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Proceptive patterns of behavior throughout the menstrual cycle in female rhesus monkeys
B E H A V I O R A L A N D N E U R A L BIOLOGY
27, 342-353 (1979)
Proceptive Patterns of Behavior throughout the Menstrual Cycle in Female Rhesus Monkeys CAROL G.
COCHRAN 1
Yerkes Regional Primate Research Center, Atlanta, Georgia 30322 The reproductive behavior of captive female rhesus monkeys living in a large social group was examined to determine what patterns of proceptive behavior occur and how they are distributed throughout the menstrual cycle. Ten intact adult females and six vasectomized adult males were observed during the breeding season. The males were housed separately overnight and released into the social group for a 4-hr observation period. The female menstrual cycles were monitored by daily capture for vaginal swabbing. A total of 18 cycles in which females showed estrous behavior between intervals of menstruation were observed for nine females between October 4 and February 4. A composite of all the cycles revealed a significant rise in proceptive behavior during the follicular period culminating in a midcycle peak, with an abrupt cessation of female sexual invitations during the early luteal period. The specific patterns of proceptive behavior observed consisted primarily of female-initiated proximity and following of males. Solicitation patterns such as sexual presentation, hand slap, head bob/duck, and threat out were displayed to a lesser extent. Overall, these data suggest that underlying endocrine events strongly influence the behavior of female rhesus monkeys living in a complex social environment and that social factors such as dominance rank do not appear to override these hormonal variables.
The cyclic occurrence of sexual activity during the annual breeding season of free-ranging rhesus monkeys (Macaca mulatta) has been widely reported (Altmann, 1962; Carpenter, 1942; Conaway & Koford, 1964; Kaufmann, 1965; Southwick, Beg, & Siddiqi, 1965). Duration of these "estrous" periods is approximately 8-11 days (Kaufmann, 1965; Loy, 1971; Southwick et al., 1965). Estrus has generally been identified by increased incidence of copulation, formation of consort pairs, and increased heterosexual grooming (Altmann, 1962; Carpenter, 1942; Loy, 1971). Other changes in social interactions between males and females 1 This research was supported by NIMH Grant MH-20483 and by NIH Grant RR-00165. The study was in partial fulfillment of requirements for the degree of Doctor of Philosophy at the University of Georgia, Athens, Ga. I am grateful to Dr. Irwin S. Bernstein and Thomas P. Gordon for their helpful comments and suggestions. 342 0163-1047/79/110342-12502.00/0 Copyright © 1979 by Academic Press, Inc. All rights of reproduction in any form reserved.
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such as following and seeking proximity to each other have also been observed (Carpenter, 1942). Similar periodicity of reproductive behavior has been recorded in the laboratory. Although copulations may occur throughout the menstrual cycle of female rhesus monkeys, the frequency of copulations generally increases during the follicular phase, reaching a peak around the expected time of ovulation, and progressively declines during the luteal phase (Ball & Hartman, 1935; Goy & Resko, 1972; Michael, Herbert, & Welegalla, 1967a). This pattern, however, is not consistent among all individuals tested in a laboratory setting (Ball & Hartman, 1935; Michael & Welegalla, 1968). Since the copulatory sequence is due to a complex of interactions between male and female, the distinction between attractiveness and receptivity has been valuable in discriminating their respective roles (Herbert & Trimble, 1967; Michael, Saayman, & Zumpe, 1967b). Female attractiveness is inferred by the male's sexual behavior presumably in response to either peripheral or behavioral cues emanating from the female. Sexual receptivity, which in a general sense is a measure of the female's willingness to engage in copulation, encompasses Beach's (1976) concepts of proceptivity and receptivity. Proceptive behavior by the female consists of active behavior in response to stimuli received from the male and is expressed as sexual invitations or solicitations. Receptivity involves acceptance of male copulatory attempts such as assumption of postures which facilitate mounting and intromission. Although field researchers have not defined a distinction between attractiveness and receptivity, they have described components of both when referring to the behavior of estrous females and the social interactions in which they participate. Carpenter's (1942) description of estrous females showing affinitive approaches and gestures toward males indicates that females actively sought copulation with a male and were thus proceptive. The various patterns of female sexual invitations have been found by laboratory investigators to fluctuate with different stages of the menstrual cycle (Ball & Hartman, 1935; Czaja & Bielert, 1975; Goy & Resko, 1972; Keverne, 1976). However, Rowell (1963) and Czaja and Bielert (1975) did not observe an increase in presentations while Michael and Welegalla (1968) even noted a midcycle depression in presenting. In any regard, presentations per se do not always serve as sexual invitations and often occur in other social contexts (Rowell, 1972). Cyclic variation of proceptive behavioral responses is likely to reflect the well-documented patterns of endocrine events occurring during the female rhesus menstrual cycle. The various patterns of female invitations which can occur in large social groups of rhesus monkeys have not been identified. Furthermore, the cyclicity of their occurrence in direct relation
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to menses has not been reliabily measured in the social context. A captive social group living in a large outdoor enclosure was therefore deemed to be appropriate for investigation of patterns of proceptive behavior during the breeding season since some manipulation was possible with minimal disruption of social relations among individuals. Such a study was conducted to see specifically what patterns of proceptive behavior can be observed in group living, adult female rhesus monkeys and to examine their mode of distribution in relation to the females' menstrual cycles. METHODS
Subjects Ten intact adult female rhesus monkeys and six vasectomized adult males living in a social group of 35 animals were the subjects of this study. The group was formed 2 years previously with the exception of two adult males which were introduced 2 months prior to the study. The remaining composition of the group consisted mostly of previous offspring or younger siblings of the adult females. The group was maintained in a 38.1-m square outdoor enclosure with adjoining indoor quarters. The indoor quarters (3.1 x 9.3 x 2.6 m) were designed to provide shelter and facilitate capture and handling. The animals were able to enter an enclosed capture area (5 x 1.1 x 2.6 m) through a swinging door to the outdoor compound. Six individual cages located in an office area adjacent to the indoor quarters were used to house the males overnight. Standard monkey chow and water were continuously available with daily supplement of fresh fruits and vegetables.
