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Dominance index A simple measure of relative dominance status in primates.

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American Journal of Primatology 10: 291-300 (1986)
Dominance Index: A Simple Measure of Relative
Dominance Status in Primates
DORIS ZUMPE AND RICHARD P. MICHAEL
Department of Psychiatry, Emory University School of Medicine and The Georgia Mental
Health Institute, Atlanta, Georgia
A simple measure of relative dominance status (cardinal rank) is described
which we have termed the dominance index. Like more familiar techniques
for assessing rank order, it is based on the direction of aggressive and
submissive b,ehaviors between all possible paired combinations of animals
in a social group. Using data from five groups of female rhesus monkeys, it
reliably produced the same ordinal ranks as fight interaction matrices.
There was also good agreement with the cardinal ranks produced by two
additional measures of dominance and with those produced by observer
ratings. The dominance index can be calculated when fights have not
actually occurred and is largely independent of the frequency of agonistic
interactions. It has, therefore, wide application and can estimate dominance
during brief sampling periods (one hour) and also in stable groups when
agonistic interactions are low. Its application is described in experiments in
which the male in a group of females was changed and the hormonal status
of the females was altered. Estrogen increased female dominance status
relative to other females.
Key words: rank, agonistic behavior, social groups, hormones, primates, rhesus macaques, Macaca mulutta
INTRODUCTION
It is usual to assess the rank order of individuals in social groups of animals on
the basis of the direction of their agonistic behavior. The animal that directs aggressive but not submissive gestures toward other group members is considered to be
the highest ranking, while the individual directing submissive but not aggressive
gestures toward others is judged to be lowest ranking. The intervening ranks are
assessed on the basis of consistent wins and losses during agonistic interactions
between particular pairs of animals [Schjelderup-Ebbe, 1922; Richards, 1974; Bernstein, 1981; McMahan & Morris, 19841. However, such observations merely assign a
rank order (ordinal rank) and do not determine the degree or extent to which a
higher-ranking animal dominates the next lower-ranking individual (cardinal rank).
Received November 4, 1985;revision accepted January 26,1986.
Address reprint requests to Richard P. Michael, MD, Department of Psychiatry, Emory University School
of Medicine, 1256 Briarcliff Road, N.E., Atlanta, GA 30306.
0 1986 Alan R. Liss, Inc.
292 I Zumpe and Michael
A technique has recently been developed [Boyd & Silk, 19831 that permits the
assessment of relative as well as absolute rank in social groups of primates, but it
requires the application of a rather complex, iterative computer procedure and a
fairly large body of behavioral data. This limits its use with small captive groups in
which agonistic interactions may be infrequent and usually do not involve fights.
The dominance index described here is very simple to calculate and does not even
require the aid of a pocket calculator. It is based on the proportion of aggressive and
submissive behaviors between pairs of animals and is largely independent of the
absolute number of agonistic gestures made. Relative dominance can therefore be
evaluated on a day-by-day basis, and any changes can readily be related to other
behavioral or experimental variables. Its application to data from female-female
interactions is described here. This index has been informally used in our laboratory
for a number of years, and it now seems appropriate to provide sufficient detail to
facilitate its use by others.
METHODS
Animals
The behavioral data reported here were obtained from five groups of rhesus
monkeys (groups 1-5), each containing four females tested either alone or together
with one male. The 18 females and five males were all obtained a s adults from the
wild through dealers in North India. Males were intact, and females were ovariectomized several months before their use in a variety of behavioral studies from
which the data reported here were obtained. Except during tests, all animals were
housed in individual cages in large cage rooms where artificial lighting gave a 14hour day between 0615 and 2015 and temperature was maintained between 20 and
24°C. Food consisted of Purina Monkey Chow supplemented by fruit and vegetables,
and water was available ad libitum.
