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Adolescent impulsivity predicts adult

dominance attainment in male
vervet monkeys

ARTICLE in AMERICAN JOURNAL OF PRIMATOLOGY · SEPTEMBER 2004

Impact Factor: 2.14 · DOI: 10.1002/ajp.20057 · Source: PubMed

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 American Journal of Primatology 64:1–17 (2004)

Adolescent Impulsivity Predicts Adult Dominance

Attainment in Male Vervet Monkeys
LYNN A. FAIRBANKS1,2n, MATTHEW J. JORGENSEN1, ADRIANA HUFF1,
KARIN BLAU1, YUNG-YU HUNG3, and J. JOHN MANN3
1
Neuropsychiatric Institute, University of California–Los Angeles, Los Angeles, California
2
Department of Veterans Affairs Greater Los Angeles Healthcare System, Los Angeles,
California
3
Department of Neuroscience, New York State Psychiatric Center, New York, New York

Adolescence is characterized by behavioral and physiological changes

that prepare individuals for the transition to adulthood. The purpose
of this study was to evaluate the effects of behavioral, morphological,
neurobiological, and developmental characteristics of adolescent
male vervets in predicting later dominance attainment. Thirty-six
adolescent male vervets were tested for social impulsivity by means of
the Intruder Challenge test while they were still living in their natal
groups. Body weight and cerebrospinal fluid (CSF) metabolites of
serotonin, dopamine, and norepinephrine were measured before they
were introduced into new matrilineal breeding groups at age 5. Stable
adult dominance rank was determined at age 6, 1 year following
introduction. The results indicated that body weight, adolescent
impulsivity, and levels of 5-hydroxyindoleacetic acid (5-HIAA) and
homovanillic acid (HVA) in CSF predicted adult dominance attain-
ment. As expected, males that were above average in body weight
prior to introduction were significantly more likely to become dominant.
Males that were high in impulsivity as adolescents, and low in 5-HIAA
prior to introduction were more likely to achieve stable alpha male
status 1 year following introduction. The combination of these three
factors resulted in correct prediction of rank attainment for 92%
(33/36) of the males. Two other factors–maternal dominance rank
and a measure of social anxiety from the Intruder Challenge test–were
not related to adult dominance attainment in this sample. These
results support the idea that there are benefits of a high-risk, high-gain
strategy is beneficial for adolescent and young adult male vervets.
They also demonstrate that adolescent impulsivity is age-limited.
Males that achieved high rank moderated their behavior as adults,

Contract grant sponsor: Department of Veterans Affairs; Contract grant sponsor: NIMH; Contract
grant number: R01-MH61852-02; Contract grant sponsor: Conte Neuroscience Center; Contract
grant number: 5P50 MH62185; Contract grant sponsor: Center for Primate Neuroethology,
Neuropsychiatric Institute, UCLA.
n
Correspondence to: Lynn A. Fairbanks, Ph.D., Neuropsychiatric Institute, UCLA, 760 Westwood
Plaza, Los Angeles, CA 90024. E-mail: Lfairbanks@mednet.ucla.edu
Received 26 March 2004; revised 4 July 2004; revision accepted 6 July 2004
DOI 10.1002/ajp.20057
Published online in Wiley InterScience (www.interscience.wiley.com).

r 2004 Wiley-Liss, Inc.

2 / Fairbanks et al.

and no longer scored high in impulsivity relative to their age peers.

Am. J. Primatol. 64:1–17, 2004. r 2004 Wiley-Liss, Inc.

Key words: adolescence; impulsivity; dominance; dopamine; serotonin;

