captive animals. Rhesus infants of parents
derived from Indian vs. Chinese populations were compared on temperamental
measures using the Brazelton assessment scale adapted for nonhuman primates
[Schneider & Suomi, 19921. The investigators found dramatic differences between
infants derived from the two populations, with Chinese-derived infants rated as far
more irritable, reactive, and aggressive than their Indian-derived counterparts
[Champoux et al., 19941.
116 I Clarke and Boinski
Thus, the available information suggests that population variation in temper-
ament may represent a significant contribution to observed variability along with
species and individual differences.

EVOLUTION AND TEMPERAMENT IN NONHUMAN PRIMATES

Social systems of animals are perceived as emerging as a result of relation-
ships between individuals [Hinde, 19831. Individual interactions, in turn, are hy-
pothesized to reflect individual behavioral strategies which have been selected
because they maximize inclusive fitness [Silk, 19871. Selection on a physiological
system, which can dramatically affect patterns of individual interactions, is thus
an obvious candidate as a proximate mechanism in the evolution of social organi-
zation and behavior. Several workers have explicitly suggested that temperamen-
tal differences among primate species represent, in many instances, evolved func-
tional adaptations yet admit that it is unclear to which specific ecological and
social selection pressures the physiological systems are responding [Clarke et aI.,
1988a; Richard et al., 1989; Thierry, 19851.
Individual variation within species and populations provides the opportunity
for selection, and thus for behavioral differentiation, to occur. Evolution of pheno-
typic traits, such as physiological and behavioral reactivity, has three require-
ments [Endler, 1986; Stamps, 19911: 1)within-population variation in the individ-
ual expression of the trait, 2) a genetic component affecting the expression of the
trait, and 3) a consistent effect of trait expression on overall fitness. Aside from
lethal genes, the logistical difficulties of documenting the final requirement are
challenging in primates, although individual variation and a genetic basis for the
expression of physiological and behavioral traits are well established [e.g., Suomi,
1991; Plomin, 19901.
Several other factors possibly contribute to individual variation. Broad within-
species differences in reactivity may be maintained due to age and sex differences
in selective regimes [Mendoza et al., 19911. Behavioral polymorphism in offspring
could be an evolutionary strategy of parents to maximize survival during fluctu-
ations in social and ecological conditions [Bekoff, 19771. Frequency-dependent se-
lection also could potentially make mere phenotypic deviation from the norm ad-
vantageous [Clark & Ehlinger, 19871. Selection on any one phenotypic trait may
result in a net positive or negative expression of an array of behavioral andlor
nonbehavioral traits. Given the potential complexity of selective regimes and the
pervasive effects of environmental influences on the development and expression
of these traits [Gottlieb, 19921, it is not surprising that genetic covariance seldom
explains more than half of the observed behavioral variance and that many genes,
each accounting for a very small amount of genetic variance, are probably involved
[Plomin, 19901.
To date, species-level comparisons have not offered many testable comparative
models. This is probably due to the confounding effects of large phylogenetic dis-
tances of uncertain origin, inadequate knowledge of ecological and social condi-
tions in the wild, and/or drift and convergent evolution [Boinski, in press]. Little
progress has yet been made in understanding the evolution of stress response
patterns in primates because suitable species-level comparative systems are rare
or underexploited. Research might be particularly profitable with several rela-
tively recent and speciose primate radiations: 1) the understudied species of
Macaca, especially the Sulawesi macaques, 2) Cercopithecus species, and 3 ) Sagu-
inus spp. Within these genera, a number of species and subspecies show contrast-
ing dietary and habitat regimes and adaptations. Controlled studies (including
 Temperament in Primates / 117
field studies) of these genera would thus contribute substantially to understanding
the basis for contrasting life history regimes among closely related taxa.
The marked contrasts in behavioral and physiological reactivity among cap-
tive Roman and Gothic squirrel monkey populations observed by Gonzalez et al.
[1981] led them to speculate that these differences reflected adaptations to “vary-
ing ecological demands” in the wild. Boinski [in pressl presented a population-level
comparative mode! to explain the evolution of these observed differences based on
a synthesis of data from captive populations (see above) and recently available
field data. In wild squirrel monkeys, geographic variation in the distribution of
desirable food patches (and the pattern of food competition it engenders) appears to
be a powerful variable in explaining geographic differences in social behavior
[Mitchell et al., 1991; Boinski & Mitchell, 19941. Together the physiological, be-
havioral, and ecological data suggest that a large component of geographic varia-
tion in the social behavior of adult Roman and Gothic squirrel monkeys can be
explained by different “settings” of the stress response system [sensu Mendoza &
Mason, 19891. Roman squirrel monkeys in captivity have a much greater stress
response than do Gothic squirrel monkeys. This is consistent with the much higher
levels of food competition and need for social vigilance against aggression among
Roman squirrel monkeys in Peru as compared to Gothic squirrel monkeys in Costa
Rica [Boinski, in press; Boinski & Mitchell, 19941.
Comparisons of geographically and genetically partitioned primate popula-
tions or subspecies may thus be an alternative and more successful strategy to