Hormone Treatments
In some of the behavioral studies, one or more females in a group were treated
with ovarian hormones. Details of the hormone treatments are not reported here
since they are irrelevant in the present context with the exception of group 4. In
group 4,each female in turn was treated first with 10 pg estradiol benzoate subcutaneously (sc)/day alone (EB) and then in combination with 50 mg progesterone sc/
day (EB + P) for five group tests while the other females in the group remained
untreated. When all four females had completed the hormone treatments, the male
was changed, and the process was repeated with each of three other males. With
each male, therefore, each female was observed during 30 tests while she was
untreated, during five tests while she received EB, and during five tests while she
received EB + P (see Fig. 3). Further details of this study have been given elsewhere
[Michael & Zumpe, 19841.
Behavioral Tests
Observations were made during 60-min behavioral tests conducted five days a
week on groups of four female rhesus monkeys, either with or without a male, in a
room 4.9 m wide by 4.9m deep by 2.1 m high [Michael & Zumpe, 19821. In addition
to social, grooming, and sexual behavior, the following behavioral interactions were
routinely scored (1)aggressive behaviors-the total numbers of bites, chews, grabs,
pulls, hits, chases, open-mouth threats, and aggressive jerks per test given and
received by each individual; (2) submissive behaviors-the total numbers of flees,
crouches, submissive presentations, and grimaces per test given and received by
each individual; (3) approaches-the total number of approaches to within touching
Dominance Index I 293
distance made and received by each individual; (4)departures-the total number of
departures (from within touching distance) made and received by each individual in
the group.
Dominance Index
The dominance index is based on the direction of aggressive and submissive
behaviors between the two members of all possible paired combinations of animals
in a group. It is calculated in four simple steps.
Percent aggressive behaviors given. For each pair, the number of aggressive
behaviors given by one animal to the other is expressed as a percentage of the total
number of aggressive behaviors given by both animals to one another. Thus, if
female A gives seven aggressive gestures to female B and if female B gives three
aggressive gestures to female A, female A scores 7/10 = 70% aggression given
while female B scores the reciprocal, ie, 3/10 = 30%aggression given.
Percent submissive behaviors reeeived. For each pair, the number of submissive
behaviors received is calculated exactly as described above for percent aggression
given. Thus, if female A receives eight submissive gestures from female B and if
female B receives two submissive gestures from female A, female A scores 8/10 =
80% submission received while female B scores the reciprocal, 2/10 = 20%submission received.
Percent aggression given and submission received per pair. For each pair, the
percent aggression given and percent submission received scores are combined for
each animal. Thus, female A scores (70% 80%)/2 = 75%, and female B scores
(30%+ 20%)/2= 25%.Where there are no aggressive interactions, percent submission received is used, and where there are no submissive interactions, percent
aggression given is used.
Dominance index. The dominance index is produced by averaging, for each
animal, the percent aggression given and submission received scores with all the
other animals in the group. Thus, if female A scores 75%with female B, 80% with
female C, and 100%with female D, her dominance index for the test would be (75%
+ 80% + 100%)/3= 85%. Animals not showing any agonistic interactions with
others are excluded from the averaging procedure.
+
Other Behavioral Measures
The dominance index was compared with some other behavioral measures,
namely: (1) rank order derived from fights unambiguously won and lost, ie, any
agonistic interaction in which the recipient of aggression responded with submission
toward the aggressor; fight interaction matrices were constructed by ranking animals so a s to minimize the numbers of interactions below the diagonal (see Table I);
(2) percent aggression given, calculated as described above and averaged for each
female in the group; (3) percent submission received, calculated as above and averaged for each female in the group; and (4)percent approaches made and departures
received, calculated like the dominance index but by using approaches and departures instead of aggression and submission; this resembles in some respects the
measures used by Hinde and colleagues to study mother-infant proximity interactions [Hinde & Spencer-Booth, 19671.