body weight

INTRODUCTION
Female vervets, like macaques and baboons, remain in their natal group for
life and share the dominance rank of their female kin [Chapais & Schulman,
1980; Horrocks & Hunte, 1982; Pereira, 1995]. Males, in contrast, must leave the
natal group and compete for status without support from matrilineal kin [Pusey
& Packer, 1987]. When a vervet male enters a new group, he is threatened and
chased by the resident males and coalitions of females and juveniles [Cheney,
1983; Henzi & Lucas, 1980; Horrocks & Hunte, 1993]. He must not only compete
with other males for dominance, but he must also win the tolerance and
acceptance of the resident females [Raleigh & McGuire, 1989].
The time a male first goes through this process is when he is an adolescent or
young adult [Pusey & Packer, 1987]. This is a time of life when behavioral and
physiological changes prepare males to leave the natal group and meet the
challenges of emigration [Dixson & Nevison, 1997]. The rise in testosterone and
the development of adult secondary sexual characteristics are typically accom-
panied by increases in impulsivity and aggressiveness.
While all males go through the process of emigration and immigration, some
do better than others. Male mortality increases at adolescence, and some males do
not survive the transition to a new group [Fedigan & Zohar, 1997]. Of those that
do, a few rise rapidly in rank, while others remain low-ranking for the duration of
their tenure in the group [Henzi & Lucas, 1980; van Noordwijk & van Schaik,
1985]. Several studies have looked at factors that influence male dominance
attainment following immigration or introduction into new groups. Male
competitive ability is related to age and body weight, and both have been found
to be important in dominance acquisition. Males rise in rank as they achieve full
size and sexual maturity [Bercovitch, 2000; Packer, 1979]. When age is held
constant, larger males have an advantage over smaller males in rank acquisition
in newly formed groups [Morgan et al., 2000].
Behavioral characteristics also play a part in determining the outcome of
initial encounters. In a previous study, van Noordwijk and van Schaik [1985]
observed two different strategies used by immigrating male long-tailed macaques
in Sumatra. The majority of males attempted to be unobtrusive when they
entered a new group. The unobtrusive males did not initiate aggression to the
resident males, and they submitted when challenged. In contrast, the young adult
male immigrants were more likely to use a bluff strategy. Bluff males were bold
and confrontational; they initiated aggression against resident males, counter-
attacked when threatened, and used branch-shaking displays for attention and
intimidation. All of the successful takeovers were accomplished by bluff
immigrants, and none of the males that used the unobtrusive strategy became
high ranking [van Noordwijk & van Schaik, 1985]. A similar pattern was observed
in a captive study of rhesus monkey first encounters [Mendoza, 1993]. Males that
were predicted by caretakers to be dominant initiated more aggression, rarely
showed submission, and never gave fear responses during dyadic encounters with
unfamiliar males. In contrast, males that were predicted to be submissive
 Adolescent Impulsivity in Vervets / 3

initiated few aggressive interactions, and showed frequent submissive and fear
responses. The initial response was rarely reversed for the remainder of the
observation period [Mendoza, 1993].
Matrilineal rank has been proposed as a factor that is likely to influence a
male’s response to the challenges of immigration. Males from high-ranking
matrilines have grown up in a relatively protected social environment, with
experiences of success in competitive encounters with other group members
[Chapais & Gautier, 1993], and there is evidence that sons of high-ranking
females mature and develop adult sexual characteristics at a younger age than
sons of low-ranking mothers [Alberts & Altmann, 1995; Bercovitch, 2000; Dixson
& Nevison, 1997; Setchell & Dixson, 2002]. These characteristics may provide a
physical and psychological advantage for sons of high-ranking mothers when they
leave the natal group.
Measures of monoamine neurotransmitter activity related to impulsivity,
aggressiveness, and novelty seeking have also been proposed as predictors of
dominance for male nonhuman primates [Higley & Linnoila, 1997]. Low levels of
5-hydroxyindoleacetic acid (5-HIAA), the metabolite of serotonin in cerebrospinal
fluid (CSF), are related to earlier age at emigration, higher rates of escalated
aggression, higher levels of adolescent mortality, and higher levels of impulsive
approach and aggression to an unfamiliar male in free-ranging rhesus and captive
vervet monkeys [Higley et al., 1996a; Kaplan et al., 1995; Fairbanks et al., 2001;
Mehlman et al., 1994, 1995]. Levels of homovanilic acid (HVA), a metabolite of
dopamine, have also been linked to aggression, wounding, and dominance in
rhesus and fascicularis macaques [Mehlman et al., 1994; Kaplan et al., 2002], and
3-methoxy, 4-hdroxy-phenylglycol (MHPG), a metabolite of norepinephrine, has
been associated with impulsive novelty-seeking in vervets in Ethiopia [Fairbanks
et al., 1999]. Individual differences in activity in these neurotransmitter systems
may predispose males to respond differently to the challenges of emigration and
immigration.
In the present study we sought to determine whether individual differences
in adolescent behavior, morphology, and neurochemistry in captive vervet
monkeys predict eventual dominance attainment following introduction into
adult breeding groups. Adolescent behavior in the natal group was measured by
means of the Intruder Challenge Test, a standardized resident/intruder test that
measures an individual’s readiness to approach and challenge a social stranger
[Fairbanks, 2001]. Animals that score high on social impulsivity immediately
approach the intruder, and engage in frequent risky, challenging, and aggressive
behaviors. Those that score in the moderate range are more cautious and
tempered in their responses. Animals with the lowest social impulsivity scores
avoid the intruder, and if they interact at all, do so from a safe distance. A second
index, which is independent of approach to a stranger, measures behaviors
related to generalized tension and anxiety during the test.
The present study was designed to test the hypothesis that the responses of
adolescent males on the Intruder Challenge Test, while they were still living in
the natal group, could be used to predict adult male dominance attainment
following emigration and integration into new groups. Based on our prior results
that alpha male vervets are more likely to score in the moderate range on the
social impulsivity index derived from this test, we predicted that adolescent
males that scored in the moderate range would be more likely to achieve a stable
high-ranking position in their new groups [Fairbanks, 2001]. We also predicted
that males that scored high in anxiety would be less likely to achieve high rank
[Huff, 2002].
4 / Fairbanks et al.