Procedure Since seasonal breeding females are often impregnated during their first ovulatory cycle of the season (Conaway & Koford, 1964; Gordon, personal communication), the six adult males were vasectomized in August, 2 months prior to the predicted start of the breeding season in order to allow repeated cycling by the females. One week later, four of the adult males were reintroduced into the group while two of the males were introduced for the first time. All subjects were trained for capture and adapted to handling. The six males were housed overnight in the individual cages and were allowed daily access to the females during a 4-hr observation period. Behavioral data were recorded from a vantage point overlooking the entire compound. This entailed an initial 30-min group scan followed by 10 focal animal samples, terminating with a 1-hr group scan. Focal animal samples concentrated upon a single individual at a time and concerned behavioral interactions involving the focal animal. Group scans entailed observation of the entire group and scoring behavioral responses involv-
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ing interactions between males and any of the adult female subjects. Each day following the observation period, the females were captured and transferred individually to the restraining cage for daily vaginal swabbing and venipuncture for selected hormonal assays. Swabbing consisted of insertion of a moistened cotton swab into the vagina to check for the presence of menses. The above schedule was followed initially 5 days a week, then 7 days a week from October 31 when the first female showed intense sexual activity including copulation. More than 380 hr of behavioral observations were made over the 4-month period between October 4 and February 4, 1977. Selected blood serum samples were assayed for progesterone in order to confirm the presence of functional corpora lutea and thus ovulatory cycles.
Behavioral Definitions Patterns of proceptive behavior referred to as "invitational behavior" were defined as those responses which increase the likelihood of being mounted. The following response categories by females towards males (summarized in Table 1) were scored. Proximity. Reduction of interindividual distance to the male by at least 50%. Following. Female walks behind, stopping and starting as the male does. A subcategory of sexual invitations involved patterns of behavior which were more closely associated with initiation of copulatory behavior. These are referred to as solicitations and include the following: Hand slap. Rapid lifting and extending of the arm, slapping ground as hand is replaced, termed "hand reach" by Michael and Zumpe (1970) and "spasmodic arm reflex" by Carpenter (1942). Head bob/duck. Vertical movement of the head relative to the shoulders. Threat out. Female opens mouth and stares at any animal within vicinity, sometimes with vocalization, while repeatedly glancing back at male, referred to as "threaten away" (Altmann, 1962; Czaja & Bielert, 1975). Presentation (sexual or nonsexual). Orientation of the perineum toward the male often with slight leg flexion and tail elevated with a head turn toward the male. Male sexual and social responses directed toward the females were also recorded. The definitions of the following are included in Table 1: sex invite; male-initiated proximity; following; sniff; hip touch; mounts; and ejaculation. Agonistic behavior involving adult females and males was noted principally to confirm dominance relationships. Dominance relationships were determined by the outcome of agonistic interactions.
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CAROL G. COCHRAN TABLE 1 C ~ e g o ~ of Definitions Female proceptive
Male sexual
Presentation--orientation of hindquarters toward the male, with tail slightly raised, often leg flexion, and head turned toward the male. Hand slatr----rapid lifting and extending hand and arm, slapping ground as hand is replaced. Head bob/duck--vertical rapid movement of head. Threat out female close to male, opens mouth and stares at any animal within vicinity while repeatedly glancing at male. Proximity--reduction of at least 50% of interindividual distance. Following--walks behind or shadows another, stopping and starting at same time.
Sex invite---exaggerated prancing gait by male, face often with wide grin, teeth showing oriented toward female. Hip touch--(grab waist) places hands on hips or waist of female. aMount--foot clasping of female's ankles with grab waist. aIntromission--penile insertion. aEjaculation--semen ejaculation.
a Components of copulation.
Data Analysis The frequencies of female sexual behavior including the various patterns of solicitations, proximity, following, and sexual presentations were computed for each day across different phases of the menstrual cycle. The day of the cycle was determined by counting backward from the first day of menses for 28 days. All cycles by each of the female subjects were pooled to form a composite cycle which was then divided into three portions. The "follicular" portion encompassed the first 9 days of the cycle; the second portion labeled "periovulatory" included the following 9 days of the cycle; the remaining 10 days were labeled "luteal." The differences in frequencies of female proceptive behavior across the cycle were tested by determining the percentage of hourly rates above and below the grand mean for each day and performing a one-way analysis of variance. RESULTS
Throughout the study, 9 of the 10 females showed evidence of cyclicity in which females showed periods of intense sexual activity between intervals of menstruation. Although the 10th female who was older than most eventually cycled, this occurred after the period of data collection had terminated. Since some females began menstruating, though irregularly, prior to the onset of ovulatory cycles, behavioral criteria were also
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used to define at least initial cycles. Onset of intense sexual activity which included at least two copulations or marked increase in female invitations was the defining characteristic. A total of 18 cycles were observed among the nine females and their distribution is shown in Fig. 1. Progesterone levels were examined and were found to be ovulatory in at least 12 of these. Mean cycle length was 28.9 days _+ 3.6 SE.
Patterns of Proceptive Behavior The predominant pattern of invitational behavior displayed by all females during both focal and scan observations was initiation of proximity to the male. This pattern constituted 60% of all proceptive patterns and therefore occurred significantly more often than any of the other patterns combined [X2(1) = 427, p < .001]. Twenty-two percent consisted of following, and 6% of the proceptive patterns were sexual presentations. The remaining 12% consisted of various solicitations including hand slap, head bob/duck, threat out, or crouch. Patterns of solicitation were differentially displayed by the females. Even for those females which showed the highest number of solicitations, these never exceeded 28% of the females' total repertoire of invitational behavior. The highest percentage of any single pattern was shown by female Mf where 20.4% of all invitational patterns displayed by this female consisted of the hand slap pattern. Therefore, sexual solicitations constituted a small proportion of all proceptive behavior. At the onset of the breeding season a qualitative difference between presentations in sexual versus nonsexual contexts was observed in this study. The presentation posture assumed by the females in a sexual context appeared to differ from the classically defined posture in which O¢-
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FIG. 1. females.
