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Decrease in sexual initiative and responsiveness in female rhesus macaques (Macaca mulatta) during pregnancy.

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American Journal of Primatology 2:301-306 (1982)
Decrease in Sexual Initiative and Responsiveness in
Female Rhesus Macaques (Macaca mulafta) During
Primate Behavior, Oregon Regional Primate Research Center, Beaverton
Although the sexual behavior of female rhesus macaques (Macacamulatta) has
been reported to decrease during pregnancy, systematic studies have been
largely confined to reports of male behavior. Therefore, we designed a study to
examine changes in female sexual behavior during pregnancy. Six cycling
multiparous female rhesus macaques were paired during the periovulatory
period of the menstrual cycle and during the first and second halves of pregnancy with six sexually experienced males of the same species. Each female
was paired with the same male in all tests. The means of the behavioral measures scored on days 11-13 of the menstrual cycle, 35-56 of pregnancy, and
147-168 of pregnancy were compared. Females showed a significant decrease
in the present:contact ratio and the rate of threat-aways during pregnancy.
Males showed lower rates of threatening-away, contacting, mounting, intromitting, and ejaculating when females were pregnant. The extent to which the
decrease in male sexual behavior can be accounted for by an increase in female
rejection is uncertain, but it is probably as significant as any loss of attractiveness that might accompany pregnancy.
Key words: pregnancy, proceptivity, receptivity, rhesus macaques, sexual behavior,
Macaca mulatta
Sexual activity during pregnancy has been observed in resus macaques both in the
field and in the laboratory [Conaway& Koford, 1965; Kaufman, 1965; Loy, 1971; Bielert
et al, 19761. Most sexual activity during pregnancy occurs between weeks 6 and 10;very
little activity occurs during the last half of pregnancy [Bielert et al, 19761. However,
sexual activity has been examined only in terms of mounting and ejaculation by the
male. Ball [1937] and Zumpe & Michael [197Oa] have studied female sexual invitations
during pregnancy, but inboth cases the observations were based on only one female.
Because there is a decline in male sexual activity, it might be inferred that there is a
decline in the sexual attractiveness of pregnant females. Even if true, it says little about
Received November 12, 1981; accepted December 5, 1981
Address reprint requests to Kathleen C. Chambers, Oregon Regional Primate Research Center, 505 N.W. 185th
Ave., Beaverton, OR 97006.
02752565/82/0203-0301$02.000 1982 Alan R. Liss, Inc.
Chambers and Phoenix
the receptivity or proceptivity of pregnant females. This study was undertaken to
compare the sexual behavior of females during the periovulatory period of the menstrual
cycle with their behavior during pregnancy. Because female behavior depends, at least
in part, on male behavior, the males’ responses were also considered.
The subjects were six multiparous female rhesus macaques (Macaca muhztta); five
were wild-born, and one was born and reared in the Primate Center animal colony. The
males were six adults of the same species: five were colony-bornand -reared, and one was
wild-born. All wild-born animals had been in the colony at least 3 yr. All monkeys were
part of a breeding program, and assignment to the program was based on established
fertility. Selection of individuals and assignment of partners were determined randomly.
Both females and males were housed in single cages in a light- and temperature-controlled room. Each pair was tested in the male’s home cage. At the time of testing, a partition was placed in the male’s cage to bisect it. The female was brought to the male’s
cage and was placed in the empty half. The partition was removed after approximately
30 s, a stopwatch was started, and the sexual and social behaviors of both females and
males were recorded. Tests lasted 30 min or until the male ejaculated. The behaviors
recorded were: present to contact, present a t a distance, invitation (hand-reach, headduck, and head-bob). contact, mount, intromission, ejaculation, threat-away, groom,
proximity response, jerk, threat, aggression, and grimace. ALI of these behaviors have
been defined elsewhere [Michael & Zumpe, 1970; Zumpe & Michael, 1970b; Phoenix,
1974;Chambers & Phoenix, in press]. A present:contact ratio (femalepresenkmale contacts), an index of female receptivity, was computed for each female. The ratio is similar
to the lordosis quotient widely used in estimating the receptivity of female rats. This
ratio includes only presents in response to a male contact; it does not include present at a
distance, a present in the absence of a contact. The frequencies of occurrence of other
behaviors were converted to rates (per min) since the test durations varied with the
latencies to ejaculation.
On days 11,12. and 13of the menstrual cycle, each female was paired with amale. Pregnancy was determined by means of rectopalpation 34 d after the first pairing date. If a
female was pregnant, the second pairing day was considered the day of conception. The
females were paired on the llth, 12th, and 13th d of each menstrual cycle untilimpregnation occurred. Four females became pregnant during the first menstrual cycle, one during the second, and one during the third. All females were paired with the same male in
all prepregnancy (Prep)and pregnancy tests. Each female was given eight tests while
pregnant. The tests were given on days 35, 42,49, 56, 147, 154, 161, and 168 of pregnancy. There is no evidence that such a test schedule alters performance.
The means of the behavioral measures scored for the six female-male pairs during the
three tests given when conception occurred, the four tests given during weeks 5-8 of
pregnancy (first half:Pl), and the four tests given during weeks 21-24 of pregnancy (second halfP2) were computed. A single-factor analysis of variance with repeated measures and the Newman-Keulstest were used to determine the significance of the differences in Prep, PI, and P2 behaviors.
The females showed a decrease in the present:contact ratio (F[2,10]= 75.08, P < 0.01)
and the rate of threat-aways (F[2,10]= 5.02, P < 0.05 [see Fig. 11).The present:contact
ratio was significantly higher in Prep tests than in both P1 and P2 tests (P < 0.01).The
ratio also was significantly higher during P1 tests than during P2 tests (P < 0.01).The
rate of threatening-away was significantly higher in Prep than in P2 tests (P < 0.05).
