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Effects of ovarian hormones on the behavior of captive Macaca fascicularis.

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American Journal of Primatology 8:167-181 (1985)
Effects of Ovarian Hormones on the Behavior of Captive
Macaca fascicularis
DORIS ZUMPE AND RICHARD P. MICHAEL
Department of P.sychiatry, Emory University School of Medicine, Atlanta, and The Georgia
Mental Health Institute. Atlan.ta
To examine the effects of ovarian hormones on the behavior of female
Macaca fascicularis and their male partners, daily 1-hr behavior tests were
conducted while ovariectomized females were (1)untreated, (2) given estradiol benzoate (EB) (5 pg subcutaneously [s.c.]/day), (3) given estradiol benzoate together with increasing doses of progesterone (P)(5 mg, 10 rng, and
20 mg. s.c./day), and (4)given testosterone propionate (TP)(0.25 mg s.c.iday)
(six pairs, 540 tests). Weekly blood samples were analyzed by radioimmunoassay for plasma hormone levels (81 samples). Estrogen treatment produced plasma estradiol levels similar to those of intact females during the
late follicular phase of the menstrual cycle. Additional progesterone at the
lowest dose produced plasma progesterone levels similar to or somewhat
higher than those during the midluteal phase, while higher doses produced
supraphysiological levels. Androgen treatment resulted in plasma levels
well above the physiological range. Hormone treatments produced highly
significant effects on the sexual, social, and aggressive interactions of the
pairs. As in rhesus monkeys, estrogen increased male and female sexual
activity, and increasing doses of additional progesterone reversed these
effects. Unlike in rhesus monkeys, testosterone propionate increased both
female sexual motivation (invitations) and also male sexual activity and
ejaculatory performance. The direction of the hormone-dependent changes
in grooming and aggressive interactions confirmed earlier results with
intact females and indicated that aggressive interactions and male grooming times were highest, and female grooming times were lowest, when
copulatory activity was at its height.
Key words: Macaca fascicularis, estradiol, progesterone, testosterone, sexual behavior,
grooming, aggression
INTRODUCTION
In a previous study [Zumpe & Michael, 19831, we compared the behavioral
interactions of oppositely-sexed pairs of Macaca fascicularis under controlled laboratory conditions with those of M. mulatta tested by the same observers under
Received August 4, 1984; revision accepted October 21, 1984
Address reprint requests to Dr. Richard P. Michael, Department of Psychiatry, Emory University School
of Medicine, Post Office Box AF, Atlanta, GA 30322.
0 1985 Alan R. Liss, Inc.
168 I Zumpe and Michael
identical circumstances. The results suggested that M. fascicularis would be a
suitable species for studying the neuroendocrine mechanisms underlying the behavior of higher primates, since the behavioral interactions of the pair appeared to be
strongly influenced by the changing hormonal status of the female during the
menstrual cycle. In M. fascicularis, ejaculatory performance and thrusting rates
were higher than in M. mulatta during the follicular phase of the menstrual cycle
and declined more sharply after the expected time of ovulation. In addition, there
was also evidence that female sexual motivation was consistently higher during the
follicular than during the luteal phase of the cycle. However, there were some
notable behavioral differences between the two species, and these were thought t o
have their origins in the fact that M. fasuicularis is less sexually dimorphic than M.
mulatta. In particular, a n analysis of their agonistic interactions demonstrated that
female M. fascicularis were less dominated by their male partners than were female
M. mulatta, and changes in the female’s motivational state were more readily
expressed by changes in overt behavior in M. fascicularis than in M. mulatta. Thus,
M. fascicularis, under our test conditions, showed larger changes in measures of
female sexual motivation and smaller changes in measures of male sexual motivation during the menstrual cycle than did M. nulatta. The present study was undertaken to extend these findings in M. fascicularis to ovariectomized females by
examining the behavioral effects of exogenous estradiol benzoate, progesterone, and
testosterone propionate in doses comparable with those used previously in M. muZatta [Michael et al, 1968; Michael et al, 1972; Michael and Zumpe, 19771, whose
body weights are about twice those of cynomolgus monkeys.
METHODS
Animals
Four mature male (weighing 4.9-5.1 kg) and three adult female (weighing 2.63.7 kg) M. fascicularis were obtained as adults through dealers directly from the
wild in Malaysia. Animals were housed in individual cages together in a room in
which natural daylight was supplemented by artificial lighting, which was activated
by a photocell controlled by the natural daylength. Temperature was maintained
between 20°C and 24°C. Food consisted of Purina Monkey Chow, supplemented by
vitamins, fresh fruit, and vegetables; water was available ad libitum.