Factors that have been related to rank attainment and reproductive

maturation in prior studies of captive and free-ranging monkeys were also
included for analysis in this study. These include age, body weight, matrilineal
rank, and CSF concentrations of 5-HIAA, HVA, and MHPG (the metabolites of
serotonin, dopamine, and norepinephrine, respectively) measured prior to
introduction.

MATERIALS AND METHODS

Subjects
The subjects of this study were 36 male vervets (Chlorocebus aethiops, also
known as Cercopithecus aethiops), living in captive social groups at the UCLA/VA
Vervet Research Colony (VRC). All of the subjects were born at the VRC and
raised by their mothers in relatively stable, matrilineally-organized groups. Social
groups at the VRC are managed to simulate the natural processes of female
philopatry and male emigration. Females remain in the natal group as adults, and
males are removed at adolescence and transferred into other groups. The study
subjects included 16 males from the 1995 birth cohort, and 20 from the 1996
cohort.

Design
This was a longitudinal study that measured attributes of males as
adolescents in the natal group, and as adults before and 1 year after immigration
into adult breeding groups. The males were first tested on the Intruder Challenge
Test as adolescents (3.6–4.8 years old) while they were still living in the natal
group.
Males from the same birth cohort were removed from their natal groups and
placed together in an all-male group. Males from the 1995 birth cohort were
removed at 3.7–4.0 years of age. Those from the 1996 cohort were 4.4–4.9 years
old. Body weight was measured and CSF was collected while the males were living
in the all-male groups.
Sixteen males from the 1995 birth cohort were introduced into four
matrilineal breeding groups in February 2001. Twenty males from the 1996
birth cohort were introduced into five matrilineal breeding groups in February
2002. The nine groups each received four males from the same birth cohort,
stratified according to their natal group Social Impulsivity scores. The four males
included individuals in the upper, middle, and lower ranges, and no two males
were from the same natal group. All resident adult and adolescent males (44.5
years old) were removed prior to introduction of the new males. The subject males
were 5.3–5.8 years of age at the time of introduction.
Male dominance rank was determined 1 year following introduction to the
breeding groups. Seven of the original 36 males were removed during the first
year for treatment of wounds (n = 6) or illness (n = 1), and were not returned.
The remaining 29 males were tested again in the Intruder Challenge test in their
adult breeding groups 1 year following introduction.

Intruder Challenge Test

The Intruder Challenge test was conducted in the home group, in subgroups
of three to four animals tested at the same time. Prior to the initiation of the test,
all group members were confined in the indoor night room, with the exception of
 Adolescent Impulsivity in Vervets / 5

the test animals that remained in the outdoor portion of the home cage. After 20
min, an unfamiliar adult male (the ‘‘intruder’’) in a covered individual cage was
placed at the periphery of the enclosure in contact with and facing the chain-link
fence. The cover of the intruder’s cage was removed, and the responses of each of
the test animals were observed continuously for 30 min. The occurrence of the
following behaviors directed toward the intruder was recorded during each of 30
1-min intervals: approaching within 1 m of intruder, sitting within 1 m of the
intruder, touching the intruder or the intruder’s cage, pressing the face against
the fence to sniff or muzzle the intruder, threatening the intruder, and
presenting an agonistic display to the intruder. Scratching, pacing, and yawning
were also coded as indicators of generalized anxiety. Interrater reliability on
individual items on the Intruder Challenge Test score sheet ranged from .90 to
1.00 [Fairbanks, 2001].