Observer Ratings
Many ethological insights originated from unconscious as well as conscious
mental processing of somewhat unstructured observations made on animals with
which observers were thoroughly familiar [Lorenz, 19811. The dominance index
would, in our view, be validated with the greatest level of confidence if it matched
294 I Zumpe and Michael
TABLE I. Interaction Matrix for Fights Clearly Won and Lost in a Group of Four Female
Rhesus Monkeys (Group 1): Data From 3 Successive Daily 1-Hr Behavior Tests After the
Introduction of an Unfamiliar Male
No. of fights
won by
Female A
Female L
Female E
Female I
Total
No. of fights lost by female
A
**
0
0
0
L
E
I
Total
1
3
15
1
20
15
5
35
15
0
55
**
**
0
0
1
0
0
**
18
36
TABLE 11. Comparison of Rank Order in Groups of Female Rhesus Monkeys as
Determined by Fights Won and Lost and as Determined by Dominance Index (Means
SEs for 3 Behavior Tests)*
Grauu
Group 1t?V = 55)
Rank order determined by fights
Dominance Index including fights
Dominance Index excluding fights
Group 2 (N = 12)
Rank order determined by fights
Dominance Index including fights
Dominance Index excluding fights
Group 3 (N = 43)
Rank order determined by fights
Dominance Index including fights
Dominance Index excluding fights
Group 4 (N = 13)
Rank order determined by fights
Dominance Index including fights
Dominance Index excluding fights
Group 5 RJ = 19)
Rank order determined by fights
Dominance Index including fights
Dominance Index excluding fights
n
Females
A
1
267
96 f 2.2
97 100 f 0.0
I
1
88 98 f 2.1
60 98 f 2.1
474
357
189
123
122
56
L
2
90 f 9.0
95 & 5.0
G
2
70 f 15.0
72 k 13.9
E
3
I
4
1 & 0.9
1 f 0.6
H
F
3
4
18 f 17.6
6 f 5.6
2 f 2.1
18 f 17.7
P
0
R
Q
3
1
2
4
100 f 0.0 89 _+ 11.0 33 f 0.0
0 0.1
100 f 0.0 83 f 16.3 33 +_ 0.0
1 f 0.5
N
K
J
M
2
3
1
4
100 & 0.0 66 f 1.0 22 f 11.1 12 f 12.1
100 f 0.0 66 f 1.2
28 k 14.7 12 f 12.3
C
H
B
D
2
3
4
1
95 f 4.9 52 f 11.3 41 f 22.6
0 f 0.0
92 f 8.4 44 f 5.6
50 f 9.6
0 0.0
34 k 0.8
57 f 21.5
*
*N, total number of fights; n, total number of agonistic behaviors used to calculate dominance index.
the independent ratings of highly trained observers thoroughly familiar with the
animals involved. To this end, the four trained observers who made observations on
the animals in group 1 (see Tables I, 111, Fig. 1)also rated the dominance ranks of
the females. Each observer was given a ten-inch horizontal line drawn on 0.1-inch
graph paper starting with 0% (lowest rank) on the left and ending with 100%
(highest rank) on the right. The observers were asked, for each of the four females
in the group, to place on the line a mark whose position indicated the dominance
rank of each animal with respect to the others.
Selection of Tests and Analysis
For each group of females (groups 14),three tests were selected that between
them provided at least one fight clearly won and lost for each of the six possible
Dominance Index I 295
paired combinations of females. The rank order produced by this fight interaction
matrix was compared with the dominance hierarchies produced by (1)the mean
dominance index per test for each female calculated on the basis of all agonistic
behaviors; (2) the mean dominance index per test for each female calculated on
agonistic behaviors excluding data from fights clearly won and lost; (3) the means
per test for percent aggression given, percent submission received, and percent
approaches made and departures received during the same three tests with group 1;
and (4) the mean observer ratings for group 1. Mean dominance indices were also
calculated for three tests with group 1conducted six months earlier. Finally, mean
dominance indices were calculated for the entire study involving group 4 to ascertain
if the dominance index would change with changes in the female's hormonal status
and with changes in the identity of the male in the group.
RESULTS
Dominance Index Compared With Fights Won and Lost
Although fights between females under our conditions were occasionally rather
severe, they generally involved only certain individuals and rarely all combinations
of animals. Of the 13 different groups of females observed between 1974 and 1985,
in only five groups (groups 1-5) was it possible to construct a n interaction matrix in
which a t least one fight (unambiguous outcome) was observed between every pair of
females. Table I shows the fight interaction matrix of group 1 females from which
the rank order was established. Rank orders were similarly obtained from the fight
interaction matrices of the other four groups. In the eight groups remaining, certain
individuals occasionally directed aaonistic behavior toward others, but either the
recipient failed to respond or, in thecase of fights, the outcome was unclear.