Operative Prncedures and Hormone Treatments
All females were ovariectomized bilaterally through a midline subumbilical
incision several weeks before the experiments started. Histological examination
confirmed that ovariectomy was complete. All hormone treatments were given for
periods of four weeks and were administered daily subcutaneously (s.c.) in oil at
0800 hr. However, the first injection of each treatment was given at 1200 hr after
testing. In conformity with earlier studies on M. mulatta, treatments were given in
the following order: (i) 5 p g estradiol benzoate alone; (ii) 5 pg estradiol benzoate
together with 5 mg progesterone; (iii) 5 pg estradiol benzoate together with 10 mg
progesterone; (iv) 5 p g estradiol benzoate together with 20 mg progesterone; (v) 5 pg
estradiol benzoate alone; and after a n interval of 5 weeks, (vi) 0.25 mg testosterone
propionate. New hormone treatments were started at 1200 hr on Fridays after that
day’s behavioral test, and data collection began 3 days later on the following
Monday.
Collection of Plasma Samples and Steroid Assays
Blood (3 ml) was obtained at 1600 h r once a week (Thursdays) from the untranquillized females that had previously been adapted to the sampling procedure. Since
Hormones and Behavior in M . fascicularis I 169
the saphenous veins of females were small and not always suitable for repeated
blood sampling, the tail vein was sometimes used instead. Plasma levels of estradiol,
progesterone, and testosterone were analyzed in the same duplicate 0.5 ml plasma
aliquots by a method that involved chromatography on Sephadex LH-20. Steroid
concentrations were measured by radioimmunoassay with highly specific antisera,
and results were calculated using a four-parameter mass-action equation and a
computer. Inter- and intra-assay coefficients of variation were less than 12% (estradiol) and less than 6% (progesterone and testosterone), and water blanks read -2.6
to 2.6 pg (estradiol and testosterone) and 0 to 13.4 pg (progesterone). Plasma testosterone levels during androgen treatment were estimated by radioimmunoassay
without chromatography as previously described for males [Bonsall et al, 19761. We
report here on the last three samples from each treatment period when conditions
were fully stabilized (81 samples).
Behavioral Testing Procedures
Observations were made during 60-min test sessions on oppositely-sexed pairs
of animals behind one-way vision mirrors. Tests were conducted 5 days a week in
special observation cages 1.19 m wide by 1.07 m deep by 1.14 m high, into which
first the male and then the female were introduced a t the beginning of each test
session. At all other times animals were caged singly. Each female was tested with
each of two male partners on alternate test days. Two females and two males were
tested in a cross-over design controlling for individual differences and partner
preferences, while the third female (initially together with one that died) was tested
with two other males (six pairs, 540 1-hr behavior tests).
Definitions and Terminology
The following measures of behavior, described in detail elsewhere [Zumpe &
Michael, 19831, receive numerical treatment here: (1)number of ejaculations per
test; (2) time to first ejaculation-time in seconds from the start of the test to the
first ejaculation (in the absence of any ejaculations, a default value of 3,600 sec was
assigned); (3) number of mounts per test; (4)number of male mounting attempts per
test-sum of male-initiated mounts and attempts to mount by the male that were
refused by the female; (5) number of male-initiated mounts per test; (6) latency to
first male mounting attempt-time in seconds from the start of the test to the first
male mounting attempt; (7) number of female sexual invitations per test; (8)number
of female-initiated mounts per test; (9) latency to first female invitation-time in
seconds from the start of the test to the first female sexual invitation; (10) male
success ratio-percentage of male mounting attempts that initiated a mount (in the
absence of any male mounting attempts, a default value of 100% was assigned for
statistical purposes only); (11)male grooming time per test fsecf;(12) female grooming time per test (sec); (13) male direct aggression-number of aggressive gestures
directed by the male a t the female; and (14) female direct aggression-number of
aggressive gestures directed by the female at the male.
Selection of Tests for Numerical Treatment
For each pair of animals, the data from the last ten tests with the female
ovariectomized and untreated (6 months post-ovariectomy) were compared with the
data from each of the ten test periods (4weeks) that followed when females were
treated with ovarian hormones. After estrogen withdrawal, and again after androgen withdrawal, 10 days were allowed to elapse between the last hormone injection
and the first of the ten tests used to re-establish behavioral baselines. Thus, quantitative comparisons were made between data from ten tests per pair during each of
"Single value.