Dominance Rank
Adult male dominance rank was determined from all occurrences of
aggressive behavior observed during behavioral observations in the home group.
The direction of aggression was recorded and summarized quarterly. Following
introduction, adult male rank is often unstable for up to 9 months, with shifts
likely to occur at the beginning of the mating season in November–December. The
male with the highest rank in December typically retains the alpha position
throughout the remainder of his tenure in the group. The outcome variable for
this study was adult male rank determined 1 year following introduction. Rank
determination was made by behavioral observers without knowledge of the males’
prior Impulsivity Index scores on the Intruder Challenge Test.
Rank for males was recorded as alpha vs. other. In vervets, the alpha male
position is clearly differentiated, while linear relationships among lower-ranking
males are difficult to determine. Paternity determinations for animals at the VRC
have shown that in multimale groups, the alpha male fathers most of the infants
born in the group (Vervet Research Colony, unpublished results).
Matrilineal rank during development was determined by the rank of the
subjects’ mothers (recorded as high, middle, or low) as assessed qualitatively in
1998, and quantitatively in 2001. Female ranks are relatively stable in vervet
groups, and all mothers that were classified as high-ranking in 1998 were also
scored as high-ranking in 2001.

Age and Weight

The exact age of each subject was known from colony birth records. Body
weight was measured 1–2 months prior to introduction into the matrilineal
breeding groups. Weight was recorded to the nearest .01 kg with a digital platform
scale (Detecto 758C; Cardinal Scale Manufacturing Company, Webb City, MO).

CSF Metabolites of Dopamine, Serotonin, and Norepinephrine

CSF was sampled for each male 1–2 months prior to introduction. The males
were anesthetized with 10 mg/kg ketamine, and approximately 1 cc of
cerebrospinal fluid was collected from the cisterna magna within 15 min of
anesthesia. CSF was successfully obtained from 33 of the 36 subjects. The samples
were centrifuged and frozen at –801C until they were analyzed. The samples were
assayed for 5-HIAA, HVA, and MHPG by high-performance liquid chromato-
graphy (HPLC) with an electrochemical detector [Placidi et al., 2001].
6 / Fairbanks et al.

Social Impulsivity and Anxiety Scores

We computed Social Impulsivity scores by combining the latency to approach
the intruder with the number of intervals that males were engaged in risky,
assertive, and aggressive behaviors directed toward the intruder (Social
Impulsivity = (30 – latency) + intervals within 1 m + sit within 1 m + touch
intruder’s cage + press muzzle to intruder’s cage + agonistic display to intruder
+ threaten intruder). This index was originally derived from factor analysis of
behavioral responses toward the stranger in a large sample of adolescent and
adult males [Fairbanks, 2001]. In the initial sample, Cronbach’s alpha for the
seven-item scale was 0.84. Two subscales of the Impulsivity Index are also
considered here: 1) the Approach Subscale includes the number of intervals
within 1 m, sitting within 1 m, and touching and sniffing the intruder; and 2) the
Aggression Subscale includes threats and agonistic displays directed toward the
intruder. These two subscales represent different aspects of impulsivity. They
each have high internal reliability (Approach Subscale, alpha = 0.88; Aggression
Subscale, alpha = 0.83), while the correlation between the two subscales is more
modest (alpha = 0.47) [Fairbanks et al., 2004].
We also derived a Social Anxiety score from the Intruder Challenge test by
summing the number of intervals that the subject engaged in scratching, pacing,
and yawning. Social Anxiety scores were negatively correlated with the Social
Impulsivity scores in this sample (r = –0.48).

Statistical Analysis
The unit of analysis was the group, and males were rank-ordered within each
of the nine groups on the variables of interest. For the adolescent Social
Impulsivity and Social Anxiety scores, and maternal rank, weight, and age prior
to introduction, males were rank-ordered into lowest, second, third, and highest
ranks. Since monoamine data were missing for three of the 36 males, we rank-
classified 5-HIAA, HVA, and MHPG into lowest, middle, and highest ranks for
each group. We tested the relationships of each of these measures with eventual
rank attainment using Kendall’s tau for ordinal predictions, and the Chi-square
test of independence for nonlinear associations. There were no significant
differences between the seven males that were removed before the year was over
and the remaining 20 lower-ranking males in any of the measures under
consideration here, so all 27 were classified as lower-ranking for these analyses.
We also ran comparisons between the alpha (n = 9) and other (n = 27) males
on the total and the subscales of the Social Impulsivity Index using t-tests for
independent groups, with separate estimates of the variance where appropriate.
A stepwise logistic regression was used to determine whether the variables
found to predict adult rank were independent and additive. For the multivariate
analysis, the three subjects with missing data for monoamine levels were replaced
with the mean for the missing variables.
A repeated-measures analysis of variance (ANOVA) was used to compare the
Social Impulsivity scores over time for the nine males that achieved alpha male
status with those for the 20 lower-ranking males that remained at the end of the
first year following introduction.
There were no significant differences between the two birth cohorts in
adolescent impulsivity scores, matrilineal rank, age, or weight at the time of
introduction. We controlled for cohort differences in mean values of HVA, 5-
HIAA, and MHPG by rank-ordering the monoamine values within groups, as
described above.
 Adolescent Impulsivity in Vervets / 7

