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Determinants of behavioral rhythmicity during artificial menstrual cycles in rhesus monkeys (Macaca mulatta).

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American Journal of Primatology 15:157-170 (1988)
Determinants of Behavioral Rhythmicity During Artificial
Menstrual Cycles in Rhesus Monkeys (Macaca mulatta)
RICHARD P. MICHAEL AND DORIS ZUMPE
Department of Psychiatry, Emory University School of Medicine and The Georgia Mental
Health Institute, Atlanta
Reproductive success in many mammals depends on synchrony between
copulation and ovulation, which is insured by the phenomenon of heat in
the female. Certain anthropoid primates including rhesus monkeys do not
show heat but may copulate throughout the menstrual cycle, especially
when pairs are isolated from conspecifics. In social groups, however,
mating mostly occurs around midcycle. We wished to test the hypothesis
that copulations are more closely linked to ovulation when males have
simultaneous access to several females in different cycle phases. Artificial
menstrual cycles were therefore induced by giving hormones to ovariectomized female rhesus monkeys observed in small social groups that each
consisted of four females and one male. The cycles of two hormone-treated
females in each group were either made to synchronize or be offset by
7-day increments so that the estradiol peak of one female occurred 7 days
before, and 7 and 14 days after, the estradiol peak of the other. Radioimmunoassay of plasma samples (N = 224) confirmed the timing of the
estradiol peaks. Results from eight unique male-female groups (4 males,
8 females, 16 male-female pairs, 718 tests) fully supported the hypothesis.
Compared with synchronized cycles, the amplitudes of rhythmic changes
in offset cycles were reduced for ejaculations made by males but greatly
enhanced for ejaculations received by females. We propose that this
socio-hormonalintegration of behavior in the group is highly adaptive and
enhances the reproductive success of both males and females.
Key words: menstrual cycle, hormones, behavioral rhythms, mate choice
INTRODUCTION
In mammals, the reproductive success of both males and females depends
heavily on synchrony between the timing of ovulation and maximum copulatory
activity. From a reproductive and genetic standpoint, copulations occurring during
unfertile phases of the ovarian cycle are simply wasted. Mechanisms that prevent
this wastage therefore have enormous adaptive significance, and the familiar heat
behavior of many female mammals is one such mechanism.
Rhesus monkeys, like several other primates including the human, do not
Received September 21, 1987; revision accepted January 31, 1988.
Address reprint requests to Dr. Richard P. Michael, Department of Psychiatry, Emory University School
of Medicine, 1256 Briarcliff Road, N.E., Atlanta, GA 30306.
0 1988 Alan R. Liss, Inc.
158 I Michael and Zumpe
show heat but can copulate throughout the entire menstrual cycle. Fertility is
confined to a period of a few days near midcycle when plasma estradiol levels peak
and are followed 24-48 hours later by ovulation [Norman et al., 1976; Ferin et al.,
1977; Knobil, 19831. Earlier field studies reported that rhesus monkeys live in
semi-closed social groups containing several adult males and females with their
young. It was noted that mating occurred seasonally during the fall, and that there
was a monthly periodicity in female mating activity [Carpenter, 1942; Altmann,
1962; Kaufmann, 1965; Southwick et al., 1965; Lindburg, 19711. In laboratory
studies, the length of the menstrual cycle was determined [Hartman, 19321, as
were the associated hormonal events [Hess & Resko, 1973; Knobil, 1974; Bonsall
et al., 19781. Studies in observation cages with male-female pairs established that
frequencies of copulatory activity increased a t midcycle and that gonadal hormones determined this increase [Michael et al., 1967, 1968; Michael & Welegalla,
1968; Johnson & Phoenix, 1976; Wallen & Goy, 19771. There was much variability
in the behavior. In some pairs, rhythmic changes were well marked, while in
others they were virtually absent. As more data accumulated, however, the
species-typical pattern gradually emerged [Michael & Zumpe, 1970a; Michael &
Bonsall, 19771. The amplitudes of the rhythms of copulatory activity in pair tests
were much less marked than those in feral social groups and in large outdoor
enclosures [Wilson et al., 19821, although seasonal influences can modulate the
amplitude of changes [Herndon et al., 19871.