0.25 mg
TP
Untreated
Untreated
5pgEB +
5mgP
5ggEB +
10 mg P
5pgEB +
20 mg P
5 !G EB
Ovariectomized
5 Pg EB
*
10.5 &
3.59
85.0 k
28.60
95.8 k
29.44
81.9 k
14.79
71.8 k
19.12
194.9 k
53.94
9.5
4.79
17.3 k
2.71
3.2
1.62
26.1 i
12.64
127.8 f
44.78
68.3 &
5.37
58.2 k
4.99
48.5 &
8.54
65.7 &
6.22
18.5 &
5.59
18.6 &
13.00
29.6 &
6.13
No data
No data
No data
6.4
1.07
110.3 ?i
28.33
61.2 -t
11.62
37.3 t
2.29
44.6 k
11.21
48.6"
Plasma Ez (pg/ml)
Female 1
Female 2
Female 3
2.9
0.32
2.3
0.03
63.8 &
5.10
60.2 &
8.50
118.5 f
11.9
0.9 &
0.41
0.3 +
0.00
1.0 I
0.27
0.4 i
0.09
*
0.3 k
0.30
0.0 &
0.00
32.2 i
3.92
69.8 &
9.11
102.6 k
6.10
0.3 &
0.15
1.4 f
1.04
0.8 k
0.06
0.5 &
0.27
*
*
0.8 f
0.22
1.1
0.12
17.6 +_
2.65
49.4 &
8.94
68.6 f
6.85
0.9 k
0.15
1.2 f
0.46
0.4 &
0.12
1.1
0.20
Plasma P (ng/ml)
Female 1
Female 2
Female 3
96.1 _+
5.94
94.7 &
2.18
119.0 +
14.89
134.3 k
5.42
188.0 &
17.47
141.2 k
22.73
126.9 +
10.96
17934 i
2831
68.3 f
13.31
Female 1
80.2 &
2.44
100.8 k
11.04
118.3 5
4.77
119.5 k
8.50
147.9 &
7.70
73.6 k
3.87
130.0 I
12.50
5596 i;
791
251.1 _C
36.96
31.7 &
6.41
69.4 i
11.87
33.4 &
6.95
48.8 j~
12.87
59.3 k
5.05
67.8
35.00
72.7 f
42.50
11519 +
719
63.9 k
13.55
Plasma T (pg/ml)
Female 2
Female 3
TABLE I. Changes in Plasma Hormone Levels for Each of Three Ovariectomized iM. fasciculuris in Response to Different Hormone
Treatments (Means + S.E.M. for Three Samples)
L
r
5n
!
z
s
C
N
-4
0
.
Y
Hormones and Behavior in M. fasciculuris I 171
nine experimental conditions when the female was (1) untreated, (2) treated with
estradiol benzoate, (3-5) treated with estradiol together with three increasing doses
of progesterone, (6) treated with estradiol alone, (7) untreated (estrogen withdrawal),
(8) treated with testosterone propionate, and (9)untreated (androgen withdrawal).
We have also provided data for the purpose of comparison h o t analyzed statistically)
from 149 one-hr behavior tests conducted during two menstrual cycles with each of
the same six pairs of animals when the females were still intact. These latter data
are a subset of those published previously [Zumpe & Michael, 19831.
Statistical Treatment of Results
The significance of the differences in behavior among the nine experimental
conditions was assessed by standard analysis of variance for repeated measures
using a treatment by animal-pair by test-order design. The Scheffi. test was used to
make comparisons between means [Winer, 19711. These results are given in the
tables, where underlining groups data not significantly different from each other.
Latencies to the first male mounting attempt and to the first female invitation,
which showed a bimodal distribution, were analyzed by the median test [Siegel,
19561.
RESULTS
Plasma Hormone Levels
Table I gives the mean plasma estradiol, progesterone, and testosterone levels
for each ovariectomized female during each treatment condition. Estrogen treatment
resulted in plasma estradiol levels similar to those during the latter part of' the
follicular phase of the menstrual cycle when these females were intact (about 100
pgiml). Additional treatment with 5 mg progesterone produced plasma progesterone
levels that were similar to or higher than those occurring during the midluteal
phase when these females were intact (5.0-16.0 ng/ml), and higher doses produced
progesterone levels well above the physiological range. Testosterone propionate
administration resulted in plasma testosterone levels greatly in excess of the physiological range for these females when intact (about 500 pgjml).
Sexual Behavior
Table I1 gives, for each of the nine treatment conditions, the means per test for
numbers of ejaculations, time t n ejaculation, and numbers of' mounts for all six pairs
combined. For the purpose of comparison, the top line in the table gives data from
these pairs when the females were intact. Treating ovariectomized females with
estradiol benzoate, progesterone, and testosterone propionate produced highly significant changes in all three measures of behavior. Estradiol restored ejaculatory
and mounting activity, and the additional administration of increasing doses of
progesterone progressively reversed these effects. When progesterone was withdrawn, behavior reverted to the levels observed during treatment with estradiol
alone. Testosterone propionate produced significant changes in all three behavioral
measures. In summary, the sexual performance of male M. fascicularis was enhanced by treating their female partners with both estradiol and testosterone and
was progressively suppressed by increasing doses of progesterone.