RESULTS
Adolescent Impulsivity by Adult Rank
Figure 1 shows the percentage of males that achieved alpha male status by
rank order of Social Impulsivity scores 2 years before as adolescents in the natal
group. The results indicate that males that show greater impulsivity as
adolescents are more likely to achieve high rank as adults. When considered on
a group by group basis, the individual male with the highest adolescent
impulsivity index score became the alpha male in six of the nine groups (67%).
None of the nine males in the lowest impulsivity group became high ranking.
Males in the moderate range for impulsivity group achieved alpha status at less
than a chance level (3 of 18 (17%)). The X2 test showed a significant association of
adolescent impulsivity scores and eventual male status (X2 = 12.30, df = 3, P =
0.006). The significant Kendall’s t-b indicated that the relationship was linear
(t = –0.45, n = 36, P = 0.001).
Males that achieved alpha status were higher in all three components of the
adolescent Social Impulsivity Index. The means for the total score, latency, and
Approach and Aggression subscale scores are shown in Fig. 2. All of the males that
later attained alpha status rushed over to the intruder’s cage immediately. They
spent almost twice as many intervals in close proximity to the intruder (sitting
near, muzzling, and reaching into the intruder’s cage), and more than four times
as many intervals threatening and displaying to the stranger compared to
adolescent males that did not achieve high rank. The mean differences between
the two groups were statistically significant for the total index and for all three

80

6/9

60
% Alpha

40

2/9

20
1/9

0/9
0
Lowest Low-Mid High-Mid Highest
Adolescent Impulsivity
Fig. 1. Percentage of males that achieved alpha status as adults, by adolescent Social Impulsivity
scores, rank-ordered within groups.
8 / Fairbanks et al.

100

Alpha
80
Lower

60
Score

40

20

0
Total Approach Aggression Latency
Social Impulsivity Index and Subscales
Fig. 2. Mean (+SE) Social Impulsivity scores and subscores for adolescent males tested in the natal
group, by eventual dominance status in adult breeding groups.

components (t-test for unequal variances: total index: t = 3.35, P = 0.004;

Approach subscale: t = 2.75, P = 0.014; Aggression subscale: t = 3.20, P = 0.010;
Latency: t = 2.73, P = 0.011).
The adolescent Social Anxiety Index from the Intruder Challenge test was
not significantly associated with later adult rank in this study (Kendall’s t-b =
0.13, n = 36, P = 0.40).

Matrilineal Rank
Of the 36 males, 13 had been raised by high-ranking mothers, 10 by middle-
ranking mothers, nine by low-ranking mothers, and four had lost their mothers
before they left the natal group. Matrilineal rank in the natal group did not
predict adult male rank attainment (X2 = 2.03, df = 3, P = 0.57). Four of the
males that achieved alpha status came from high-ranking matrilines, two came
from middle-ranking matrilines, and three came from low-ranking matrilines.
None of the four males that had lost their mothers as juveniles became high-
ranking.
 Adolescent Impulsivity in Vervets / 9

Age and Body Weight

The mean age and body weight prior to introduction for males achieving
alpha vs. lower-ranking status are shown in Table I. Male age at the time of
introduction was relatively uniform (5.3–5.8 years), and age rank within the nine
groups was not related to dominance attainment (Kendall’s t-b = 0.09, P = 0.55).
There was considerable variation in body weight among the males, from a low
of 5.7 Kg to a high of 10.0 Kg. Examination of the raw data showed that the
males that eventually became high-ranking entered the group in a relatively
narrow weight range (7.2–8.4 Kg). On a group by group basis, the eventual alpha
male was initially the heaviest male in four of the groups, and the second heaviest
in the other five groups (Fig. 3). The two lightest males in each group never

TABLE I. Mean (+ Standard Error) Values for Demographic and Neurochemical Measures
Prior to Introduction by Eventual Rank Attainment

Variable Alpha Lower ranking

mean + s.e. mean + s.e.
Age (years) 5.4+0.05 5.5+0.02
Weight (kg) 7.8+0.2 7.3+0.2
5-HIAA 157+16 168+10
HVA 603+65 709+45
MHPG 70+14 75+7

80

60 5/9

4/9
% Alpha

40

20

0/9 0/9
0
Lowest Low-Mid High-Mid Highest
Body Weight
Fig. 3. Percentage of males that achieved alpha status as adults, by body weight prior to
introduction rank, ordered within groups.
10 / Fairbanks et al.

became alpha. The positive relationship between initial weight rank and
dominance attainment was statistically significant (Kendall’s t=–0.45, n=36,
Po0.001).