Most copulations occur in the context of temporary but exclusive consortships,
during which a male and female remain in close proximity; feeding, grooming, and
copulating together. There is reason to suppose that consortships during unfertile
periods involve not only the wastage of copulations but also energetic and
nutritional costs [Hausfater, 1975; Dittus, 1979; Bercovitch, 19831. In certain
macaques and baboons, for example, consorting males spend more time in
aggressive interactions, and consorting females spend less time feeding. A mechanism insuring that consortships are restricted to periods of maximum fertility is
therefore likely to be highly adaptive for these species. Because of the differential
between the sexes in gamete production and investment in offspring, evolutionary
theory [Darwin, 1871; Williams, 1966; Trivers, 19721 predicts that male rhesus
monkeys will attempt to maximize reproductive success by maintaining a stable,
high level of copulatory activity with as many mates as possible throughout the
mating season. On the other hand, females would be expected to copulate
exclusively during periods of maximum fertility. In pair tests conducted in the
absence of other conspecifics, a mix of the opposing tendencies of males toward
constancy and of females toward periodicity would result in only moderately
rhythmic mating activity. In a social context when other females are present, as
long as their menstrual cycles are not synchronized, one would predict the
continuously active male to mate with several females in succession as each one
approaches midcycle, moving from female to female as the previous partner enters
the luteal phase. This would result in high, constant levels of male copulatory
activity (total numbers of ejaculations given by males) and high-amplitude
rhythms of female copulatory activity (ejaculations received by females). The
pattern of change would depend on the precise timing of one female’s menstrual
cycle in relation to those of others in the group.
This hypothesis cannot be tested under natural conditions because there is no
practical or reliable way to regulate the timing and length of menstrual cycles in
the wild. We have developed an “artificial” menstrual cycle in ovariectomized
females [Michael et al., 19781that enabled us to test these predictions experimentally under rigorously controlled conditions. With the advent of specific radioim-
Behavioral Cycles in Rhesus Monkeys I 159
munoassays, we now have detailed information about the plasma levels of the
principal ovarian hormones as they change during the menstrual cycles of intact
females. It is possible to reproduce these changes accurately with daily subcutaneous injections of a changing mixture of different doses of estradiol benzoate,
progesterone, and testosterone propionate [Michael et al., 19821. Ovariectomized
females so treated have 28-day cycles that are terminated by 1-2 days of vaginal
bleeding indistinguishable from normal menstruation; animals have the typical
midcycle change in basal body temperature, and the anterior pituitary gland
responds to the fluctuations in circulating plasma hormone levels by producing a
pulse of luteinizing hormone that resembles the ovulatory pulse of intact females.
The behavioral changes seen in pair tests conducted during these cycles are
virtually identical to those observed when the same animals were intact [Michael
et al., 19821. We have used these hormonally induced artificial menstrual cycles in
small groups of rhesus monkeys, consisting of one male and four ovariectomized
females, to examine the behavioral effects of varying the timing of one female's
cycle in relation to that of another female in the group.
MATERIALS AND METHODS
Animals
Four mature male (weighing 9.2-11.3 kg) and eight adult female (weighing
4.6-5.9 kg) rhesus monkeys were obtained as adults from the wild. Animals were
housed in individual cages in large colony rooms where temperature was maintained between 20-24 "C and artificial lighting gave a 14-hour day between 06:15
and 20:15 hours. Food consisted of Purina Monkey Chow, supplemented by
vitamins, fresh fruit, and vegetables, and water was available ad libitum. General
maintenance procedures have been previously described [Zumpe & Michael, 19771.
