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Exposure to men influences the occurrence of ovulation in women
Physiology & Behavior, Vol. 31, pp. 313-315. PergamonPress Ltd., 1983. Printedin the U.S.A.
Exposure to Men Influences the Occurrence of Ovulation in Women J A N E L. V E I T H , M I C H A E L B U C K , S H E L L Y G E T Z L A F , PAMELA VAN DALFSEN AND SUE SLADE W a s h i n g t o n S t a t e University, P u l l m a n , W A 99163
R e c e i v e d 22 April 1983 VEITH, J. L., M. BUCK, S. GETZLAF, P. VAN DALFSEN AND S. SLADE. Exposure to men influences the occurrence of ovulation in women. PHYSIOL BEHAV 31(3) 313-315, 1983.--It has been demonstrated that exposure to men has the capacity to shorten the menstrual cycle in women. In the present study, the impact of the variables of sleeping arrangements and sexual activity were examined on both menstrual cycle length and the occurrence of ovulation as determined by basal body temperature charts. It was found that women who spent at least two or more nights with men during a forty day period exhibited a significantly higher rate of ovulation (0<0.05) than those spending no or one nights. Cycle length was not affected by sleeping arrangements. Furthermore, frequency of sexual intercourse was unrelated to either cycle length or likelihood of ovulation. The mechanism underlyingthis phenomenon is unknown but it is conjectured that it is pheromonal in nature. Ovulation
Menstrual cycle
Pheromones
Sexual activity
IN THE now classi c study [6], it was found that roommates and close friends living in an all female college exhibited a significant increase in menstrual synchrony over a period of seven cycles. The possible influential factors of diet, geographic location in the dormitory and photoperiodic effects were ruled out as causative. Of note, women seeing men less than three times per week experienced significantly longer menstrual cycles (mean=30.0) as compared to those dating on a more frequent basis (mean=28.5). The purpose of the present report was to extend these findings concerning the impact of males on the female menstrual cycle by examining a population of women attending a coeducational university. Exposure to males was defined in terms of both level of daily sexual activity and sleeping arrangements. In addition, while cycle length was included as a dependent variable, occurrence of ovulation was also determined by means of basal body temperature charting, insofar as absence of such an event has the capacity to prolong the cycle [5]. METHOD Subjects
Subjects consisted of 29 undergraduate women who had not employed oral contraception for at least six months. They were recruited from an introductory course in human sexuality and were given extra course credit for their participation. Their mean age was 20.89 years. Procedure
At the initiation of the forty day study, participants received detailed instructions concerning basal body temperature (BBT) charting, considered to be a sensitive and accu-
rate method of determining the occurrence of ovulation [5]. They were also given a packet containing a BBT chart constructed to include information on onset and duration of menses along with illness, and 40 sheets designed to record their level of sexual activity in the past 24 hours along with their sleeping arrangements. All subjects were informed that missing data were highly preferable to information filled in retrospectively. The experimenter was available throughout the 40 day period to answer any questions. At the termination of the study, the subjects handed in their packets. Occurrence of ovulation was determined by two raters using a three point criteria consisting of: (1) a marked dip in temperature followed by an increase of approximately 0.6°F (2) occurring 13 to 15 days preceding the onset of the next menses (3) during which the overall mean temperature was greater than the period preceding estimated ovulation. RESULTS The participants were divided into two groups: Group 1 consisting of women spending no nights with a man during the forty day period and Group 2 comprised of those who had spent one or more nights with a man. Due to the extremely small sample size of Group 1, the groups were redefined. Group 1 consisted of those females spending no or one nights with a man during the forty day period and Group 2 comprised of those spending two or more nights with a male. A t test was employed to examine for possible differences in cycle length between Group 1 (mean=33.31) and Group 2 (mean=30.46). This analysis revealed no significant differences across this variable. A chi square test was then used to analyze possible differences in the percentage of women who ovulated in each group. In Group 1, nine (56°~) ovulated as compared to seven
Copyright © 1983 Pergamon Press Ltd.--0031-9384/83/090313-03503.00
314
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0-1 Nights > 1 Nights FIG. 1. The percentage of women who ovulated (striped bars) compared to those who did not (white bars) in groups of women that spent either no or one nights with a man during a forty day period versus those who spent two or more nights with a male during the same period (,o>0.05).