Serotonin, Dopamine, and Norepinephrine Metabolites

The mean concentrations of the metabolites of dopamine (HVA),
serotonin (5-HIAA), and norepinephrine (MHPG) in cisternal CSF collected
1–2 months prior to introduction are shown in Table I. Concentrations of
5-HIAA were highly correlated with HVA (r = 0.89). Within groups, the
relative rank order of HVA corresponded closely with that of 5-HIAA (t = 0.82,
n = 33, Po0.001). Males with lower levels of HVA and 5-HIAA were more
likely to become the alpha males of the group (HVA: t = 0.396, n = 33, P = 0.005;
5-HIAA: t = 0.272, n = 33, P = 0.047). None of the nine males with the
highest concentrations of these two metabolites in each group achieved alpha
status (Fig. 4a and b).
Levels of MHPG did not predict rank attainment in this sample (t = 0.07,
n = 33, P = 0.68).

Multivariate Analysis
A stepwise logistic regression was run to determine whether the
significant predictors of adult rank (described above) were independent and
additive. The binary-dependent variable was dominance rank at 1 year
post-introduction, and the independent variables were the within-group
rank order of natal adolescent Social Impulsivity scores, rank order of body
weight prior to introduction, and rank order of 5-HIAA and HVA concentra-
tions prior to introduction. Missing values were replaced with the mean
for the three cases with no values for the monoamine neurotransmitters.
The results supported the independent contributions of behavioral, morpho-
logical, and neurochemical factors in predicting adult dominance attainment
(Table II). Body weight was the first variable to enter the equation, followed
by natal Social Impulsivity. After step 2, both 5-HIAA and HVA were ready to
enter the model (5-HIAA, P = 0.013; HVA, P = 0.022). After the inclusion
of 5-HIAA in step 3, the independent contribution of HVA dropped to near zero
(P = 0.85). The final model predicted the correct dominance attainment for
33 of the 36 (92%) males.
The multivariate analysis produced the same results when the three subjects
with missing monoamine values were removed from the analysis.

Changes in Impulsivity From Adolescence to Adulthood

Figure 5 shows the Social Impulsivity scores for the same males tested as
adolescents and later as adults, by adult rank attainment. There was a significant
overall decline in scores from adolescence to adulthood (F = 31.3, df = 1,26,
Po0.001). There was also a significant interaction between age and eventual
status (F = 6.62, df = 1,26, P = 0.016). The males that became alpha were
significantly higher in impulsivity as adolescents, but then declined to the same
mean level of impulsivity as the lower-ranking males after they had achieved
alpha status as adults. As adults, five of the nine alpha males scored in the middle
third of the distribution of adult scores, three scored in the upper third, and one
scored in the lower third.
 Adolescent Impulsivity in Vervets / 11

80

60

4/9
% Alpha

40

4/15

20

0/9
0
Lowest Middle Highest
(a)
HVA
80

60
% Alpha

40
3/9 5/15

20

0/9
0
Lowest Middle Highest
(b) 5-HIAA
Fig. 4. Percentage of males that achieved alpha status as adults, by (a) HVA and (b) 5-HIAA levels
prior to introduction, rank-ordered within groups.
12 / Fairbanks et al.

TABLE II. Summary Table for Logistic RegressionFStep 3

Variable Wald df Significance

Body weight 4.76 1 .029
Adolescent impulsivity 4.69 1 .030
5-HIAA 3.96 1 .047

120

Alpha
100
Lower
Social Impulsivity Score

80

60

40

20

0
Adolescent Adult
Age
Fig. 5. Change in mean (7SE) Social Impulsivity scores for males tested as adolescents in the natal
group, and as adults 1 year following introduction to breeding groups, by eventual rank attainment.