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Distribution of peak days of sexual behavior during 18 menstrual cycles by nine
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the female stands upright with the tail arching upward in that sexual presentations generally involved greater leg flexion and tail elevation at a lower level, often with a head turn toward the male. Since these distinctions were in part context dependent, a post facto analysis of preseasonal versus inseasonal occurrence of sexual versus nonsexual presentations (based on postural differences) revealed that prior to the season nonsexual presentations were seen almost exclusively. Only one sexual presentation was seen before the onset of cyclicity. Furthermore, nearly 95% of the nonsexual presenting was directed toward the alpha male, thus providing evidence for its probable social context. A comparison of preseasonal frequencies with a comparable period during the breeding season showed that the incidence of nonsexual presentations significantly decreased from preseasonal levels [X~(1) = 37.7; p < .01]. The increase in sexual presentations from preseasonal levels to inseasonal levels was also significant [ X2(1) = 84.2, p < .01], although there was an overall increase in presentations. A posture wherein the female sits with her back to the male, previously recorded by Wallen & Goy (1977) was also found to occur in the context of sexual solicitation. Although this posture, referred to as the precopulatory posture, was not a predefined measure and therefore not quantified, it was observed during intense periods of sexual activity throughout the study. Additionally, females which generally showed high levels of invitational behavior displayed the precopulatory posture more often, even when the males did not respond with mounting activity. Distribution across Menstrual Cycle
Mean hourly rates of female proceptive behavior for each of the nine females composed a 28-day composite cycle. Division of this composite cycle into follicular, periovulatory, and luteal portions revealed significant differences in percentages of hourly rates of behavior above and below the grand mean (5.98) by a one-way ANOVA, F(2,25) = 32.5, p < .01 (Table 2). As expected, follicular and luteal portions of the cycle contained significantly lower mean hourly rates than the periovulatory portion. The luteal portion, characterized by the lowest levels of proceptive behavior, was also significantly lower than the follicular portion. The composite of mean hourly rates of invitational behavior across all 18 cycles recorded for the nine females also revealed a similar pattern as shown in Fig. 2. This was most apparent for the individual cycles by the females. The larger variance during the peak period was due to individual differences in onset and cessation of proceptive behavior. Overall, however, the females showed a discernible rise during the follicular phase which declined during the early luteal phase of the 28-day menstrual cycle. Although the composite cycles demonstrated a clear pattern of be-
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P R O C E P T I V E B E H A V I O R IN R H E S U S F E M A L E S TABLE 2 Invitational Behavior of Nine Females across the Menstrual Cycle (Mean Hourly Rate _+ SE) ~ Interval Follicular* Day of cycle
Periovulatory c Day of cycle
Mean ± SE
1 2 3 4 5 6 7 8 9
2.33 3.08 3.61 4.85 2.41 3.08 8.25 8.72 8.67
+- 1.3 -+ 2.6 ± 2.1 ± 3.5 --- 0.8 ± 2.1 ± 9.8 ± 5.2 ± 5.4
10 I1 12 13 14 15 16 17 18
Mean ± SE 11.89 16.14 13.24 16.11 9.90 11.93 8.74 8.08 4.63
--- 10.7 -+ 6.7 ± 5.4 -+ 6.4 ± 6.0 +-- 12.7 ± 13.6 ± 2.14 ± 7.1
Luteal a Day of cycle 19 20 21 22 23 24 25 26 27 28
Mean ± SE 2.13 1.20 1.32 1.13 0.83 1.27 0.53 1.11 1.68 2.11
± 0.88 ± 0.22 --- 0.29 ± 0.36 ± 0.06 +-- 0.28 ± 0.11 ± 0.12 ± 0.39 ± 1.08
a Grand mean = 5.98; F(2,25) = 32.5;p < .01. b ~ , 5.0. c )T = 11.18. a .~ = 1.33.
havioral cyclicity, one female, Nf, during two of her four cycles exhibited sexual behavior during all portions of the cycle including frequent and regular copulations. This particular female, however, did display a midcycle proceptive peak, but showed greater variation in distribution of her sexual invitations. Three females, Ah, Hf, Nf, demonstrated perimenstrual elevations of proceptive behavior in 5 of the 18 cycles 18"
IS 12z
9 6
lie
2
4
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$ 10 12 14 16 18 20 22 24 26 28 M DAY OF CYC LE
FIG. 2. Composite of 18 cycles by nine females of mean hourly rates of female invitations per cycle day across a 28-day menstrual cycle. Standard error (SE) is s h o w n in one direction. Day 28 is 1 day prior to menses (M) for all cycles.
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observed, but only female Nf engaged in copulatory series during menstruation. The dominance rank of the females did not seem to influence the expression of female sexual invitations. A Spearman rank order correlation between mean hourly rates of proceptive behavior per cycle day for each female and the social rank of the female was nonsignificant, rs = 0.12. DISCUSSION Sexual invitations by female rhesus monkeys consisting of defined behavioral patterns, appear to reflect underlying endocrine events during the menstrual cycle. Despite the complexity of social interactions occurring in a group of the composition in this study, the hormonal state of the females strongly influenced expressions of sexually motivated behavior. Not only did females initiate sexual solicitations toward males during a discrete period within their cycles, but the behavior of the males in the form of invitations and copulatory patterns also changed in response to either behavioral or physiological cues from the females. This finding is in general agreement with both laboratory (Michael & Welegalla, 1968) and field studies (Altmann, 1962; Carpenter, 1942; Kaufmann, 1965). The results in this study, however, run contrary to observations by Rowell (1963) that rhesus females in captive social groups show little behavioral cyclicity. The discrepancy between this study and that of Rowell (1963) may have been due to the different composition and housing which perhaps involved frequent disruption of the groups. In Rowell's study, rhesus females lived in groups of three or four with one male housed in outdoor runs. This contrasts greatly with the complexity of the multiple male group in the present study which consisted of a matriarchal organization including siblings and offspring. In view of Rowell's (1972) contention that "with further complication of the social situation one may speculate whether the cyclic effect might be submerged entirely" (p. 80), the data from this investigation indicate that underlying hormonal variables are correlated with the cyclic behavior of female rhesus monkeys more so in the complex than in the simpler setting. All nine of the females exhibited at least some amount of proceptive behavior regardless of social rank. This was not found to be the case for female pigtail macaques (Macaca nemestrina) in laboratory multiphased triads composed of one female in the follicular, another in the preovulatory, and a third in the midluteal phase of the menstrual cycle (Goldfoot, 1971). The lowest ranking females of the triads which were in the preovulatory stage of the cycle inhibited their sexual solicitations in the presence of higher ranking females. In the present study, not only did all the rhesus females display proceptive behavior, but there was no correlation between female social rank and frequency in the solicitation of males.