(44%) who did not. In contrast, of Group 2, 12 (92%) ovulated and only one (8%) did not. The greater number of ovulators in Group 2 as compared to Group 1 was found to be statistically significant X2(1)=4.67, p<0.05 (see Fig. 1). In order to assess additional potential variables contributing to this phenomenon, the impact of sexual intercourse on cycle length and ovulation was examined. Again using a chi square test, the percentage of ovulators in the group that had intercourse either no or one times during the forty day period was compared to the number of ovulators in the group engaging in intercourse two or more times. No significant differences between the two groups were revealed. Also, a t test was employed to compare cycle length between the two groups; this analysis proved insignificant. DISCUSSION
On the basis of these findings, it appears that a significant variable contributing to the likelihood of ovulation are the number of nights a woman spends in the same bed with a man. Insofar as cycle length was not influenced by this factor, it may be suggested that ovulation and length of menstrual cycle are two discrete and separate phenomena. The nature of the mechanism underlying this finding is presently unclear. A number of reviews have been published [1, 4, 10, 13, 14] examining the relationships of pheromones and both animal and human behavior. Perhaps one of the most studied aspects is that known as the Whitten effect [16] which refers to the phenomenon that when female mice are
housed in overcrowded conditions, a high incidence of anestrus occurs. However, if a male is introduced, the females' cycles synchronize and a significantly greater number of matings occur on the third night after the introduction of the male than on any other night. This effect is thought to be pheromonai insofar as male excretia is as effective as the male himself in inducing estrus synchrony [15]. The present study may be viewed as a possible human parallel of the Whitten effect to the extent that the act of sharing a bed with a man influences the fertility of the woman. There is also evidence suggesting that at least one of the underlying mechanisms of menstrual synchrony is pheromonal. Airborne communication between otherwise isolated female rats is adequate to induce the same level of estrus synchrony that is found among rats housed together [7]. Furthermore, women who were rubbed on their upper lip with the underarm perspiration of a single female donor exhibited a significant shift in the timing of their menstrual cycle which closely conformed to that of the donor [12]. Moreover, an abundance of literature suggests both the production of human pheromones and human reactivity to odor. Volatile aliphatic acids have been shown to influence cognitive performance without the person's awareness [3]. Humans were able to identify their own apparel by smell alone and to distinguish between clothing worn by males or females [111. Volatile fatty acids, termed copulins, have been identified in human vaginal secretion; their concentration has been shown to vary across the menstrual cycle, peaking at ovulation [9]. Moreover, human vaginal secretions, when smeared on the sex skin of an ovariectomized female rhesus monkey, stimulated the sexual behavior of a male rhesus [8]. Together, this and other research [2] leads one to speculate that the physiological trigger of male induction of ovulation is pheromonal. However, its exact nature is unknown at the present time; the point has been made [10] that a bias exists among male researchers insofar that more is known about female sex attractants and little work has been completed with regards to male pheromones. The lack of replication of the earlier study [6] concerning lengthening of cycles in those women with limited exposure to males is surpising. However, it may be argued that the present study was completed under conditions that might be considered more naturalistic to the extent that the subjects were enrolled in a coeducation institution. The participants may well have had sufficient exposure to men so their cycle length was not unduly increased. In conclusion, this is the first study to suggest that a specific type of exposure to men has the capacity to alter the occurrence of ovulation in women. A hierarchy of effects of male exposure may exist with extreme limitaitons of the presence of men impacting upon cycle length and occurrence of ovulation being a more finely tuned index of male exposure. Certainly, this effect if replicated, has implications in terms of its adaptive values controlling women's fertility. Further work is called for to determine the underlying mechanism of this phenomenon.
REFERENCES I. Birch, M. C. Pheromones. New York: American Elsevier, 1974. 2. Comfort, A. Likelihood of human pheromones. Nature 230: 432-433. 1971.
3. Cowley, J. J., A. L. L. Johnson and B. W. L. Brooksbank. The effect of two odorous compounds on performance in an assessment-of-people test. Psychonettroendocrinology 2: 159--165, 1977.
MALE INDUCED OVULATION
IN WOMEN
4. Gleason, K. K. and J. H. Reynierse. The behavioral significance of pheromones in vertebrates. Psychol Bull 71: 58-73, 1969. 5. Lanson, L. From Woman to Woman. New York: Alfred A. Knopf, 1978. 6. McClintock, M. Menstrual synchrony and suppression. Nature 229: 244-245, 1971. 7. McClintock, M. K. Estrous synchrony and its mediation by airborne chemical communication (Rattus norvegicus). Horm Behav 10: 264-276, 1978. 8. Michael, R. P. Role of olfaction in sexual response. Med Asp Hum Sex 6: 63-69, 1972. 9. Michael, R. P., R. W. Bonsall and P. Warner. Human vaginal secretion: Volatile fatty acid content. Science 186: 1217-1219, 1974. 10. Rogel, M. J. A critical evaluation of the possibility of higher primate reproductive and sexual pheromones. Psychol Bull 85: 810-830, 1978.
