Decrease in sexual initiative and responsiveness in female rhesus macaques (Macaca mulatta) during pregnancy.код для вставкиСкачать
American Journal of Primatology 2:301-306 (1982) BRIEF REPORT Decrease in Sexual Initiative and Responsiveness in Female Rhesus Macaques (Macaca mulafta) During Pregnancy K.C. CHAMBERS AND C.H.PHOENIX 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 INTRODUCTION 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  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. 302 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. METHODS 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. RESULTS 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 303 I.Or I .3 r 3r 1'1 - Prep PI Pz 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 < 0.05). 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. DISCUSSION 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 304 Chambers and Phoenix 1.2rT 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, 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  found an increased ejaculation frequency. Sexual Behavior in Pregnant Rhesus 305 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. CONCLUSIONS 1. The frequency of rejection of male copulation attempts increased when females were pregnant. 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. ACKNOWLEDGMENTS 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. REFERENCES Ball, J. Sexual responsiveness and temporally related physiological events duringpregnancy in the rhesus monkey. ANATOMICAL RECORD 67~507-512,1937. Ball, J . Effect of progesterone upon sexual excitability in the female monkey. PSYCHOLOGICAL BULLETIN 38:533, 1941. Baum, M.J.; Everitt, B.J.; Herbert, J.; Keverne, E.B.; de Greef, W.J. 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