Examination of data from individual pairs of animals revealed that the behavioral effectiveness of the various hormone treatments depended very much on the
identity of the female of the pair. This is illustrated in Figure 1, which shows
changes in the ejaculations of males paired with different females. It can be seen
that with female 1 there was a major effect with estrogen but a trivial effect with
both progesterone and testosterone. With female 3, both estrogen and progesterone
P
F8,40
Intact
(1) Ovariectomized
(2) 5 p g EB
(3) 5 p g E B + 5 m g P
(4) 5 pgEB t 1 0 m g P
(5) 5 p g EB + 20 mg P
(6) 5 p g EB
(7) Untreated
(8) 0.25 mg TP
(9) Untreated
S.E.
*
2.2 k 0.07
0.9 k 0.11
2.4 k 0.10
1.8 k 0.14
1.4 + 0.15
1.2 i 0.13
2.3 k 0.12
1.0 0.10
1.6 f 0.10
0.8 k 0.10
12.1
< 0.001
9 1 7 5 4 8 3 6 2
149
60
60
60
60
60
60
60
60
60
N
No. of
ejaculations
Mean
149
60
60
60
60
60
60
60
60
60
N
*
448.8 & 77.83
1785.9 209.12
95.2 f 49.37
874.7 i 177.16
1266.8 212.73
1476.3 k 218.36
414.4 k 139.28
1505.1 f 201.52
635.9 i 139.50
1874.1 i 213.35
4.8
< 0.001
2 6 8 3 4 5 7 1 9
Time to
ejaculation (sec)
Mean k S.E.
*
*
12.3 k 0.53
5.8 0.53
9.8 k 0.62
7.3 k 0.67
5.4 f 0.61
4.6 0.59
8.6 0.65
4.4 k 0.47
8.5 i 0.60
3.9 k 0.47
4.3
< 0.001
9 7 5 4 1 3 8 6 2
149
60
60
60
60
60
60
60
60
60
N
No. of
mounts
Mean & S.E.
TABLE 11. Effects on Male Sexual Performance of Treating Ovariectomized M . fasciculuris With Gonadal Hormones (Six Pairs)
k
z$
P
5a
9
N
.
!si
h3
Hormones and Behavior in M. farsciculuris I 173
I
FEMALE I
c,
G
h
8
2I
I
o
No. of tests. 23
I
0
10
I0 1010 10 10
10
10
10
10
10 I 0 0 10 10
10
10
I0
24
10
:O 10 : O K 10
10
10
10
28
10
10 101010 10
10
I0
10
23
FEMALE 2
2 N o . o f tests. 23
10
10 I 0 0 I0 10
10
LO
FEMALE 3
No. of t e s t s , 28
I0
I0 1010 10 10
10
10
10
HORMONAL STATUS OF FEMALES.
0
Intact
Untreated
5 pg E B
2 5 mg T P
5 p g EB + 5, 10 and 20 rng P respectively
DO
Fig. 1. The effects on the ejaculatory performance of male M. foseicrtlnris of' treating nvariectomized
females with exogenous hormones. With female 1 (top) estrogen treatment (EB) increased ejaculations,
hut additional progesterone (P)and testosterone (TP)had rather weak effects. With female 2 (middle) both
EB and P had very strong behavioral effects, while with female 3 (butturn) the effects of TP were
particularly obvious. Vertical bars give standard errors of the means.
P
F8,40
Intact
(1) Ovariectomized
(2) 5 pgEB
(3) 5 p g E B + 5 m g P
(4) 5 pg El3 + 10 mg P
(5) 5 pg ER + 20 mg P
(6) 5 pg EB
(7) Untreated
(8) 0.25 mgTP
(9) Untreated
9.8 k 0.59
5.2 & 0.60
8.6 k 0.70
6.1 + 0.58
4.5 k 0.50
3.2 k 0.39
7.0 & 0.84
4.4 k 0.67
6.5 k 0.77
3.2 k 0.49
3.2
< 0.01
5 9 7 4 1 3 8 6 2
149
60
60
60
60
60
60
60
60
60
N
No. of
male mounting
attempts
Mean k S.E.
46.0 k 13.85
504.1 k 145.52
13.0 i 3.22
107.9 k 68.46
627.0 + 181.11
811.6 k 198.27
140.6 & 87.49
560.4 k 161.89
121.2 & 70.58
660.5 182.48
1.8
N.S.
2 3 8 6 1 7 4 9 5
140
49
57
56
51
48
53
47
52
48
N
Latency of first
male mounting
attempt (sec)
Mean k S.E.