All experimental procedures were in accordance with institutional regulations and
with the NIH Guide for the Care and Use of Laboratory Animals (NIH Publication
Number 85-23, revised 1985).
Operative Procedures and Hormone Treatments
Six months before the start of behavioral observations, all females were
ovariectomized bilaterally through a midline subumbilical incision, and histological examination confirmed that ovariectomy was complete. In each of two groups
of four females (females A-D, females E-H), two females (females A and B, females
E and F) were given eight artificial menstrual cycles produced by daily subcutaneous injections of a changing mixture of steroids in 0.2 ml oil. Each injection was
given a t 08:OO hours and contained estradiol benzoate (pg), testosterone propionate
(pg), and progesterone (mg) as shown in Table I. This dose schedule was slightly
modified from that published previously [Michael et al., 19821 to replicate more
accurately the plasma hormone levels of intact females. Day 1 was always a
Saturday so that all estradiol peaks (day 12) occurred on Wednesdays. Cycles were
offset by treating one of the two females with daily subcutaneous injections of 5 pg
estradiol benzoate for the offset interval (7 or 14 days). The two other females in
each group (females C and D, females G and H) received daily subcutaneous
injections of 0.2 ml oil throughout.
Collection of Plasma Samples and Steroid Assays
Once daily during days 10-15 (Monday through Friday) and three times a
week a t all other times (Mondays, Wednesdays, and Fridays), 3 ml blood was
obtained from the saphenous veins of the untranquilized, hormone-treated females
160 / Michael and Zumpe
TABLE I. Doses of Steroids Administered in Daily Subcutaneous Injections of 0.2 ml
Oil to Produce Artificial Menstrual Cycles in Ovariectomized Female Rhesus Monkeys
Cycle
Days
1-7
8-9
10
11
12
13
14
15
16
17
18-19
20-21
22
23-24
25
26
27
28
Estradiol
benzoate
Testosterone
propionate
(Fd
(FLR)
Progesterone
(md
5.0
7.5
10.0
17.5
30.0
2.5
2.5
2.5
2.5
5.0
5.0
5.0
5.0
5.0
2.5
2.5
5.0
5.0
14.0
14.0
14.0
17.5
25.0
5.0
7.5
10.0
10.0
10.0
10.0
10.0
10.0
10.0
10.0
14.0
14.0
14.0
0.00
0 .oo
0.00
0.00
0.20
0.30
0.30
0.75
1.oo
1.00
1.25
1.50
1.25
0.75
0.75
0.50
0.20
0.00
that previously had been adapted to the procedure. Blood samples from oil-treated
females were obtained once a week (Wednesdays). All samples were collected at
16:OO hours, 8 hours after injection. To verify the timing of the midcycle estradiol
peaks in hormone-treated females, samples from alternate cycles were analyzed for
plasma estradiol levels by radioimmunoassay without chromatography, using a
highly specific antiserum [Wright et al., 19781. Inter- and intra-assay coefficients
of variation were less than 8.4%, and water blanks read 6.7 ? 3.6 pg (224 samples).
Behavioral Testing
In the period 1983-1986, 1-hour behavior tests (N = 718) were conducted
twice daily 5 days a week with groups, each consisting of one male and four
females. Two tests are not included in the total: one because of computer
malfunction and one because of injury. Testing took place in a large room (4.9 m
wide by 4.9 m deep by 2.1 m high) where animals were observed from behind a
partition. Behavioral observations were made by nine experienced observers who
were assigned tests in random order and unaware of the compositions of the
hormone injections, which were numerically coded. TRS Model 100 computers
were used to record all behavioral interactions and the identities of the animals
involved, and interactions were timed to the nearest second from the start of the
test [Bonsall et al., 19853. A group of four females (females A-D) was tested with
each of the four males (males 1-4) in turn during successive tests: with males 1
and 2 (morning and afternoon, respectively) on one test day, and with males 3 and
4 (morning and afternoon, respectively) on the next. Two successive test days
therefore provided data from a 1-hour behavior test with each of four unique
male-female groups, and each 28-day artificial cycle produced data from ten tests
with each of these four male-female groups. At the conclusion of these tests, the
entire study was repeated using the same four males and a second group of females
Behavioral Cycles in Rhesus Monkeys / 161
(females E-H), thus providing data from a total of 16 male-female pairs with
artificial cycles in eight uniquely composed male-female groups.