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It is not surprising that some perimenstrual elevation in invitational behavior was observed in three females since Loy (1970) has reported the occurrence of "peri-menstrual estrus" in free-ranging rhesus females and Czaja and Bielert (1975) also observed its occurrence under laboratory conditions. Nevertheless, it must be emphasized that these elevations did not approach the levels exhibited during midcycle, with the exception of the two cycles of female Nf in which she showed high levels of proceptive behavior through a large portion of these cycles. The patterns of invitational behavior, defined prior to the study, appeared to be a general indication of female sexual motivation as evidenced by their temporal occurrence which was coincident with increases in mounting and ejaculation (to be reported in a subsequent paper). All the females exhibited proximity, following, and sexual presentations, while various individuals displayed one or more of the other solicitation patterns such as hand slap, head bob/duck, threat out, and crouch. Given that presentations are observed in other social contexts, it is not surprising that the occurrence of presentations does not necessarily fluctuate with various stages of the menstrual cycle (Czaja & Bielert, 1975; Rowell, 1963). However, in view of the observations indicating differences between sexual and nonsexual presentations, this suggests that the presentation pattern could represent two responses which are distinguishable. Further investigation of these possible differences should be pursued under more controlled experimental conditions. Observations of the precopulatory posture indicate that this pattern serves as a sexual solicitation. This posture may be just a particular position assumed by the female, but it often appeared during a copulatory series or just prior to a series. Furthermore, Wallen and Goy (1977) have found testosterone and estrogens to increase its incidence. Female-initiated proximity and following of a male occurred far more frequently than patterns of solicitation. These patterns per se do not always serve as sexual invitations, but may occur in other social contexts. Nevertheless, the increase in seeking proximity and following males is quite dramatic when a female is cycling. Additionally, Czaja and Bielert (1975) have also noted that females spent maximum time in proximity to a restrained male around the ovulatory period. Perhaps the discrepancy in frequency of occurrence between proximity and following and the other solicitation patterns is that they serve different functions. Proximity and following serve to place the females in close physical relationship with the male so that copulation is more likely, while hand slap, threat out, etc., may function in maintaining copulatory behavior, or more specifically to initiate mounting. For example, it was incidentally observed that females showing low levels of proceptive behavior, primarily proximity and following, often ceased exhibiting any further patterns once they had engaged a male in copulatory activity.
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These females may not have needed to initiate or maintain copulatory mounts with sexual invitations. On the other hand, they might have passively maintained male copulatory behavior by remaining in proximity or in the precopulatory posture. The distinction in function between gaining access to males and initiating mounts should be examined further in large social groups since the availability of multiple potential mates as well as ample space may be essential to the display of these reproductive strategies. REFERENCES Altmann, S. A. (1962). A held study of sociobiology of rhesus monkeys, Macaca mulatta. Annals of the New York Academy of Science, 102, 181-514. Ball, J., & Hartman, C. G. (1935). Sexual excitability as related to the menstrual cycle in the monkey. American Journal of Obstetrics and Gynecology, 29, 117-119. Beach, F. A. (1976). Sexual attractivity, proceptivity, and receptivity in female mammals. Hormones and Behavior, 7, 105-138. Carpenter, C. R. (1942). Sexual behavior of free-ranging rhesus monkeys (Macaca mulatta). Journal of Computational Physics, 33, 113-142. Conaway, C. H., & Koford, C. B. (1964). Estrous cycles and mating behavior in a free ranging band of rhesus monkeys. Journal of Mammalogy, 45, 557-587. Czaja, J. A., & Bielert, C. (1975). Female rhesus sexual behavior and distance to a male partner: Relation to stage of the menstrual cycle. Archives of Sexual Behavior, 4, 583-596. Goldfoot, D. A. (1971) Hormonal and social determinants of sexual behavior in the pigtail monkey (Macaca nemestrina). In G. B. A. Stoelinga and J. J. van der Werff ten Bosch (Eds.), Normal and Abnormal Development of Brain and Behavior, pp. 325-341. Leiden: Leiden Press. Goy, R. W., & Resko, J. A. (1972). Gonadal hormones and behavior of normal and pseudohermaphroditic nonhuman female primates. Record of Progress in Hormone Research, 28, 707-732. Herbert, J., & Trimble, M. R. (1967). Effect of estradiol and testosterone on the sexual receptivity and attractiveness of the female rhesus monkey. Nature (London), 216, 165-166. Kaufmann, J. H. (1965). A three-year study of mating behavior in a free ranging band of rhesus monkeys. Ecology, 46, 500-512. Keverne, E. B. (1976). Sexual receptivity and attractiveness in the female rhesus monkey. Advances in the Study of Behavior, 7, 155-200. Loy, J. (1970). Peri-menstrual sexual behavior among rhesus monkeys. Folia Primatologica, 13, 286-297. Loy, J. (1971). Estrous behavior of free-ranging rhesus monkeys (Macaca mulatta). Primates, 12, 1-31. Michael, R. P., & Welegalla, J. (1968). Ovarian hormones and sexual behavior of the female rhesus monkey (Macaca mulatta) under laboratory conditions. Journal of Endocrinology, 41, 407-420. Michael, R. P., & Zumpe, D. (1970). Sexual initiating behavior by female rhesus monkeys (Macaca mulatta) under laboratory conditions. Behaviour, 173, 168-185. Michael, R. P., Herbert, J., & Welegalla, J. (1967). Ovarian hormones and the sexual behaviour of the male rhesus monkey (Macaca mulatta) under laboratory conditions. Journal of Endocrinology 39, 81-98. (a) Michael, R. P., Saayman, G. S., & Zumpe, D. (1967). Sexual attractiveness and receptivity in rhesus monkeys, Nature (London), 215, 554-556. (b)
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Rowell, T. E. (1963). Behavior and female reproductive cycles of rhesus macaques. Journal of Reproductive Fertility, 6, 193-207. Rowell, T. E. (1972). Female reproductive cycles and social behavior in primates. Advances in the Study of Behavior, 4, 69-105. Southwick, C. H., Beg, M. A., & Siddiqi, M. R. (1965). Rhesus monkeys in North India. In I. De Vore (Ed.), Primate Behavior, pp. 111-159. New York: Holt. Wallen, K., & Goy, R. W. (1977). Effects of estradiol benzoate, estrone, and propionates of testosterone or dihydrotestosterone on sexual and related behaviors of ovariectomized rhesus monkeys. Hormones and Behavior, 9, 228-248.