149
60
60
60
60
60
60
60
60
60
N
*
9.3 k 0.55
4.1 k 0.46
7.9 i 0.62
5.2 k 0.51
3.5 & 0.44
2.6 0.39
6.1 k 0.68
2.3 i 0.27
5.2 i 0.51
1.6 0.22
4.1
< 0.005
9 7 5 4 1 3 8 6 2
No. of
male-initiated
mounts
Mean 5 S.E.
TABLE 111. Effects on Male Sexual Motivation of Treating Ovariectomized M . fuscieuZurisWith Gonadal Hormones (Six Pairs)
E
1
zi;’
B
lu
i2
3
F
Ib
.
s
Hormones and Behavior in ill. fascieularis I 175
exerted massive effects, while that of testosterone was quite minor. With female 3 ,
all three hormones exerted quite well-marked effects.
Male and Female Sexual Motivation
Table I11 gives, for each of the nine treatment conditions, the means per test for
three measures of male sexual motivation (mounting attempts, latency to the first
mounting attempt, and male-initiated mounts) for all six pairs combined. There
were significant treatment effects for mounting attempts and male-initiated mounts,
which increased during estradiol and testosterone treatments and declined during
treatment with even the lowest dose of progesterone. Latencies to the first male
mounting attempt did not reach statistical significance by analysis of variance
because of high within- and between-pair variance and a bimodal distribution.
Because of this, the data were re-analyzed by median test (chi-square = 49.2, df 8,
P < 0.001). Latencies shortened significantly with estradiol and testosterone, and
lengthened progressively with increasing doses of progesterone.
Table IV gives, for each of the nine treatment conditions, the means per test for
four measures of female sexual motivation (female sexual invitations, latency to the
first female invitation, female-initiated mounts, and male success ratio) for all six
pairs combined. While these measures showed trends similar to those for male
sexual motivation, results were not strongly significant and were not significant at
all for two indices by analysis of variance (median test on latencies to the first
female invitation, chi-square = 18.4, df 8, P < 0.02), suggesting that female sexual
motivation was less affected by the hormone treatments. However, examination of
data from individual pairs showed that this was not quite so; effects depended upon
the identity of the female. This is illustrated in Figure 2, which shows data for
females 2 and 3 from tests with male 4.With both females there were systematic,
hormone-related changes in male mounting attempts. Female 2, which received
consistently more mounting attempts than female 3, made few sexual invitations
and many refusals, so that there were marked hormone-dependent changes in male
success ratios (Fig. 2, middle). Female 3, on the other hand, received fewer mounting
attempts and made relatively few refusals, so that male success ratios were high
throughout (Fig. 2, middle). However, this female made large numbers of sexual
invitations, which increased with both estrogen and androgen treatment and declined with progesterone administration; these contributed importantly to the
changes in ejaculatory activity (Fig. l., bottom right). Both females, therefore,
demonstrated hormone-dependent changes in sexual motivation but differed in the
behavioral mechanisms by which they were expressed: by refusing in female 2 and
by inviting in female 3 .
Grooming and Agonistic Behavior
Table V gives, for each of the nine treatment conditions, the means per test for
male and female grooming times and male and female aggression for all six pairs
combined. There were significant hormone effects on both male and female grooming
times and on male aggression. Estrogen alone significantly decreased male grooming times and increased female grooming times, and these effects were reversed
when females received 10 mg progesterone in addition. Androgen, like estrogen,
tended to decrease male grooming and increase female grooming, but these changes
were not statistically significant. Estrogen also significantly increased male aggression; additional progesterone, even at the lowest dose, resulted in a significant
decline that was reversed when progesterone was withdrawn. Examination of data
from individual pairs revealed a large amount of variability, although most pairs
reflected the changes outlined here. Figure 3 gives the results for one representative
P
F8,40
+
+
+
Intact
(1) Ovariectomized
(2) 5 p g EB
(3) 5 p g E B 5 m g P
(4) 5 pg EB 10 mg P
(5) 5 gg EB 20 mg P
(6) 5 pgEB
(7) Untreated
(8) 0.25 mg TP
(9) Untreated
Mean f S.E.
149
60
60
60
60
60
60
60
60
60
+
19.2 + 1.63
5.9 f 0.64
9.0 i: 1.14
7.8 f 0.88
6.9 f 0.80
7.3 & 0.73
8.4 k 0.96
7.8 k 0.92
10.2 1.16
6.2 f 0.69
2.2
< 0.05
1 9 4 5 3 7 6 2 8
N
No. of
female sexual
invitations
N.S.
376.2 i 117.49
572.5 f 156.39
10.3 5.74
430.8 i 155.92
656.6 C! 197.93
835.2 k 197.56
437.6 f 205.44
302.5 i 115.20
275.2 i 152.83
385.9 i 122.39
1.9
Mean k S.E.