Cycle Offsetting
To assess the behaviorial impact of varying the timing of the cycle of one
female relative to that of the other hormone-treated female in the group, their
estradiol peaks were either synchronized (zero offset) or offset by 7-day increments
so that the estradiol peak of one female occurred 7 days before (-7 offset), 7 days
after ( + 7 offset), and 14 days after (A14 offset) the estradiol peak of the other.
After a period of testing to permit acclimatization and behavioral stabilization, the
following sequence provided data for 2 cycles per offset per female: 1) two
successive cycles in which the estradiol peak of female A coincided with day 19 of
the cycle of female B (-7 offset for female A and + 7 offset for female B); 2) one
synchronized cycle (zero offset);3) two successive cycles in which the estradiol peak
of female A coincided with day 5 of the cycle of female B ( + 7 offset for female A and
-7 offset for female B); 4) one synchonized cycle (zero offset); and 5) two successive
cycles in which the estradiol peak of female A coincided with day 26 of the cycle of
female B and vice versa ( + 14 offset for female A and - 14 offset for female B). This
sequence was repeated with females E and F in the second group of females.
Behavioral Definitions
Twelve behavioral categories were used: 1) number of ejaculations made by a
male-the total number of ejaculations per test made by a male with all females,
2) number of ejaculations received by each female, 3) time to first ejaculationtime in seconds from the start of the test to the first ejaculation received by each
female (a default of 3,600 seconds was given when a female received no ejaculations), 4) number of male mounting attempts-number of successful and unsuccessful male mounting attempts received by each female, 5 ) latency to the first
male mounting a t t e m p t t i m e in seconds from the start of the test to the first male
mounting attempt received by each female, 6) number of male redirected aggressive gestures [Zumpe & Michael, 1970,19791 received by each female-threats and
attacks by a male at other females or nothing in particular while in proximity
(within touching distance) with the female, 7) number of female sexual invitations-total number of presents, hand-reaches, head-ducks, and head-bobs [Michael & Zumpe, 1970bl made by each female to the male, 8) number of redirected
aggressive gestures by each female-threats and attacks by a female a t other
females or nothing in particular while in proximity with the male, 9) number of
approaches by a male received by each female-number of times a male approached to within touching distance of a female, 10) number of approaches by
each female received by a male-number of times a female approached to within
touching distance of the male, 11)time spent in proximity-time in seconds when
a male and female were within touching distance, 12) time spent allogroomingtime in seconds spent by a male and female grooming each other.
Numerical Treatment of Results
The behavior of an individual can be considered in terms of all other
individuals in the group together or in terms of each individual singly. Thus, a
male’s copulations can be considered as the number of ejaculations made with all
four females or as ejaculations made with each of the four females individually
(male-female pair). To test the hypothesis, a comparison of these two very different
behavioral measures was made. For brevity, other behaviors are reported only in
166 I Michael and Zumpe
SYNCHRONIZED
- 7 OFFSET
+7
OFFSET
f 14 OFFSET
4
?
h
4
2
4
ru
P
?