27, 342-353 (1979)
Proceptive Patterns of Behavior throughout the Menstrual Cycle in Female Rhesus Monkeys CAROL G.
COCHRAN 1
Yerkes Regional Primate Research Center, Atlanta, Georgia 30322 The reproductive behavior of captive female rhesus monkeys living in a large social group was examined to determine what patterns of proceptive behavior occur and how they are distributed throughout the menstrual cycle. Ten intact adult females and six vasectomized adult males were observed during the breeding season. The males were housed separately overnight and released into the social group for a 4-hr observation period. The female menstrual cycles were monitored by daily capture for vaginal swabbing. A total of 18 cycles in which females showed estrous behavior between intervals of menstruation were observed for nine females between October 4 and February 4. A composite of all the cycles revealed a significant rise in proceptive behavior during the follicular period culminating in a midcycle peak, with an abrupt cessation of female sexual invitations during the early luteal period. The specific patterns of proceptive behavior observed consisted primarily of female-initiated proximity and following of males. Solicitation patterns such as sexual presentation, hand slap, head bob/duck, and threat out were displayed to a lesser extent. Overall, these data suggest that underlying endocrine events strongly influence the behavior of female rhesus monkeys living in a complex social environment and that social factors such as dominance rank do not appear to override these hormonal variables.
The cyclic occurrence of sexual activity during the annual breeding season of free-ranging rhesus monkeys (Macaca mulatta) has been widely reported (Altmann, 1962; Carpenter, 1942; Conaway & Koford, 1964; Kaufmann, 1965; Southwick, Beg, & Siddiqi, 1965). Duration of these "estrous" periods is approximately 8-11 days (Kaufmann, 1965; Loy, 1971; Southwick et al., 1965). Estrus has generally been identified by increased incidence of copulation, formation of consort pairs, and increased heterosexual grooming (Altmann, 1962; Carpenter, 1942; Loy, 1971). Other changes in social interactions between males and females 1 This research was supported by NIMH Grant MH-20483 and by NIH Grant RR-00165. The study was in partial fulfillment of requirements for the degree of Doctor of Philosophy at the University of Georgia, Athens, Ga. I am grateful to Dr. Irwin S. Bernstein and Thomas P. Gordon for their helpful comments and suggestions. 342 0163-1047/79/110342-12502.00/0 Copyright © 1979 by Academic Press, Inc. All rights of reproduction in any form reserved.
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such as following and seeking proximity to each other have also been observed (Carpenter, 1942). Similar periodicity of reproductive behavior has been recorded in the laboratory. Although copulations may occur throughout the menstrual cycle of female rhesus monkeys, the frequency of copulations generally increases during the follicular phase, reaching a peak around the expected time of ovulation, and progressively declines during the luteal phase (Ball & Hartman, 1935; Goy & Resko, 1972; Michael, Herbert, & Welegalla, 1967a). This pattern, however, is not consistent among all individuals tested in a laboratory setting (Ball & Hartman, 1935; Michael & Welegalla, 1968). Since the copulatory sequence is due to a complex of interactions between male and female, the distinction between attractiveness and receptivity has been valuable in discriminating their respective roles (Herbert & Trimble, 1967; Michael, Saayman, & Zumpe, 1967b). Female attractiveness is inferred by the male's sexual behavior presumably in response to either peripheral or behavioral cues emanating from the female. Sexual receptivity, which in a general sense is a measure of the female's willingness to engage in copulation, encompasses Beach's (1976) concepts of proceptivity and receptivity. Proceptive behavior by the female consists of active behavior in response to stimuli received from the male and is expressed as sexual invitations or solicitations. Receptivity involves acceptance of male copulatory attempts such as assumption of postures which facilitate mounting and intromission. Although field researchers have not defined a distinction between attractiveness and receptivity, they have described components of both when referring to the behavior of estrous females and the social interactions in which they participate. Carpenter's (1942) description of estrous females showing affinitive approaches and gestures toward males indicates that females actively sought copulation with a male and were thus proceptive. The various patterns of female sexual invitations have been found by laboratory investigators to fluctuate with different stages of the menstrual cycle (Ball & Hartman, 1935; Czaja & Bielert, 1975; Goy & Resko, 1972; Keverne, 1976). However, Rowell (1963) and Czaja and Bielert (1975) did not observe an increase in presentations while Michael and Welegalla (1968) even noted a midcycle depression in presenting. In any regard, presentations per se do not always serve as sexual invitations and often occur in other social contexts (Rowell, 1972). Cyclic variation of proceptive behavioral responses is likely to reflect the well-documented patterns of endocrine events occurring during the female rhesus menstrual cycle. The various patterns of female invitations which can occur in large social groups of rhesus monkeys have not been identified. Furthermore, the cyclicity of their occurrence in direct relation
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to menses has not been reliabily measured in the social context. A captive social group living in a large outdoor enclosure was therefore deemed to be appropriate for investigation of patterns of proceptive behavior during the breeding season since some manipulation was possible with minimal disruption of social relations among individuals. Such a study was conducted to see specifically what patterns of proceptive behavior can be observed in group living, adult female rhesus monkeys and to examine their mode of distribution in relation to the females' menstrual cycles. METHODS
Subjects Ten intact adult female rhesus monkeys and six vasectomized adult males living in a social group of 35 animals were the subjects of this study. The group was formed 2 years previously with the exception of two adult males which were introduced 2 months prior to the study. The remaining composition of the group consisted mostly of previous offspring or younger siblings of the adult females. The group was maintained in a 38.1-m square outdoor enclosure with adjoining indoor quarters. The indoor quarters (3.1 x 9.3 x 2.6 m) were designed to provide shelter and facilitate capture and handling. The animals were able to enter an enclosed capture area (5 x 1.1 x 2.6 m) through a swinging door to the outdoor compound. Six individual cages located in an office area adjacent to the indoor quarters were used to house the males overnight. Standard monkey chow and water were continuously available with daily supplement of fresh fruits and vegetables.