2 8 7 9 3 6 1 4 5
43
52
14
34
43
52
30
46
30
56
N
Latency to first
female sexual
invitation (sec)
3.0 0.29
1.7 0.25
1.9 i: 0.28
2.1 0.29
1.9 & 0.28
2.1 i 0.28
2.5 f 0.32
2.1 k 0.33
3.3 0.46
2.3 & 0.35
2.3
< 0.05
1 2 4 5 7 3 9 6 8
149
60
60
60
60
60
60
60
60
60
No. of
female-initiated
mounts
N
Mean + S.E.
97.1 0.62
84.6 & 3.24
93.7 k 1.50
87.2 i 3.52
83.2 f 4.56
74.8 -t 5.83
93.0 f 2.11
72.5 + 5.08
89.9 f 2.17
65.1 k 6.02
2.0
N.S.
9 7 5 4 1 3 8 6 2
147
58
59
58
54
51
59
54
58
50
N
Male
success ratio
Mean & S.E.
TABLE IV. Effects on Female Sexual Motivation of Treating OvariectomizedM . fmciculariv With Gonadal Hormones (Six Pairs)
h
1
s
i;'
BEU
fi
8
N
s
3.
Intact
+
P
F8,40
(5) 5 pg EB + 20 mg P
(6) 5 p g E B
(7) Untreated
(8) 0.25 mg TP
(9) Untreated
(1) Ovariectomized
(2) 5 pg EB
(3) 5 p g E B + 5 m g P
(4) 5 fig EB 10 mg P
149 1575.4 47.14
60 1270.7 f 79.65
60 2085.2 & 76.78
60 1860.5 k 105.61
60 1686.1 i 96.49
60 1687.5 & 79.30
60 1752.1 k 96.77
60 1612.7 k 74.44
60 1833.2 k 110.14
60 1602.0 93.54
2.6
< 0.025
1 9 7 4 5 6 8 3 2
169.5 k 28.27
788.3 f 96.79
495.4 f 71.66
688.7 & 87.13
1066.1 & 99.84
982.7 k 90.84
618.4 k 77.84
821.6 -t 96.56
674.3 k 77.17
797.8 i 104.77
4.5
< 0.001
2 6 8 3 1 9 7 5 4
149
60
60
60
60
60
60
60
60
60
Female grooming
time (sec)
N
Mean k S.E.
Male grooming
time (sec)
N
Mean S.E.
*
2.3 0.27
0.0 f 0.00
1.1 k 0.28
0.1 k 0.04
0.1 0.03
0.1 0.04
1.3 k 0.30
0.0 i 0.02
0.4 i 0.13
0.1 k 0.09
4.8
< 0.003
1 7 4 5 3 9 8 2 6
149
60
60
60
60
60
60
60
60
60
Male direct
aggression
N Mean i S.E.
N.S.
*
*
1.6 k 0.24
0.7 k 0.41
1.1 & 0.30
1.3 f 0.35
1.6 0.50
1.1 i 0.31
1.2 k 0.32
1.3 0.36
0.6 k 0.12
0.7 k 0.19
0.9
8 9 1 5 2 6 3 7 4
149
60
60
60
60
60
60
60
60
60
Female direct
aggression
N Mean + S.E.
TABLE V. Effects of Treating Ovariectomized M . fascicuZarisWith Gonadal Hormones on Grooming and Aggressive Interactions With
Their Male Partners (Six Pairs)
.
2
5.
178 I Zumpe and Michael
MALE 4
FEMALE
I
2
I
f
T
20
10
,mm
0
N o of
tests. 24
10
10 10 10 10 10
10
10
10
28
10
I0 10 10 IC I0
10
li
IC
HORMONAL STATUS OF FEMALES:
a5 pg
.Intact
0Untreated
m 5 pg E B
EB t 5, 10 and 20 rng P reSp8CtlVeIy
DO 25 rng T P
Fig. 2. “ k o different mechanisms by which two females, both paired with the same male, expressed
hormone-dependent changes in sexual motivation. Female 2 (left), receiving many male mounting attempts, showed hormone-dependent changes in receptivity (changes in male success ratios); female 3
(right), receiving fewer male mounting attempts, generally accepted them but showed hormone-depcndcnt
changes in proceptivity (changes in sexual invitations). Vertical bars give standard errors of the means.
pair and shows that the male directed most aggression at the female, and groomed
her least, when she was treated either with estrogen or with androgen, that is,
during treatments when copulatory activity was maximal (Fig. 1). In contrast,
female grooming times were shortest when copulatory activity was minimal.