Table I1 shows, for each of the five groups for which ordinal ranks could be
GROUP 2
GROUP I
FIGHTS
PER TEST:
20
15
20
-
0-1-x
DATE: 6/15
FIGHTS
PER-TEST:
loo
x-x
6/16
6
6/17
O
6
3
4
l0/6
10/11
7/3
10/3
15
3
I
1 *--.-'
0-0
X-X
3/16
7/5
7/6
KEY
0-0
1/19
18
GROUP 5
3
.-a
DATE:
21
-
,-,
GROUP 4
4
GROUP 3
3
5/11
6/20
6/29
RANK I
RANK 2
RANK3
RANK 4
FEMALE
FEMALE
FEMALE
FEMALE
7/6
Fig. 1. The dominance index, for each individual in five groups of female rhesus monkeys, during three
behavior tests giving fight interaction matrices. For some females, the dominance index was stable, while
for others, major changes in dominance status occurred.
296 I Zumpe and Michael
assigned, the rank of every female determined by the fight interaction matrix
compared with the mean dominance index per test. There was complete concordance
for every group between the dominance hierarchy as assessed by fights and the
hierarchy as assessed by the mean dominance index (binomial test, P = .031). From
the dominance index data it appeared that the dominance status of certain females
was very similar. For example, in groups 1 and 3 there appeared to be little
difference between the two highest-ranking females in each group (A and L; 0 and
&I. In some cases this reflected a true equality between females, but in others there
were rank reversals, which balanced each other, over the time required to fill the
fight interaction matrix (Fig. 1).
For the purpose of comparison, the dominance index was recalculated by omitting all agonistic behaviors that occurred during fights won and lost. Because of
possible changes in dominance from test to test, this procedure was preferred to
selecting tests in which fights did not occur. Table I1 shows that, except for group 5,
there was complete concordance again between the fight rank order and the dominance index rank order calculated in this way. In group 5, however, there was a
rank reversal between females B and C between the second and third tests (Fig. 11,
which resulted in large test-to-test variance in dominance indices calculated by both
methods. This produced almost identical means per test for both females that were
slightly higher for female B when all agonistic interactions were used and slightly
higher for female C when fight interactions were excluded.
Dominance Index Compared With Other Behaviors and Observer Ratings
In order to examine how the dominance index compared with other behavioral
measures and with observer ratings of dominance rank, the data from the three
tests with group 1were analyzed in greater detail. Table I11 gives, for each female,
the means per test for the dominance index and for various other measures of
dominance during the same three tests. Also given are the mean observer ratings
for each female obtained one week later. There was quite close agreement between
the objective and subjective measures of relative dominance but not between these
and percent approaches made and departures received. Figure 2 compares the
dominance indices of females during each of three tests without a male (left) and
during three tests with a male (right) conducted six months later. The dominance
index for a given female generally remained quite stable despite large test-to-test
variations in the total numbers of agonistic behaviors. However, the relative dominance status of female E was clearly higher during the later sampling time than
during the earlier one.
Application of the Dominance Index
Does the dominance index have any utility? Since it provides a numerical
TABLE 111. Comparison of the Dominance Ranks of 4 Female Rhesus Monkeys (Group 1)
as Assessed by Dominance Index, Other Behavioral Measures, and Observer Rating (Means
SEs for 3 Daily Behavior Tests and 4 Observers)
Female A
Female L
Female E
Female I
Behavioral measures
% submission % approaches made + Observer
given
received
% departures received
rating
Dominance
index
% aggression
96 k 2.2
90 k 9.0
34 k 0.8
0.3 k 0.3
91 f 4.4
91 f 6.9
35 k 1.6
0.6 _+ 0.6
100 k 0.0
89 f 11.1
39 f 5.6
0 0.0
*
52
86
41
4
k 13.7
k 2.7
k 8.0
k 4.2
86
81
35
13
f 2.4
k 3.8
f 9.9
k 3.3
Dominance Index I 297
AGONlSTlC
BEHAVIORS
PER TEST:
./:\26
WITH MALE
WITHoUT MALE
66
e
129
100
75
50
25
a
0
Q
Q
-
I
1/15
x-x-x
-Female
I
1
1/16
1/19
6/15
6/16
6/17
Fig. 2. Comparison of test-to-test changes in the dominance indices of group 1 females during three
successive tests without a male Ueft) and during three successive tests with a male (right) conducted six
months later. In both situations, the dominance index for each female remained stable, although there
were large differences in the numbers of agonistic behaviors occurring in tests. The dominance status of
female E was consistently higher in tests with a male than in those without one.