Procedure Since seasonal breeding females are often impregnated during their first ovulatory cycle of the season (Conaway & Koford, 1964; Gordon, personal communication), the six adult males were vasectomized in August, 2 months prior to the predicted start of the breeding season in order to allow repeated cycling by the females. One week later, four of the adult males were reintroduced into the group while two of the males were introduced for the first time. All subjects were trained for capture and adapted to handling. The six males were housed overnight in the individual cages and were allowed daily access to the females during a 4-hr observation period. Behavioral data were recorded from a vantage point overlooking the entire compound. This entailed an initial 30-min group scan followed by 10 focal animal samples, terminating with a 1-hr group scan. Focal animal samples concentrated upon a single individual at a time and concerned behavioral interactions involving the focal animal. Group scans entailed observation of the entire group and scoring behavioral responses involv-
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ing interactions between males and any of the adult female subjects. Each day following the observation period, the females were captured and transferred individually to the restraining cage for daily vaginal swabbing and venipuncture for selected hormonal assays. Swabbing consisted of insertion of a moistened cotton swab into the vagina to check for the presence of menses. The above schedule was followed initially 5 days a week, then 7 days a week from October 31 when the first female showed intense sexual activity including copulation. More than 380 hr of behavioral observations were made over the 4-month period between October 4 and February 4, 1977. Selected blood serum samples were assayed for progesterone in order to confirm the presence of functional corpora lutea and thus ovulatory cycles.
Behavioral Definitions Patterns of proceptive behavior referred to as "invitational behavior" were defined as those responses which increase the likelihood of being mounted. The following response categories by females towards males (summarized in Table 1) were scored. Proximity. Reduction of interindividual distance to the male by at least 50%. Following. Female walks behind, stopping and starting as the male does. A subcategory of sexual invitations involved patterns of behavior which were more closely associated with initiation of copulatory behavior. These are referred to as solicitations and include the following: Hand slap. Rapid lifting and extending of the arm, slapping ground as hand is replaced, termed "hand reach" by Michael and Zumpe (1970) and "spasmodic arm reflex" by Carpenter (1942). Head bob/duck. Vertical movement of the head relative to the shoulders. Threat out. Female opens mouth and stares at any animal within vicinity, sometimes with vocalization, while repeatedly glancing back at male, referred to as "threaten away" (Altmann, 1962; Czaja & Bielert, 1975). Presentation (sexual or nonsexual). Orientation of the perineum toward the male often with slight leg flexion and tail elevated with a head turn toward the male. Male sexual and social responses directed toward the females were also recorded. The definitions of the following are included in Table 1: sex invite; male-initiated proximity; following; sniff; hip touch; mounts; and ejaculation. Agonistic behavior involving adult females and males was noted principally to confirm dominance relationships. Dominance relationships were determined by the outcome of agonistic interactions.
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CAROL G. COCHRAN TABLE 1 C ~ e g o ~ of Definitions Female proceptive
Male sexual
Presentation--orientation of hindquarters toward the male, with tail slightly raised, often leg flexion, and head turned toward the male. Hand slatr----rapid lifting and extending hand and arm, slapping ground as hand is replaced. Head bob/duck--vertical rapid movement of head. Threat out female close to male, opens mouth and stares at any animal within vicinity while repeatedly glancing at male. Proximity--reduction of at least 50% of interindividual distance. Following--walks behind or shadows another, stopping and starting at same time.
Sex invite---exaggerated prancing gait by male, face often with wide grin, teeth showing oriented toward female. Hip touch--(grab waist) places hands on hips or waist of female. aMount--foot clasping of female's ankles with grab waist. aIntromission--penile insertion. aEjaculation--semen ejaculation.
a Components of copulation.
Data Analysis The frequencies of female sexual behavior including the various patterns of solicitations, proximity, following, and sexual presentations were computed for each day across different phases of the menstrual cycle. The day of the cycle was determined by counting backward from the first day of menses for 28 days. All cycles by each of the female subjects were pooled to form a composite cycle which was then divided into three portions. The "follicular" portion encompassed the first 9 days of the cycle; the second portion labeled "periovulatory" included the following 9 days of the cycle; the remaining 10 days were labeled "luteal." The differences in frequencies of female proceptive behavior across the cycle were tested by determining the percentage of hourly rates above and below the grand mean for each day and performing a one-way analysis of variance. RESULTS
Throughout the study, 9 of the 10 females showed evidence of cyclicity in which females showed periods of intense sexual activity between intervals of menstruation. Although the 10th female who was older than most eventually cycled, this occurred after the period of data collection had terminated. Since some females began menstruating, though irregularly, prior to the onset of ovulatory cycles, behavioral criteria were also
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used to define at least initial cycles. Onset of intense sexual activity which included at least two copulations or marked increase in female invitations was the defining characteristic. A total of 18 cycles were observed among the nine females and their distribution is shown in Fig. 1. Progesterone levels were examined and were found to be ovulatory in at least 12 of these. Mean cycle length was 28.9 days _+ 3.6 SE.