DISCUSSION
The present study, as well as the earlier one [Zumpe & Michael, 19831, using M.
fmcicularis stemmed from the fact that feral-reared M. ntulatta are generally less
Hormones and Behavior in M. fasciculuris I 179
MALE 4 WITH FEMALE 3
1000 7
NO. of tests
1
I
28
10
10 10 10 10 10
10
10
10
28
10
10 10 1010 10
10
10
10
HORMONAL STATUS OF FEMALE
Intact
5 y g EB
t
nuntreated
5 , 10 and 20 rng P respectively
59g EB
00 - 2 5 mg
TP
Fig. 3. Data from one pair illustrating hormone-dependent changes in grooming and aggressive interactions. During hormone treatments that produced high levels of ejaculatory activity (EB and TP), male
grooming times were short, and aggression, especially by the male, was high. Female grooming times
tended to increase during treatments producing high ejaculatory activity. Vertical bars b<ve standard
errors of the means.
available for behavioral studies now than in the past. All the results reported here
confirm observations made upon intact females paired with males during normal
menstrual cycles. Although only six pairs were used, the results were remarkably
clear-cut for a behavioral project involving primates, and further replications with
more animals seemed unwarranted at this stage. Despite significant differences
between individual pairs (Fs,72 = 6.4-241.3, P < 0.001), hormone treatments had
very predictable and highly significant effects on the sexual, social, and aggressive
interactions of the pair (Tables 11-V). As in rhesus monkeys, estrogen increased
ejaculatory activity and measures of both male and female sexual motivation, while
additional progesterone reversed these effects. In fact, M. fusciculuris appeared to be
more sensitive than rhesus monkeys to progesterone. With 2 pgikg estradiol benzoate (EB), most of the behavioral effects of progesterone were established at 2 mg/
kg, whereas in rhesus monkeys receiving 1 K g k g EB, 5 mgikg progesterone was
needed [Michael et al, 19681. Changes in male sexual motivation were more conspicuous throughout than were changes in female sexual motivation, and this finding
was in line with results obtained in rhesus monkeys. The old observation in rhesus
monkeys [Michael & Welegalla, 19681 that two behavioral mechanisms exhibited by
180 I Zumpe and Michael
females contributed to the decline in male ejaculatory activity during the luteal
phase was readily confirmed in M. fascicularis. The first mechanism depended upon
loss of female receptivity (increased refusals), and the second depended upon the loss
of female proceptivity (decreased invitations). This leaves out the question of declining male motivation, which could involve pheromones, as large amounts of vaginal
aliphatic acids are produced by this species (Michael, unpublished results).
However, several aspects of behavior do differ in the two species. First, levels of
sexual activity with ovariectomized, untreated, wild-caught females were generally
considerably higher in M. fascicularis, and 1-2 ejaculations per test were quitc
common; thus, baselines were higher than in M. mulatta [Michael, 19681. Of course,
the copulatory pattern in this species appears to consist mainly of a single intromission [Shively et al, 1982; Zumpe & Michael, 19831, and when females were intact,
M. fascicularis males were more potent (more ejaculations per test) than M. mulatta
males. Second, as described above, the inhibitory effects of progesterone on behavior
were more marked in M. fascicularis. Third, treating ovariectomized rhesus females
with androgen usually does not increase male ejaculatory performance [Michael el
al, 1972; Michael & Zumpe, 19771, but in M. fascicularis both male mounting
attempts and ejaculations were increased. This could be because increased female
invitational behavior in this less sexualIy dimorphic species more effectively influences the male’s behavior. Fourth, male grooming times decreased and female
grooming times increased when sexual interactions increased, whereas rhesus males
tend to groom more when sexual interactions are high. Fifth, direct aggression by
male M. fascicularis was significantly higher when females were treated with
estrogen alone than during any other treatment condition, whereas male rhesus
monkeys show little direct aggression but high levels of redirected aggression with
estrogenized partners [Michael & Zumpe, 1970; Zumpe & Michael, 19791. Again,
these results are in good agreement with observations on intact M. fascicularis, in
which male aggression tended to be highest around midcycle.
Finally, treating ovariectomized females with 5 pg estradiol benzoate alone and
in combination with 5 mg progesterone produced plasma hormone levels in the
physiological range as judged by our own studies and by those of others [Goodman
et al, 1977; Goodman & Hodgen, 19791. The plasma hormone data should be helpful
in determining physiological dose-ranges for future experiments, and the observation that the same hormone doses gave different plasma hormone levels in different
animals is consistent with recent data from rhesus monkeys [Michael et al, 19841.
CONCLUSIONS
1. Administering estradiol benzoate, progesterone and testosterone propionate
to ovariectomized female M. fascicularis had highly significant effects on their
sexual, social, and aggressive interactions with male partners.