address the possible evolutionary basis for variation in primate temperament
[Boinski, in press]. Within-species comparisons are less likely to be confounded by
large phylogenetic distances. Specific ecological factors that might underlie differ-
ences in the selective regimes acting on stress responses are also more likely to be
identified in a fine-grained, within-species comparison.
SUMMARY
The study of temperament in nonhuman primates has thus far provided a
useful framework for describing both individual and species-typical variations in
behavioral and physiological responsivity. While individuals have been found to
vary primarily along a dimension of high vs. low reactivity, taxonomic compari-
sons suggest that species-typical temperamental styles may be better regarded as
profiles or clusters of traits and that species may vary in contrasting directions
along related behavioral dimensions such as fearfulness and reactivity. Physiolog-
ical indices of reactivity generally seem to present a somewhat more coherent
profile than behavioral dimensions among both individuals and species; individu-
als and species characterized as reactive tend to be highly responsive to stimuli
across psychophysiological domains (i.e., multiple measures of sympathetic system
activity). However, this is not to suggest that generalities do not occur across
species. While conclusions must be tentative at present due to the relatively few
species studied, primate species characterized as bold, curious, unfearful, and in-
strumental in their approach to novel situations tend to have an omnivorous diet
and to utilize foraging strategies that require relatively high energy expenditure.
This suggestion is also supported by the squirrel monkey data on population dif-
ferences. Thus, commonalities in characteristic behavioral traits observed across
species so far suggest that temperamental attributes may be more related to life
history variables than to taxonomic affinity.
In parallel with studies of humans, the nonhuman primate research provides
evidence of both genetic and early experiential influences on temperamental re-
activity, including both prenatal and postnatal experience. Previous studies sug-
118 I Clarke and Boinski
gest that early social experience may have distinct and apparently long-lasting
effects on behavioral and physiological aspects of temperamental responsivity,
although thus far this has only been studied in rhesus monkeys. Individual dif-
ferences in temperamental or personality characteristics have been studied in a
number of nonhuman primate species. Individual differences in certain tempera-
mental characteristics have been associated with differences in social rank, al-
though there is some evidence to suggest that traits conducive to high rank may
vary among species [Rasmussen & Suomi, 1989; Sapolsky, 19901. Clark 11991, p.
1091has suggested that the source and degree of variation among individuals may
in t ur n vary among species and that “variation in underlying physiological char-
acteristics might allow social animals to develop behavioral characteristics which
differ from those of conspecifics. . . . [Tlhe adaptive significance of this differenti-
ation is that direct competition is reduced and a wider range of routes to social
success is open to exploitation.”
Finally, we argue here that closely related congeners, populations, and sub-
species offer particularly promising opportunities for comparative studies designed
to examine the possible ultimate basis for variation in temperament and reactivity
patterns among primates. Obviously, comparisons between closely related taxa are
less likely to be confounded by great phylogenetic distances. Specific ecological,
demographic, or other factors differing between localities that might cause differ-
ences in the selective regimes acting on temperamental reactivity are more likely
to be identified in closely related populations. Testing evolutionary models will
also be facilitated when lower-level taxonomic groups are being compared. Future
studies utilizing such comparisons are encouraged.
CONCLUSIONS
1. Studies of temperament in nonhuman primates have provided a useful
framework for characterizing consistent variations among primates in behavioral
and physiological responsivity at both the individual and species levels.
2. In parallel with studies of children, the temperamental dimension that has
been most useful for characterizing nonhuman primates is that of boldhhy or
fearfulhnfearful in response to novelty.
3. As is also the case in children, temperamental characteristics displayed by
individual nonhuman primates appear to have a constitutional basis yet are to
some extent modifiable by experience. Primate infants reared in abnormal envi-
ronments tend to show temperamental qualities of greater fearfulness and reac-
tivity to novelty than more normally reared infants.
3. At the species level, some temperamental qualities may be related to life
history variables. Tentative evidence suggests that bold primate species may uti-
lize more active and instrumental foraging strategies than less bold species. More
data on more species are needed to test this hypothesis.
4.Further studies are needed to explore the possible ultimate basis of varia-
tion in temperamental traits and reactivity patterns across species and popula-
tions.
ACKNOWLEDGMENTS
Support for manuscript preparation was provided by awards from the John D.
and Catherine T. MacArthur Foundation Mental Health Research Network on
Depression to A.S.C. A.S.C. thanks T. Bergholz, S. Mitchell, and A. Soto for manu-
script preparation, and Hermi Rojahn, and Michael Raleigh for valuable discus-
sion. S.B. thanks Dee Higley, Kathy Rasmussen, Steve Suomi, and other col-
leagues at the Laboratory of Comparative Ethology for stimulating her interest in

the evolutionary components of variation in temperament among primates. Manu-
script preparation was facilitated by the staff and resources of the Wisconsin Pri-
mate Research Center library, which is supported by PHS RR0169.
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