Patterns of Proceptive Behavior The predominant pattern of invitational behavior displayed by all females during both focal and scan observations was initiation of proximity to the male. This pattern constituted 60% of all proceptive patterns and therefore occurred significantly more often than any of the other patterns combined [X2(1) = 427, p < .001]. Twenty-two percent consisted of following, and 6% of the proceptive patterns were sexual presentations. The remaining 12% consisted of various solicitations including hand slap, head bob/duck, threat out, or crouch. Patterns of solicitation were differentially displayed by the females. Even for those females which showed the highest number of solicitations, these never exceeded 28% of the females' total repertoire of invitational behavior. The highest percentage of any single pattern was shown by female Mf where 20.4% of all invitational patterns displayed by this female consisted of the hand slap pattern. Therefore, sexual solicitations constituted a small proportion of all proceptive behavior. At the onset of the breeding season a qualitative difference between presentations in sexual versus nonsexual contexts was observed in this study. The presentation posture assumed by the females in a sexual context appeared to differ from the classically defined posture in which O¢-
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Distribution of peak days of sexual behavior during 18 menstrual cycles by nine
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the female stands upright with the tail arching upward in that sexual presentations generally involved greater leg flexion and tail elevation at a lower level, often with a head turn toward the male. Since these distinctions were in part context dependent, a post facto analysis of preseasonal versus inseasonal occurrence of sexual versus nonsexual presentations (based on postural differences) revealed that prior to the season nonsexual presentations were seen almost exclusively. Only one sexual presentation was seen before the onset of cyclicity. Furthermore, nearly 95% of the nonsexual presenting was directed toward the alpha male, thus providing evidence for its probable social context. A comparison of preseasonal frequencies with a comparable period during the breeding season showed that the incidence of nonsexual presentations significantly decreased from preseasonal levels [X~(1) = 37.7; p < .01]. The increase in sexual presentations from preseasonal levels to inseasonal levels was also significant [ X2(1) = 84.2, p < .01], although there was an overall increase in presentations. A posture wherein the female sits with her back to the male, previously recorded by Wallen & Goy (1977) was also found to occur in the context of sexual solicitation. Although this posture, referred to as the precopulatory posture, was not a predefined measure and therefore not quantified, it was observed during intense periods of sexual activity throughout the study. Additionally, females which generally showed high levels of invitational behavior displayed the precopulatory posture more often, even when the males did not respond with mounting activity. Distribution across Menstrual Cycle
Mean hourly rates of female proceptive behavior for each of the nine females composed a 28-day composite cycle. Division of this composite cycle into follicular, periovulatory, and luteal portions revealed significant differences in percentages of hourly rates of behavior above and below the grand mean (5.98) by a one-way ANOVA, F(2,25) = 32.5, p < .01 (Table 2). As expected, follicular and luteal portions of the cycle contained significantly lower mean hourly rates than the periovulatory portion. The luteal portion, characterized by the lowest levels of proceptive behavior, was also significantly lower than the follicular portion. The composite of mean hourly rates of invitational behavior across all 18 cycles recorded for the nine females also revealed a similar pattern as shown in Fig. 2. This was most apparent for the individual cycles by the females. The larger variance during the peak period was due to individual differences in onset and cessation of proceptive behavior. Overall, however, the females showed a discernible rise during the follicular phase which declined during the early luteal phase of the 28-day menstrual cycle. Although the composite cycles demonstrated a clear pattern of be-
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P R O C E P T I V E B E H A V I O R IN R H E S U S F E M A L E S TABLE 2 Invitational Behavior of Nine Females across the Menstrual Cycle (Mean Hourly Rate _+ SE) ~ Interval Follicular* Day of cycle
Periovulatory c Day of cycle
Mean ± SE
1 2 3 4 5 6 7 8 9
2.33 3.08 3.61 4.85 2.41 3.08 8.25 8.72 8.67
+- 1.3 -+ 2.6 ± 2.1 ± 3.5 --- 0.8 ± 2.1 ± 9.8 ± 5.2 ± 5.4
10 I1 12 13 14 15 16 17 18
Mean ± SE 11.89 16.14 13.24 16.11 9.90 11.93 8.74 8.08 4.63
--- 10.7 -+ 6.7 ± 5.4 -+ 6.4 ± 6.0 +-- 12.7 ± 13.6 ± 2.14 ± 7.1
Luteal a Day of cycle 19 20 21 22 23 24 25 26 27 28
Mean ± SE 2.13 1.20 1.32 1.13 0.83 1.27 0.53 1.11 1.68 2.11
± 0.88 ± 0.22 --- 0.29 ± 0.36 ± 0.06 +-- 0.28 ± 0.11 ± 0.12 ± 0.39 ± 1.08
a Grand mean = 5.98; F(2,25) = 32.5;p < .01. b ~ , 5.0. c )T = 11.18. a .~ = 1.33.
havioral cyclicity, one female, Nf, during two of her four cycles exhibited sexual behavior during all portions of the cycle including frequent and regular copulations. This particular female, however, did display a midcycle proceptive peak, but showed greater variation in distribution of her sexual invitations. Three females, Ah, Hf, Nf, demonstrated perimenstrual elevations of proceptive behavior in 5 of the 18 cycles 18"
IS 12z
9 6
lie
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$ 10 12 14 16 18 20 22 24 26 28 M DAY OF CYC LE
FIG. 2. Composite of 18 cycles by nine females of mean hourly rates of female invitations per cycle day across a 28-day menstrual cycle. Standard error (SE) is s h o w n in one direction. Day 28 is 1 day prior to menses (M) for all cycles.
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observed, but only female Nf engaged in copulatory series during menstruation. The dominance rank of the females did not seem to influence the expression of female sexual invitations. A Spearman rank order correlation between mean hourly rates of proceptive behavior per cycle day for each female and the social rank of the female was nonsignificant, rs = 0.12. DISCUSSION Sexual invitations by female rhesus monkeys consisting of defined behavioral patterns, appear to reflect underlying endocrine events during the menstrual cycle. Despite the complexity of social interactions occurring in a group of the composition in this study, the hormonal state of the females strongly influenced expressions of sexually motivated behavior. Not only did females initiate sexual solicitations toward males during a discrete period within their cycles, but the behavior of the males in the form of invitations and copulatory patterns also changed in response to either behavioral or physiological cues from the females. This finding is in general agreement with both laboratory (Michael & Welegalla, 1968) and field studies (Altmann, 1962; Carpenter, 1942; Kaufmann, 1965). The results in this study, however, run contrary to observations by Rowell (1963) that rhesus females in captive social groups show little behavioral cyclicity. The discrepancy between this study and that of Rowell (1963) may have been due to the different composition and housing which perhaps involved frequent disruption of the groups. In Rowell's study, rhesus females lived in groups of three or four with one male housed in outdoor runs. This contrasts greatly with the complexity of the multiple male group in the present study which consisted of a matriarchal organization including siblings and offspring. In view of Rowell's (1972) contention that "with further complication of the social situation one may speculate whether the cyclic effect might be submerged entirely" (p. 80), the data from this investigation indicate that underlying hormonal variables are correlated with the cyclic behavior of female rhesus monkeys more so in the complex than in the simpler setting. All nine of the females exhibited at least some amount of proceptive behavior regardless of social rank. This was not found to be the case for female pigtail macaques (Macaca nemestrina) in laboratory multiphased triads composed of one female in the follicular, another in the preovulatory, and a third in the midluteal phase of the menstrual cycle (Goldfoot, 1971). The lowest ranking females of the triads which were in the preovulatory stage of the cycle inhibited their sexual solicitations in the presence of higher ranking females. In the present study, not only did all the rhesus females display proceptive behavior, but there was no correlation between female social rank and frequency in the solicitation of males.