315 11. Russell, M. J. Human olfactory communication. Nature 260: 520-522, 1976. 12. Russell, M. J., G. M. Switz and K. Thompson. Olfactory influences on the human menstrual cycle. Pharmacol Biochem Behav 13: 737-738, 1980. 13. Shorey, H. H. Animal Communication by Pheromones. New York: Academic Press, 1976. 14. Thiessen, D. and M. Rice. Mammalian scent gland markings and social behavior. Psychol Bull 83: 505-539, 1976. 15. Whitten, W. K. Modification of the estrous cycle of the mouse by external stimuli associated with the male: Changes in the estrous cycle determined by vaginal smears. J Endocrinol 17: 307-313, 1958. 16. Whitten, W. K. Occurrence of anestrous in mice caged in groups. J Endocrinol 18: 102-107, 1959.
Exposure to Men Influences the Occurrence of Ovulation in Women J A N E L. V E I T H , M I C H A E L B U C K , S H E L L Y G E T Z L A F , PAMELA VAN DALFSEN AND SUE SLADE W a s h i n g t o n S t a t e University, P u l l m a n , W A 99163
R e c e i v e d 22 April 1983 VEITH, J. L., M. BUCK, S. GETZLAF, P. VAN DALFSEN AND S. SLADE. Exposure to men influences the occurrence of ovulation in women. PHYSIOL BEHAV 31(3) 313-315, 1983.--It has been demonstrated that exposure to men has the capacity to shorten the menstrual cycle in women. In the present study, the impact of the variables of sleeping arrangements and sexual activity were examined on both menstrual cycle length and the occurrence of ovulation as determined by basal body temperature charts. It was found that women who spent at least two or more nights with men during a forty day period exhibited a significantly higher rate of ovulation (0<0.05) than those spending no or one nights. Cycle length was not affected by sleeping arrangements. Furthermore, frequency of sexual intercourse was unrelated to either cycle length or likelihood of ovulation. The mechanism underlyingthis phenomenon is unknown but it is conjectured that it is pheromonal in nature. Ovulation
Menstrual cycle
Pheromones
Sexual activity
IN THE now classi c study [6], it was found that roommates and close friends living in an all female college exhibited a significant increase in menstrual synchrony over a period of seven cycles. The possible influential factors of diet, geographic location in the dormitory and photoperiodic effects were ruled out as causative. Of note, women seeing men less than three times per week experienced significantly longer menstrual cycles (mean=30.0) as compared to those dating on a more frequent basis (mean=28.5). The purpose of the present report was to extend these findings concerning the impact of males on the female menstrual cycle by examining a population of women attending a coeducational university. Exposure to males was defined in terms of both level of daily sexual activity and sleeping arrangements. In addition, while cycle length was included as a dependent variable, occurrence of ovulation was also determined by means of basal body temperature charting, insofar as absence of such an event has the capacity to prolong the cycle [5]. METHOD Subjects
Subjects consisted of 29 undergraduate women who had not employed oral contraception for at least six months. They were recruited from an introductory course in human sexuality and were given extra course credit for their participation. Their mean age was 20.89 years. Procedure
At the initiation of the forty day study, participants received detailed instructions concerning basal body temperature (BBT) charting, considered to be a sensitive and accu-
rate method of determining the occurrence of ovulation [5]. They were also given a packet containing a BBT chart constructed to include information on onset and duration of menses along with illness, and 40 sheets designed to record their level of sexual activity in the past 24 hours along with their sleeping arrangements. All subjects were informed that missing data were highly preferable to information filled in retrospectively. The experimenter was available throughout the 40 day period to answer any questions. At the termination of the study, the subjects handed in their packets. Occurrence of ovulation was determined by two raters using a three point criteria consisting of: (1) a marked dip in temperature followed by an increase of approximately 0.6°F (2) occurring 13 to 15 days preceding the onset of the next menses (3) during which the overall mean temperature was greater than the period preceding estimated ovulation. RESULTS The participants were divided into two groups: Group 1 consisting of women spending no nights with a man during the forty day period and Group 2 comprised of those who had spent one or more nights with a man. Due to the extremely small sample size of Group 1, the groups were redefined. Group 1 consisted of those females spending no or one nights with a man during the forty day period and Group 2 comprised of those spending two or more nights with a male. A t test was employed to examine for possible differences in cycle length between Group 1 (mean=33.31) and Group 2 (mean=30.46). This analysis revealed no significant differences across this variable. A chi square test was then used to analyze possible differences in the percentage of women who ovulated in each group. In Group 1, nine (56°~) ovulated as compared to seven
Copyright © 1983 Pergamon Press Ltd.--0031-9384/83/090313-03503.00
314
V EI T H E T A L . 100 gO 80
\\\\\\\ ~\\\\\\
7o
k \ \ \ \ \ \
¢~
60
•
50
~
40
,t x , t
\k\\\k\ \
30 20 lO
x \x,~
\
\
\
\
\
\
~
,txxx*,x~ xx,t
\ \ \ \ \ \ \
\\\\\\\ \\\\\\\ \\\\\\\ \\\\\\\ \\\\\\\ \\\\\\\ \\\\\\\
x-~*,~
xxx\xx,~ ~,t
x*,xx
x
\ \ \ \ \ k \
\ \ \ \ \ \ \
\\\\\\\ \ \ \ \ \ \ \
0-1 Nights > 1 Nights FIG. 1. The percentage of women who ovulated (striped bars) compared to those who did not (white bars) in groups of women that spent either no or one nights with a man during a forty day period versus those who spent two or more nights with a male during the same period (,o>0.05).