Sexual Behavior in Pregnant Rhesus
.3 r
Prep PI
Fig. 1. Thepresentmntact ratio and the threat-away, present at adistance (PAD),and invite rates (frequencies
per min) for females before pregnancy (Prep),during the first half of pregnancy (Pl),and during the second half of
pregnancy (El.(a) differs Significantly from Prep value ( P < 0.05). (b) differs significantly from P1 value (P <
There were no significant differences in the rates of presenting at a distance, inviting,
grimacing, grooming, proxing, jerking, threatening the partner, or aggressing.
The males showed higher rates of contacting (F[2,10] = 17.77), mounting (F[2,10] =
18.23), intromitting (F[2,10] = 13.32) (P < 0.01 in each case), and threatening-away
(F[2,10]= 4.72, P < 0.05) in Prep tests than in P1 and P2 tests (Fig. 2). The male rates of
contacting, mounting, and intromitting were significantly higher in Prep tests than in
P1 and P2 tests (P < 0.01 in each case).The male rates of threatening-away were significantly higher in Prep tests than in P2 tests (P < 0.05). There were no differences in rates
of grooming, proxing, jerking, threatening the partner, or aggression. Ejaculation
occurred in 17 of the 18 Prep tests. During 24 P1 tests there was only one ejaculation,
and during 24 P2 tests ejaculation did not occur.
Sexual receptivity decreased during pregnancy, i.e., there was a significant drop in the
present:contact ratio. The only form of proceptivity that dropped significantly during
pregnancy was threatening-away. Although we cannot present quantitative data, it was
our impression that most threat-aways during pregnancy occurred as the male approached the female and that this behavior altered the approach response of the male. A
slight modification of our recording procedure should allow us to determine if this impression is correct.
It is our opinion that because many females did not exhibit sexual solicitations (present at a distance and invitation) in Prep tests, we failed to find a statistically significant
Chambers and Phoenix
Fig. 2. The contact, mount, intromission, and threat-away rates (frequencies per min) for males tested with
females before pregnancy (F'reP).during the first half of pregnancy (Pl),and during the second half of pregnancy
(P2).(a)differs significantly from Prep value (P < 0.05). (b) differs significantly from P1 value (P < 0.05).
decrease in P1 and P2 tests; only half of the females presented at a distance, and only
one displayed invitations (hand-reaches, head-ducks, and head-bobs). For all four of
these females, however, the frequency of display of these behaviors was lower in P1 and
P2, an indication that any form of sexual solicitation a female exhibits when not pregnant she will display at a lower frequency when pregnant. Since, however, comparisons
of sexual activity during pregnancy were made with the periovulatory period of the
cycle our conclusions must of necessity be limited to comparisons of behavior observed
in that stage of the cycle.
The most likely explanation for the changes in female sexual behavior during pregnancy is the elevated levels of progesterone that accompany pregnancy. However, evidence for this explanation drawn from studies on the behavior of intact females and
ovariectomized females treated with exogenous estradiol and progesterone is inconsistent. Although some rhesus females displayed fewer invitations and more refusals during the luted phase of the menstrual cycle, when progesterone levels were high, other
females displayed no consistent pattern [Michael & Welegalla, 1968; Johnson &
Phoenix, 19781. Estrogen-primed rhesus females given daily injections of 1-2 mg or 25
mg of progesterone showed decreases in sexual excitability [Ball, 1941; Zumpe &
Michael, 1970a,b], but those given daily 10 mg injections showed inconsistent effects
and many even showed increases in invitations and continued acceptance of male
mounts [Zumpe & Michael, 1970a; Baum et al, 19761.
Our results agree with those of Bielert et al[1976], who reported that males displayed
fewer mounts and ejaculations when females were pregnant than when they were not.
We observed only one ejaculation in the P1 and P2 tests, and that occurred during the
stage of pregnancy (from week 6 to week 10) in which Bielert et a1 [1976] found an
increased ejaculation frequency.
Sexual Behavior in Pregnant Rhesus
We also found that male contact, intromission, and threat-away rates were lower with
pregnant females. Only one male failed to contact his female partner after she became
pregnant, but the others persisted in contacting their partners, although at a lower rate,
throughout pregnancy.
The decline in male invitations to copulate during the P1 and P2 tests was associated
with a significant increase in female refusals. Female refusals are simply the reciprocal
of the present:contact ratio, i.e., the lower the present:contact ratio the higher the female
refusals. Other physiological changes (e.g., odor [Michael & Keverne, 19681)in the pregnant females may have rendered them less attractive to the males, but there is no direct
evidence. In our study, five of the six males persisted in their attempts to mount their
pregnant partners. Thus, there is no compelling evidence that pregnant females are
unattractive to most males. I t remains to be demonstrated that the decline in sexual
behavior of males is not primarily a consequence of female rejection.
1. The frequency of rejection of male copulation attempts increased when females were
2. The frequencies of threatening-away, contacting, mounting, intromitting, and ej aculating decreased when males were paired with pregnant females.
3. At least part of the decrease in male sexual activity in tests with pregnant females
appeared to be due to an increase in female rejection.
The work described in this article, Publication No. 1199 of the Oregon Regional Primate Research Center, was supported by grants AG-01608 and RR-00163 from the
National Institutes of Health. U.S. Public Health Service.
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pregnancy, decrease, responsiveness, macaque, rhesus, sexual, female, mulatta, macaca, initiative
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