measure for every test in which a n individual has any agonistic interactions with
others, it can be used to monitor changes in relation to other variables; this is
illustrated in Figure 3. The dominance index profiles are shown for the females in
group 4 during a long-term experiment reported elsewhere [Michael & Zumpe,
19841, in which the hormonal status of every female and the identity of the male in
the group were varied systematically. Female rank order, assessed by the mean
dominance index for the whole experiment with each male, remained constant
throughout. However, there were marked temporary changes in relative dominance,
and even temporary rank reversals; these occurred when the male was changed and
when females were treated with hormones. For example, when male 3 was replaced
with male 4,the dominance index of female J declined to well below that of female
K (both untreated) (Fig. 3, top panel). The dominance index profiles also changed
when females were treated with ovarian hormones (Fig. 3, middle and lower panels).
When females were given estrogen, the dominance index increased in 12 of 16 cases
(sign test on data from four females with each of four males, P = .038).
DISCUSSION
Like more familiar methods of determining rank order, the dominance index is
based on the direction of aggressive and submissive behaviors between the members
of all possible paired combinations of individuals in a group. Our data were derived
from female-female interactions but could be derived equally well from female-male
or male-male behavior. A behavioral index can be validated in terms of other
behavioral measures, and one does this by testing for concordance with other, often
simpler, behavioral measures. The dominance index was found to be perfectly concordant with fight interaction ranks (Table 111, and with aggression given, submission received, and observer ratings (Table III) in the five groups for which fight
matrices could be constructed. The advantages of the dominance index are that it
utilizes both aggressive and submissive behavior and that it can be calculated when
agonistic interactions are too infrequent to calculate one of the other two measures
reliably. There was also good agreement between the dominance index and mean
observer ratings. Observers were, however, clearly reluctant to employ the extremes
of the rating lines, and this was reflected in a 27% restriction of the range utilized.
Percent approaches made and departures received did not agree well with any of the
298 I Zurnpe and Michael
MALE :
FEMALE:
I
K J N M
2
3
K J N M
K J N M
4
K J N M
FEMALE UNTREATED
r-l
I I
h
h
0
h
N=
I 21 28 25
24 20 24 25
6 15 20 20
18 14 24 20
FEMALE GIVEN EB
83
oL
N=
5 5 3 5
4
5
5
5
2
3
5
4
1 5 4 5
2
5
FEMALE GIVEN E B + P
N*
3
4
1
4
3
5
5
4
4
1
2
3
0
0
Fig. 3. Changes in the dominance index profiles of group 4 females occurring with changes in the identity
of the male in the group and with changes in the hormonal status of females. EB = 10 pg estradiol
benzoate sciday. EB + P = 10 pg estradiol benzoate and 50 mg progesterone sc/day. N = number of tests
for which dominance index could be calculated. Vertical bars give standard errors of means.
other measures of dominance; it is obviously affected by many extraneous factors. It
was not possible to compare the dominance index described here with the method
developed by Boyd & Silk [1983] because the latter cannot be used unless there are
values in the cells below the diagonal of the interaction matrix.
The dominance index is simple to calculate and offers certain advantages. It can
be used to assess dominance in stable groups in which fights are infrequent and in
which rank order is maintained by occasional threats or submissive gestures. Such
situations are encountered in long-term studies with captive groups and in the wild.