I
s
Fig. 4., For latencies to the first ejaculation and first mounting attempt received by females, and for proximity
times, offsetting the cycles of two females in a group greatly increased the amplitudes of changes in these
behavioral measures of consort bonding. Each point is the mean of 30-32 observations. Upward arrows indicate
the timing of the estradiol peaks of the females whose data are illustrated and downward arrows indicate those
of the other females. Symbols a s in Figure 1.
or artificial cycles [Michael et al., 19821. Beyond this, the enhancement of the
rhythms in female mating activity in the presence of other females depended on
the interaction between the hormonal status of the female herself and that of the
other hormone-treated female in the group. Taken together with the male's
tendendency toward relatively stable levels of mating activity, this interaction
produced well-marked periods of maximum sexual activity in each female, periods
that would be further accentuated in a more complex social setting involving
several cycling females.
Offsetting the cycles affected other measures of behavior that are involved in
the formation and maintenance of consortships. Latencies to the first ejaculation
and to the first male mounting attempt received by females, as well as numbers of
mounting attempts, redirected aggressive gestures, approaches and grooming
times, all became more rhythmic during offset cycles. A word about Proximity
times which were completely nonrhythmic in synchronized cycles. This observation confirmed an earlier finding that proximity times did not change with
hormone treatments of the female [Michael & Zumpe, 19841. The reasons for this
somewhat surprising finding are complex but depend on an overriding effect of
partner preferences, which create strong social bonds throughout the cycle and
tend to mask any effects of changes in sexual motivation on proximity times. In
offset cycles, social bonding was overridden by changes in sexual preference, and
proximity times became highly rhythmic.
Behavioral Cycles in Rhesus Monkeys / 163
- 7 OFFSET
SYNCHRONIZED
i 14 OFFSET
+ 7 OFFSET
4
0
J
I
r
d
I
7
14
21
28
1
7
14
21
28
I
7
14
21
28
1
7
I
4
21
28
DAYS OF ARTIFICIAL CYCLE
Fig. 1. Changes in the numbers of ejaculations per test made by a male with both hormone-treated females in
a group of rhesus monkeys (four males, eight male-female groups). In synchronized cycles, ejaculatory activity
by males showed moderately rhythmic changes, but behavioral rhythmicity was virtually lost when cycles were
offset. Downward arrows indicate the timing of the estradiol peaks of females A and E and upward arrows
indicate those of females B and F. Each point is the mean of 14-16 tests. Vertical bars give S.E.M.S. Solid
squares indicate vaginal bleeding.
Ejaculations Made by Males
None of the males ejaculated with oil-treated females, whose data are not
considered further. Figure 1shows changes in the numbers of ejaculations made by
males with all hormone-treated females during synchronized cycles and during
each of the three types of offset cycles. In synchronized cycles, ejaculations showed
rhythmic changes, with a peak on days 13-14 and low levels between days 19-28.
Differences between cycle phases were significant (ANOVA,cycle segment x male
design, F[9,1201 = 2.8, P = 0.005). In offset cycles, ejaculations showed no
consistent rhythmic changes, and differences between cycle segments were not
significant except for the -7 offset (F[9,1191 = 3.1, P = 0.002), in which the first
peak (days 7-10) was higher than levels a t midcycle.
Ejaculations Received by Females
For each test there is one male but two hormone-treated females, and a + 7 or
+ 14 offset for one female is inevitably a -7 or -14 offset for the other. The number
of ejaculations received by each female can be aligned according to the female’s
estradiol peaks, which determine the offset intervals. In Figure 2, each point is the
mean of 14-16 observations (2 artificial cycles per female, two females, four males
in eight groups), and the data show the effect of cycle offsets on the ejaculations
received by each of the hormone-treated females in a group. In synchronized cycles,
ejaculations received by both females were only moderately rhythmic, and there
were no significant differences between cycle phases (cycle segment x male
design, F[9,1201 = 0.6 and 0.2, N.S.).However, during all offset cycles, the
amplitudes of the changes in the numbers of ejaculations received by both females
were massively increased, and cycle phases differed significantly in each case
(F[9,119-1201 = 2.3-7.3, P < 0.02-0.0001). Compared with synchronized cycles,
the midcycle peaks in offset cycles were higher when they coincided with the early
(-7 offset) or late (k14 offset) progestational phase of the other female, whose
copulatory activity was coincidentally lower. The exact pattern of change depended on the phase difference between cycles.