DISCUSSION
This study identified behavioral, morphological, and neurochemical factors
that influence dominance acquisition in male vervet monkeys. By combining the
information in these three domains, we were able to predict the eventual
achievement of alpha status with a high degree of certainty for males entering a
new group.
The advantage of larger body size reported in other studies of group
formation [Morgan et al., 2000] was also found to predict rank attainment for
vervet males in this study. Males in the upper half of the weight distribution prior
to introduction were more likely to rise to the alpha position. Bastian et al. [2003]
reported that weight gain was a consequence, not a predictor, of dominance rank
for juvenile rhesus monkeys. For males entering a new group as adolescents or
adults, however, size appears to be an important factor in predicting rank
attainment [Packer, 1979].
 Adolescent Impulsivity in Vervets / 13

Adolescent males with the highest scores on the Social Impulsivity

Index were more successful in achieving high rank as adults than their more
moderate and cautious competitors. This result was contrary to our initial
expectation that males in the moderate range of responses on the intruder
challenge test would be more likely to achieve high rank when compared with
males scoring at the extremes. Immigration into established and stable
matrilineal groups involves many complex social skills for vervet males. Males
must respond to aggression from coalitions of resident females in a carefully
controlled manner that enables them to integrate into the group. They must
evaluate their own capacities in reference to their male competitors, and know
when to press and when to back off. Based on our prior results, and observations
of the immigration process, we expected that males in the moderate range of
responses on the intruder challenge test would be more likely to succeed.
Adolescent impulsivity is generally considered to be a problematic trait that is
associated with negative adult outcomes. Human children and adolescents with
impulse control problems are more likely to become substance abusers and
criminal offenders [McKay & Halperin, 2001]. Impulsive adolescent male rhesus
monkeys have been reported to exhibit higher rates of escalated aggression,
wounding, and mortality in free-ranging settings [Higley et al., 1996a].
Behavioral deficits associated with early maternal deprivation (e.g., excessive
aggression and disturbed social relationships) interfere with the acquisition of
high dominance rank for adult female rhesus monkeys [Bastian et al., 2003].
These findings indicate that there are costs associated with impulsivity and
excessive aggressiveness.
From another perspective, a certain degree of impulsivity may be necessary
to motivate males to leave the natal group and face the challenges of emigration
and immigration. Observations of successful male rank acquisition following
immigration indicate that a bold and aggressive style has a higher likelihood of
success than a more cautious and measured reaction [Mendoza, 1993; Silk, 2002;
van Noordwijk & van Schaik, 1985]. In longitudinal studies of human
development, Moffitt [1993] identified two distinct categories of individuals that
engage in antisocial behavior: those that are aggressive and antisocial at every life
stage, and those that exhibit adolescent-limited antisocial behavior. These two
patterns differ in etiology and outcome. The early-onset delinquents are at high
risk for adult psychopathology, substance dependence, financial problems, work
problems, and drug-related and violent crime, while the adolescent-onset
delinquents are less extreme on all of these measures as adults [Moffitt et al.,
2002]. Moffitt [1993] concluded that adolescent-limited antisocial behavior is
relatively normative and adaptable compared to life-course-persistent antisocial
behavior.
The finding that low levels of 5-HIAA and HVA are predictors of eventual
high rank for vervet males raises the question as to what behavioral
characteristics mediate this association. Impulsive or risk-taking behaviors, such
as engaging in contact aggression, early emigration from the natal group,
impulsive approach and aggression to an unfamiliar male, and longer leaps from
branch to branch have been associated with low levels of the serotonin metabolite,
5-HIAA, in rhesus macaques [Higley et al., 1996a; Kaplan et al., 1995; Mehlman
et al., 1994] and vervets [Fairbanks et al., 2001], and many of the behavioral
attributes measured in these studies are related to determination of dominance.
There are risks associated with such behaviors that may explain the higher
adolescent mortality rates reported by Higley et al. [1996a]. Perhaps the males
with low CSF 5-HIAA that survive have qualities of aggression, lack of fear,
14 / Fairbanks et al.