2. As in M. rnulntta, estradiol increased ejaculations and male and female
sexual motivation in M. fascicularis, while additional progesterone reversed these
effects.
3. In contrast to results in M. mulatta, treating M. fascicularis females with
large doses of testosterone increased ejaculatory activity, and M. fascicularis appeared to be more sensitive to the effects of progesterone than did M. mulatta.
4. Other differences between M. fascicularis and M. mulatta in their behavioral
responses to hormones confirm previous observations on intact females during the
menstrual cycle.
5. Thus, M.fascicularis is a suitable alternative to M. mulatta as a model for
investigating the neuroendocrine mechanisms underlying the behavior of higher
primates.
Hormones and Behavior in In. fasciculark I 181
ACKNOWLEDGMENTS
This w o r k was supported b y USPHS grant MH 19506, and general research
support was provided by the Georgia Department of Human Resources. Both are
gratefully acknowledged.
P r e l i m i n a r y data were presented at the IXth Congress of the International
Primatological Society, August 8-15,1982, in Atlanta, Georgia.
REFERENCES
Bonsall, R.W.; Baumgardner, D.G.; Michael,
R.P. A computerized semi-automated radioimmunoassay for plasma testosterone.
JOURNAL OF STEROID BIOCHEMISTRY 79353-858,1976.
Goodman, A.L.; Hodgen, G.D. Menstrual
cycle characteristics in chronically hemiovariectomized cynornolgus monkeys (Macucu fasciculuris). JOURNAL OF CLINICAL
ENDOCRINOLOGY
AND
METABOLISM 48:345-347,1979.
Goodman, A.L.; Descalzi, C.D.; Johnson,
D.K.; Hodgen, G.D. Composite patterns of
circulating LH, FSH, estradiol and progesterone during the menstrual cycle i n cynomolgus monkeys. PROCEEDINGS OF
THE SOCIETY FOR EXPERIMENTAL BIOLOGY AND MEDICINE 155:479-481,
1977.
Michael, R.P. Gonadal hormones and the control of primate behaviour, pp 69-93 in
ENDOCRINOLOGY OF HUMAN BEHAVIOUR. R.P. Michael, ed. Oxford University
Press, Oxford, 1968.
Michael, R.P.; Welegalla, J. Ovarian hormones and the sexual behaviour of the female rhesus monkey (Mucaca muluttu)
under laboratory conditions. JOURNAL OF
ENDOCRINOLOGY 41:407420,1968.
Michael, R.P.; Zumpe, D. Aggression and
gonadal hormones in captive rhesus monkeys (Mucacu rnulutta). ANIMAL BEHAVIOUR 18:1-10,1970.
Michael, R.P.; Zumpe, D. Effects of androgen
administration on sexual invitations by female rhesus monkeys (Mucucu muluttu).
ANIMAL BEHAVIOUR 25:936-944.1977.
Michael, R.P.; Bonsall, R.W.; Zumpe, D. The
behavioral thresholds of testosterone in castrated male rhesus monkeys (Mucaca muluttu). HORMONES AND BEHAVIOR
18:161-176,1984.
Michael, R.P.; Saayman, G.S.; Zumpe, D. The
suppression of mounting behaviour and ejaculation in male rhesus monkeys (Mucucu
rnuluttu)by administration of progesterone
to their female partners. JOURNAL OF
ENDOCRINOLOGY 41:421-431,1968.
Michael, R.P.; Zumpe, D.; Keverne, E.B.;
Bonsall, R.W. Neuroendocrine factors in the
control of primate behavior. RECENT
PROGRESS IN HORMONE RESEARCH
28:665-706, 1972.
Shively, C.; Clarke, S.; King, N.; Shapiro, S.;
Mitchell, G. Patterns of sexual behavior in
male macaques. AMERICAN JOURNAL
OF PRIMATOLOGY 2:373-384, 1982.
Siegel, S. NONPARAMETRIC STATISTICS
FOR THE BEHAVIORAL SCIENCES. New
York, McGraw-Hill, 1956.
Winer, B.J. STATISTICAL PRINCIPLES IN
EXPERIMENTAL DESIGN. New York,
McGraw-Hill, 1971.
Zumpe, D.; Michael, R.P. Relation between
the hormonal status of the female and di
rect and redirected aggression by male rhesus
monkeys
(Macucu
rnuluttu).
HORMONES AND BEHAVIOR 121269279,1979.
Zumpe, D.; Michael, R.P. A comparison of the
behavior of Mucam fiwciculuris and Mucucu
rnuluttu in relation to the menstrual cycle.
AMERICAN JOURNAL OF PRIMATOL
OGY 4:55-72, 1983.
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