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It is not surprising that some perimenstrual elevation in invitational behavior was observed in three females since Loy (1970) has reported the occurrence of "peri-menstrual estrus" in free-ranging rhesus females and Czaja and Bielert (1975) also observed its occurrence under laboratory conditions. Nevertheless, it must be emphasized that these elevations did not approach the levels exhibited during midcycle, with the exception of the two cycles of female Nf in which she showed high levels of proceptive behavior through a large portion of these cycles. The patterns of invitational behavior, defined prior to the study, appeared to be a general indication of female sexual motivation as evidenced by their temporal occurrence which was coincident with increases in mounting and ejaculation (to be reported in a subsequent paper). All the females exhibited proximity, following, and sexual presentations, while various individuals displayed one or more of the other solicitation patterns such as hand slap, head bob/duck, threat out, and crouch. Given that presentations are observed in other social contexts, it is not surprising that the occurrence of presentations does not necessarily fluctuate with various stages of the menstrual cycle (Czaja & Bielert, 1975; Rowell, 1963). However, in view of the observations indicating differences between sexual and nonsexual presentations, this suggests that the presentation pattern could represent two responses which are distinguishable. Further investigation of these possible differences should be pursued under more controlled experimental conditions. Observations of the precopulatory posture indicate that this pattern serves as a sexual solicitation. This posture may be just a particular position assumed by the female, but it often appeared during a copulatory series or just prior to a series. Furthermore, Wallen and Goy (1977) have found testosterone and estrogens to increase its incidence. Female-initiated proximity and following of a male occurred far more frequently than patterns of solicitation. These patterns per se do not always serve as sexual invitations, but may occur in other social contexts. Nevertheless, the increase in seeking proximity and following males is quite dramatic when a female is cycling. Additionally, Czaja and Bielert (1975) have also noted that females spent maximum time in proximity to a restrained male around the ovulatory period. Perhaps the discrepancy in frequency of occurrence between proximity and following and the other solicitation patterns is that they serve different functions. Proximity and following serve to place the females in close physical relationship with the male so that copulation is more likely, while hand slap, threat out, etc., may function in maintaining copulatory behavior, or more specifically to initiate mounting. For example, it was incidentally observed that females showing low levels of proceptive behavior, primarily proximity and following, often ceased exhibiting any further patterns once they had engaged a male in copulatory activity.
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These females may not have needed to initiate or maintain copulatory mounts with sexual invitations. On the other hand, they might have passively maintained male copulatory behavior by remaining in proximity or in the precopulatory posture. The distinction in function between gaining access to males and initiating mounts should be examined further in large social groups since the availability of multiple potential mates as well as ample space may be essential to the display of these reproductive strategies. REFERENCES Altmann, S. A. (1962). A held study of sociobiology of rhesus monkeys, Macaca mulatta. Annals of the New York Academy of Science, 102, 181-514. Ball, J., & Hartman, C. G. (1935). Sexual excitability as related to the menstrual cycle in the monkey. American Journal of Obstetrics and Gynecology, 29, 117-119. Beach, F. A. (1976). Sexual attractivity, proceptivity, and receptivity in female mammals. Hormones and Behavior, 7, 105-138. Carpenter, C. R. (1942). Sexual behavior of free-ranging rhesus monkeys (Macaca mulatta). Journal of Computational Physics, 33, 113-142. Conaway, C. H., & Koford, C. B. (1964). Estrous cycles and mating behavior in a free ranging band of rhesus monkeys. Journal of Mammalogy, 45, 557-587. Czaja, J. A., & Bielert, C. (1975). Female rhesus sexual behavior and distance to a male partner: Relation to stage of the menstrual cycle. Archives of Sexual Behavior, 4, 583-596. Goldfoot, D. A. (1971) Hormonal and social determinants of sexual behavior in the pigtail monkey (Macaca nemestrina). In G. B. A. Stoelinga and J. J. van der Werff ten Bosch (Eds.), Normal and Abnormal Development of Brain and Behavior, pp. 325-341. Leiden: Leiden Press. Goy, R. W., & Resko, J. A. (1972). Gonadal hormones and behavior of normal and pseudohermaphroditic nonhuman female primates. Record of Progress in Hormone Research, 28, 707-732. Herbert, J., & Trimble, M. R. (1967). Effect of estradiol and testosterone on the sexual receptivity and attractiveness of the female rhesus monkey. Nature (London), 216, 165-166. Kaufmann, J. H. (1965). A three-year study of mating behavior in a free ranging band of rhesus monkeys. Ecology, 46, 500-512. Keverne, E. B. (1976). Sexual receptivity and attractiveness in the female rhesus monkey. Advances in the Study of Behavior, 7, 155-200. Loy, J. (1970). Peri-menstrual sexual behavior among rhesus monkeys. Folia Primatologica, 13, 286-297. Loy, J. (1971). Estrous behavior of free-ranging rhesus monkeys (Macaca mulatta). Primates, 12, 1-31. Michael, R. P., & Welegalla, J. (1968). Ovarian hormones and sexual behavior of the female rhesus monkey (Macaca mulatta) under laboratory conditions. Journal of Endocrinology, 41, 407-420. Michael, R. P., & Zumpe, D. (1970). Sexual initiating behavior by female rhesus monkeys (Macaca mulatta) under laboratory conditions. Behaviour, 173, 168-185. Michael, R. P., Herbert, J., & Welegalla, J. (1967). Ovarian hormones and the sexual behaviour of the male rhesus monkey (Macaca mulatta) under laboratory conditions. Journal of Endocrinology 39, 81-98. (a) Michael, R. P., Saayman, G. S., & Zumpe, D. (1967). Sexual attractiveness and receptivity in rhesus monkeys, Nature (London), 215, 554-556. (b)
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Rowell, T. E. (1963). Behavior and female reproductive cycles of rhesus macaques. Journal of Reproductive Fertility, 6, 193-207. Rowell, T. E. (1972). Female reproductive cycles and social behavior in primates. Advances in the Study of Behavior, 4, 69-105. Southwick, C. H., Beg, M. A., & Siddiqi, M. R. (1965). Rhesus monkeys in North India. In I. De Vore (Ed.), Primate Behavior, pp. 111-159. New York: Holt. Wallen, K., & Goy, R. W. (1977). Effects of estradiol benzoate, estrone, and propionates of testosterone or dihydrotestosterone on sexual and related behaviors of ovariectomized rhesus monkeys. Hormones and Behavior, 9, 228-248.