164 I Michael and Zumpe
:
SYNCHRONIZED
+7
OFFSET
- 7 OFFSET
+ 14 OFFSET
1-1
F:
SYNCHRONIZED
- 7 OFFSET
+ 7 OFFSET
-
u-•
FEMALES A 0 E
FEMALES B
n
14 OFFSET
4
I
c
I
I
I
7
14
21
28
I
7
14
21
28
I
7
14
21
28
I
7
14
21
28
DAYS OF ARTIFICIAL CYCLE
Fig. 2. Changes in the numbers of ejaculations per test received by each of the two hormone-treated females
in a group (four females, eight male-female groups). The amplitudes of rhythms were massively increased when
cycles were offset. Compared with synchronized cycles, females received more ejaculations during days 13-14
when these coincided with either days 19-20 or days 27-28 of the other female whose mating activity was
coincidentally decreased. Each point is the mean of 14-16 tests. Symbols as in Figure 1.
A two-way ANOVA comparing the data from females A and E with those from
females B and F showed no significant differences between them during synchronized cycles or any of the offset cycles (females x cycle segment design,
F[1,297-3001 = 0.0-2.5, N.S.), and also confirmed the analyses described above,
namely, that the differences between cycle phases were significant in -7, + 7, and
214 offsets (F[9,297-3001 = 3.8-10.4, P < 0.0001) but were not significant in
synchronized cycles (F[9,3001 = 1.4, N.S.). Data from all four females were
therefore combined in Figure 3, where each point is the mean of 30-32 observations. Figure 3 also shows the corresponding changes in plasma estradiol levels.
The enhancement of the behavioral rhythms that resulted from offsetting the
cycles becomes very obvious. ANOVAs using a cycle segment x male x female
design showed that there were no significant differences in the combined data
between cycle phases in synchronized cycles (F[9,3041 = 1.7, N.S.) but that there
were highly significant differences in offset cycles (F[9,301-304] = 5.6-15.1, P <
O.OOOl), confirming the previous analyses.
Other Measures of Sexual and Social Behavior
Many other behavioral measures (for which we have the data) could be given
the extended analysis accorded ejaculatory activity. But in the present context we
have chosen to illustrate just three additional measures, which are particularly
interesting and show dramatically increased rhythmicity during offset cycles (Fig.
4). In view of the rhythms in the numbers of ejaculations received by females
during offset cycles, it was not surprising that there were similar rhythms (but
opposite in direction) in times to first ejaculation received by females (upper
panel). The time to the first male mounting attempt received by females (middle
panel) may be regarded as a measure of male sexual motivation, and this time
showed changes that were almost identical to times to first ejaculation. Proximity
times (lower panel), a measure of consort bonding, only showed rhythms when
cycles were offset, and these resembled those in ejaculations received by females.
Behavioral Cycles in Rhesus Monkeys I 165
- 7 OCFSET
SYNCHRONIZED
I
7
14
21
28
I
7
14
21
+7
28
I
DAYS OF ARTIFICIAL
*x
Plasma estrodlol levels of Illustrated female
7
OFFSET
14
21
f 14 OFFSET
28
I
7
14
21
28
CYCLE
x----n Plorma rrtradlol levels of othu female
Fig. 3. Upper part: combined data for numbers of ejaculations received by females showed that the pattern of
change depended on both the hormonal status of the female herself and on the timing of the estradiol peak of the
other hormone-treated female in the group. Each point is the mean of 30-32 observations.Lower part: shows the
timing of the plasma estradiol peaks in these females. Each point is the mean of four plasma samples. Symbols
as in Figure 1.