risk-taking, and physical size and strength that enable them to attain a high rank
after they immigrate into a new group.
The behavioral features associated with low 5-HIAA levels have been
interpreted as indicative of low social competence [Higley et al., 1996b],
but the relationship of low 5-HIAA levels to dominance rank has been
unclear. Low indicators of serotonin metabolism have been associated with
both high and low rank in female primates [Shively, 1995; Westergaard et al.,
1999], and there is no reliable evidence that low 5-HIAA levels are associated with
low rank for males of any nonhuman primate species [Kaplan et al., 2002]. In an
earlier study, vervet males treated with tryptophan or fluoxetine were reported to
rise in rank over control males, indicating that increased serotonin neurotrans-
mission enhanced rank acquisition [Raleigh et al., 1991]. However, a recent
attempt to replicate the fluoxetine treatment study failed to find an effect of the
serotonin reuptake inhibitor on rank attainment (McGuire and Pollack, personal
communication). The results of the present study indicate that low levels of 5-
HIAA prior to introduction are associated with high rank attainment. This is
consistent with the finding that, at least to a certain extent, impulsivity and lack
of inhibition give males an advantage in first encounters with unfamiliar
competitors.
Additional predictors of dominance that have been discussed in other studies
were not found to significantly influence rank acquisition for vervet males. For
example, behavioral reactivity, measured as locomotor activity in a novel
environment, was a predictor of low rank attainment for male fascicularis
macaques [Morgan et al., 2000]. In a preliminary report for the current study,
high levels of anxiety were associated with low rank attainment in vervet males
[Huff, 2002]. This effect was ephemeral, however, and did not predict stable male
rank in the full sample. A larger sample size, with validated measures of anxiety,
is needed to test the independent effects of impulsivity and anxiety on different
aspects of male rank attainment.
Matrilineal rank has been related to the timing of maturation and the age of
emigration from the natal group in free-ranging baboons and rhesus monkeys
[Alberts & Altmann, 1995; Bercovitch, 2000; Setchell & Dixson, 2002]. Sons of
high-ranking mothers tend to mature earlier, but they are also slower to leave the
natal troop. Because it is difficult to follow males after they emigrate, not much is
known about the influence of matrilineal rank on adult dominance attainment
outside the natal group. In this study, matrilineal rank did not predict which
males would achieve high rank following emigration from the natal group. There
is evidence from the Vervet Research Colony that rank attainment by adolescent
females is influenced by the presence of the mother, and that daughters that lose
high-ranking mothers during the juvenile years fail to achieve the family rank
[Fairbanks, 2000]. The number of males that had lost their mothers as juveniles
in the current study was too small (n = 4) to determine whether this factor was a
reliable predictor of male dominance attainment following emigration.
The longitudinal aspect of this study demonstrates that the traits that
predict dominance attainment for vervet males are not necessarily the traits that
differentiate dominant from subordinate males in stable groups. Males that were
high in impulsivity as adolescents became more moderate in their response to
strangers as adults. The most successful males responded with bold over-
confidence during the intense initial competition, and then became more
measured and conservative in their behavior as alpha males. Part of this change
was the natural modulation of behavior from adolescence to adulthood. The
greater decline in impulsivity in vervet males that became dominant supports the
 Adolescent Impulsivity in Vervets / 15

idea that an age-limited increase in impulsivity in adolescence is not a

pathological trait, but instead is related to later social success.
The results of this study underscore the importance of personality in
predicting individual life courses [Capitanio et al., 1999]. The finding that both
impulsivity and low 5-HIAA levels predict eventual male rank in this study
implies that vervet males are selected for ‘‘high risk–high gain’’ personality traits
at appropriate life stages. Whether the results of this study can be generalized to
other species remains to be determined. Vervets differ from male macaques and
baboons in the bipolar nature of the male hierarchy, and vervet males rarely use
male–male coalitions to rise in rank [Silk, 1999]. On the other hand, the lack of
clear male dominance over females means that vervet males have to establish
tolerant and supportive relationships with female group members before they can
establish residence in a new group [Cheney, 1983; Henzi & Lucas, 1980; Horrocks
& Hunte, 1993; Raleigh & McGuire, 1989]. Male–male relationships involve
complex displays that can erupt into contact aggression if they are not managed
effectively. In this context, vervet males that were bold and aggressive on the first
encounter were more likely to succeed in becoming dominant in the long run.
Field studies of males from other Cercopithecine species also suggest that a
confrontational and aggressive strategy works. and that adolescent impulsivity
may be an adaptive component of male life history strategy [Kaplan et al., 1995;
Fedigan & Zohar, 1997; van Noordwijk & van Schaik, 1985].

ACKNOWLEDGMENTS
This research was funded by a Department of Veterans Affairs Merit Review
grant and NIMH grant R01-MH61852-02 to Lynn Fairbanks, Conte Neuroscience
Center grant 5P50 MH62185 to J. John Mann, and institutional funds from the
Center for Primate Neuroethology, Neuropsychiatric Institute, UCLA. The
authors thank Danielle Epstein, Amanda Turner, and Denise Gomez for their
assistance with behavioral data collecting and processing, Glenville Morton for
collecting the CSF samples, and Dan Diekmann, Raul Amaya, and Glenville
Morton for their assistance with animal care and handling.

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