Even in our newly formed groups of adult rhesus monkeys, in which aggression
frequencies are considerably higher than in stable natural troops, it required up to
four months to collect sufficient data to produce a fight interaction matrix (Fig. 1,
group 41, and in many groups it was never possible to do so. Consequently, the
assessment of ordinal rank by fights ignores temporary (or even permanent) rank
reversals during the period of data collection. Such reversals would produce values
in the cells below the diagonal of the fight interaction matrix. In contrast, the
dominance index gave almost identical values when calculated for tests including or
Dominance Index / 299
excluding fight interaction data (Table II), and it was to a large extent independent
of the total numbers of agonistic interactions taking place (Fig. 2). Thus, it can be
used with data collected during a relatively short time interval (one hour in our
case) and helps provide a numerical estimate of short-term changes in dominance.
The dominance index gives both a n animal’s position in the dominance hierarchy
(ordinal rank) and its dominance status in relation to others (cardinal rank); that is,
the index can measure whether a n animal outranks another by a wide or a narrow
margin. It also identifies social isolates with regard to agonistic interactions; namely,
those animals for which the dominance index cannot be calculated. Finally, the
dominance index is very versatile and can be adapted to specific situations. For
example, certain agonistic behaviors (eg, contact aggression and flight) may be given
greater weight than are others, or depending on the type of information sought, the
dominance index may be calculated for a social group as a whole or for specific
subgroups, such as matrilines.
The dominance index is likely to be most useful in situations in which the
method of Boyd & Silk [1983] cannot be conveniently used. These include small
groups of animals in which agonistic frequencies are low, situations in which there
are insufficient data for the construction of fight interaction matrices, and situations
in which there are no reversals during overt fighting. The dominance index does not
take the place of other measures of agonistic behavior, such as aggression and
submission frequencies, but provides a n additional measure for studies that focus on
dominance relationships. This index, like other proportional measures, is not normally distributed, and, as for the majority of behavioral measures, the index of one
animal is not completely independent of those of other group members. Despite
these shortcomings, it has proven to be a very useful measure of the influence of
dominance in our own behavioral work.
CONCLUSIONS
1. A dominance index has been developed which is based on the direction of
agonistic interactions between all individuals in a social group. It is simple to
calculate and is largely independent of changes in the absolute numbers of agonistic
interactions.
2. In five groups of female rhesus monkeys, there was complete concordance
between rank orders produced by the dominance index and those produced by fight
interaction matrices. There was also good agreement with two other measures of
agonistic behavior and with observer ratings. The dominance index can, therefore,
be considered a reliable measure of both ordinal and cardinal rank.
3. Because the dominance index can be calculated when fights with unambiguous outcomes do not occur, it is suitable for studies with short sampling periods and
with stable groups of animals in a wide range of situations.
ACKNOWLEDGMENTS
This work was supported by USPHS grant MH 19506, and general research
support was provided by the Georgia Department of Human Resources. Both are
gratefully acknowledged.
REFERENCES
Bernstein, IS. Dominance:The baby and the Hinde, R.A.; Spencer-Booth, Y.. The behavbathwater. BEHAVIORAL AND BRAIN iour of socially living rhesus monkeys in
SCIENCES 4:419-458,1981.
their first two and a half years. ANIMAL
Boyd, R.; Silk, J.B. A method for assigning BEHAVIOUR 15:169-196, 1967.
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OLOGY. THE PRINCIPAL IDEAS AND
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DISCOVERIES IN ANIMAL BEHAVIOR. Michael, R.P.; Zumpe, D. Interactions of soNew York, Springer-Verlag, 1981.
cial, spatial and hormonal factors on the
McMahan, C.A.; Morris, M.D. Application of
behavior of rhesus monkeys (Macaca mumaximum likelihood paired comparison
latta). PRIMATES 25~462-474,1984.
ranking to estimation of a linear dominance Richards, S.M. The concept of dominance and
methods of assessment. ANIMAL BEHAVhierarchy in animal societies. ANIMAL BEHAVIOUR 32:374-378,1984.
IOUR 22:914-930,1974.
Michael, R.P.; Zumpe, D. Influence of olfac- Schjelderup-Ebbe, T. Beitrage zur Sozialpsytory signals on the reproductive behaviour
chologie des Haushuhns. ZEITSCHRIF'T
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