There were significant differences between offsets for all 11measures of social and
sexual interactions between males and females shown in Table 11. ANOVAs using
a cycle segment x male x female design for each type of offset showed that the
amplitudes of almost all the behavioral changes were greater during offset than
during synchronized cycles. Differences between cycle phases were significant for
4 of 11 measures during synchronized cycles, but for 7 measures in -7 offsets, 8
measures in 7 offsets, and 10 measures in 214 offsets.
+
DISCUSSION
If it is accepted that the artificial cycle is an adequate and valid model for the
natural cycle, these results fully supported the hypothesis that, when given the
opportunity, male rhesus monkeys will maintain stable levels of ejaculatory
activity, whereas females will mate most frequently 24-48 hours after the
estradiol peak a t the time of ovulation. During synchronized cycles, both the level
of and pattern of change in ejaculations made by males were closely similar to
those reported previously [Michael & Zumpe, 1970al for intact females in pair tests
(Fig. 5), which, incidentally, gave a further behavioral validation of the artificial
cycle. Ejaculations made by males were less rhythmic in offset cycles than in
synchronized cycles, whereas the amplitudes of changes in ejaculations received by
females were dramatically increased. Hormonal factors were clearly causal because in every case the maxima (minima for latency measures) followed the
estradiol peak by 1-2 days. This was in good agreement with earlier studies on
pairs in which females were undergoing either natural [Michael & Bonsall, 19771
166 I Michael and Zumpe
SYNCHRONIZED
- 7 OFFSET
+7
OFFSET
f 14 OFFSET
4
?
h
4
2
4
ru
P
?
I
s
Fig. 4., For latencies to the first ejaculation and first mounting attempt received by females, and for proximity
times, offsetting the cycles of two females in a group greatly increased the amplitudes of changes in these
behavioral measures of consort bonding. Each point is the mean of 30-32 observations. Upward arrows indicate
the timing of the estradiol peaks of the females whose data are illustrated and downward arrows indicate those
of the other females. Symbols a s in Figure 1.
or artificial cycles [Michael et al., 19821. Beyond this, the enhancement of the
rhythms in female mating activity in the presence of other females depended on
the interaction between the hormonal status of the female herself and that of the
other hormone-treated female in the group. Taken together with the male's
tendendency toward relatively stable levels of mating activity, this interaction
produced well-marked periods of maximum sexual activity in each female, periods
that would be further accentuated in a more complex social setting involving
several cycling females.
Offsetting the cycles affected other measures of behavior that are involved in
the formation and maintenance of consortships. Latencies to the first ejaculation
and to the first male mounting attempt received by females, as well as numbers of
mounting attempts, redirected aggressive gestures, approaches and grooming
times, all became more rhythmic during offset cycles. A word about Proximity
times which were completely nonrhythmic in synchronized cycles. This observation confirmed an earlier finding that proximity times did not change with
hormone treatments of the female [Michael & Zumpe, 19841. The reasons for this
somewhat surprising finding are complex but depend on an overriding effect of
partner preferences, which create strong social bonds throughout the cycle and
tend to mask any effects of changes in sexual motivation on proximity times. In
offset cycles, social bonding was overridden by changes in sexual preference, and
proximity times became highly rhythmic.
"Significantly different from zero offset.
Number of ejaculations
received by female
Time to first ejaculation
received by female (seconds)
Number of mounting attempts
received by female
Time to first mounting attempt
received by female (seconds)
Number of redirected aggressive
gestures made by male
Number of sexual invitations
made by female
Number of redirected aggressive
gestures made by female
Number of approaches by
male to female
Number of approaches by
female to male
Time spent in
proximity (seconds)
Time spent
allogrooming
- (seconds)
3.36 2 0.24
1136 C 54
6.75 ? 0.32
1588 5 76
4.19 5 0.45
2.12 2 0.25"
3.58 2 0.48
* 0.20
3.34
2.95 5 0.17
1184 i 51
779 t 45
6.55 t 0.33
1632 t 75
3.74 t 0.40
1.33 5 0.13
2.55 -+ 0.32
3.56 t 0.23
2.86 2 0.18
1263 -+ 52
881 t 45
* 0.32"
828 2 48
3.34 2 3.20
f 0.19"
1029 ? 53"
1358 ? 60
2.15
2.50 +- 0.16"
1.81 2 0.20
* 0.41
3.16
1.47 t 0.22
11.99
6.43
10.23
8.40
5.04
4.16
3.78
4.92
* 0.47
6.09
7.59
* 0.31"
5.00
7.48
F(3,1238)
1973 2 81"
5.37
2341 5 73
0.78 f 0.04
14 Offset
N = 320
Mean -+ S.E.
-t
1.66 ? 0.18
3.29 i 0.32
1863 C 79
5.78
2400 i 72
2104 2 70
0.70 2 0.04
2205 t 68
0.04"
N = 318
Mean ? S.E.
+ 7 Offset
0.92
2
- 7 Offset
N = 317
Mean -+ S.E.
0.79 -+ 0.40
Zero Offset
N = 320
Mean -+ S.E.
0.0001
0.0001
0.0001
0.0001
0.002
0.006
0.01
0.0001
0.0001
0.002
0.0001
P
Significance
of differences
between offsets
TABLE 11. Comparisons of Levels of Behavior During Synchronized and Offset Artificial Menstrual Cycles in
Female Rhesus Monkeys Observed in Small Social Groups (ANOVAs, Offset b y Male b y Female Design f o r All
T y p e s of Cycles Combined)
168 I Michael and Zumpe
I
7
14
21
26
DAYS OF CYCLE
0-0
0-0
Group tests: synchronized artificial cycles
Pair tests: natural cycles (Michael 8 Zumpe, 1970)
Fig. 5. Both the levels of, and patterns of change in, numbers of ejaculations made by males in group
tests during synchronized artificial cycles were closely similar to those in pair tests during natural cycles
with intact females [Michael & Zumpe,197OaJ.Group tests, N = 14-16. Pair tests, N = 46-60. Symbols
as in Figure 1.
The experimental design controlled for differences in levels of behavior
between animals, in partner preferences, and in dominance rank, and also
minimized the effects of long-term testing, although all these factors contributed to
the variance. Wallen & Winston [1984] reported that in a social setting the
amplitudes of behavioral rhythms of intact females were greater, while levels of
behavior were lower, than those in a pair setting. No distinction was made between
the behavior of the male with the experimental female and his behavior with all
females in the group, which are quite different entities in a social context. The
inference, that mating in a group situation requires substantially greater hormonal stimulation, received no support from the present study in which the
hormonal and social variables could be well-controlled. We take a different view,
namely, that the presence of other females in different cycle phases greatly
enhances the behavioral effects brought about by changes in the individual’s own
plasma hormone levels. This sociohormonal integration of behavior is likely to be
highly adaptive by ensuring the mating success of both the males and females in
a social group. The data imply that effects of ovarian hormones on human sexual
activity, notoriously difficult to document in Western societies, might best be found
in cultures where polygynous mating systems are acceptable and the male has the
opportunity to select between females in different phases of the menstrual cycle.
CONCLUSIONS
1. In rhesus monkeys, the rhythms of female mating activity that are associated
with changing levels of ovarian hormones during the menstrual cycle are massively
enhanced by the presence of other females in different phases of the cycle.
2. This is a consequence both of the varying hormonal status of females and of
the male’s tendency to maintain his mating activity at a stable level by changing
sexual partners so as to consort with each female in turn as she nears midcycle.
3. This sociohormonal integration of behavior is a highly adaptive phenomenon that ensures that mating by both males and females is largely confined t o
periods of maximum fertility.
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.
Behavioral Cycles in Rhesus Monkeys / 169
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