(44%) who did not. In contrast, of Group 2, 12 (92%) ovulated and only one (8%) did not. The greater number of ovulators in Group 2 as compared to Group 1 was found to be statistically significant X2(1)=4.67, p<0.05 (see Fig. 1). In order to assess additional potential variables contributing to this phenomenon, the impact of sexual intercourse on cycle length and ovulation was examined. Again using a chi square test, the percentage of ovulators in the group that had intercourse either no or one times during the forty day period was compared to the number of ovulators in the group engaging in intercourse two or more times. No significant differences between the two groups were revealed. Also, a t test was employed to compare cycle length between the two groups; this analysis proved insignificant. DISCUSSION
On the basis of these findings, it appears that a significant variable contributing to the likelihood of ovulation are the number of nights a woman spends in the same bed with a man. Insofar as cycle length was not influenced by this factor, it may be suggested that ovulation and length of menstrual cycle are two discrete and separate phenomena. The nature of the mechanism underlying this finding is presently unclear. A number of reviews have been published [1, 4, 10, 13, 14] examining the relationships of pheromones and both animal and human behavior. Perhaps one of the most studied aspects is that known as the Whitten effect [16] which refers to the phenomenon that when female mice are
housed in overcrowded conditions, a high incidence of anestrus occurs. However, if a male is introduced, the females' cycles synchronize and a significantly greater number of matings occur on the third night after the introduction of the male than on any other night. This effect is thought to be pheromonai insofar as male excretia is as effective as the male himself in inducing estrus synchrony [15]. The present study may be viewed as a possible human parallel of the Whitten effect to the extent that the act of sharing a bed with a man influences the fertility of the woman. There is also evidence suggesting that at least one of the underlying mechanisms of menstrual synchrony is pheromonal. Airborne communication between otherwise isolated female rats is adequate to induce the same level of estrus synchrony that is found among rats housed together [7]. Furthermore, women who were rubbed on their upper lip with the underarm perspiration of a single female donor exhibited a significant shift in the timing of their menstrual cycle which closely conformed to that of the donor [12]. Moreover, an abundance of literature suggests both the production of human pheromones and human reactivity to odor. Volatile aliphatic acids have been shown to influence cognitive performance without the person's awareness [3]. Humans were able to identify their own apparel by smell alone and to distinguish between clothing worn by males or females [111. Volatile fatty acids, termed copulins, have been identified in human vaginal secretion; their concentration has been shown to vary across the menstrual cycle, peaking at ovulation [9]. Moreover, human vaginal secretions, when smeared on the sex skin of an ovariectomized female rhesus monkey, stimulated the sexual behavior of a male rhesus [8]. Together, this and other research [2] leads one to speculate that the physiological trigger of male induction of ovulation is pheromonal. However, its exact nature is unknown at the present time; the point has been made [10] that a bias exists among male researchers insofar that more is known about female sex attractants and little work has been completed with regards to male pheromones. The lack of replication of the earlier study [6] concerning lengthening of cycles in those women with limited exposure to males is surpising. However, it may be argued that the present study was completed under conditions that might be considered more naturalistic to the extent that the subjects were enrolled in a coeducation institution. The participants may well have had sufficient exposure to men so their cycle length was not unduly increased. In conclusion, this is the first study to suggest that a specific type of exposure to men has the capacity to alter the occurrence of ovulation in women. A hierarchy of effects of male exposure may exist with extreme limitaitons of the presence of men impacting upon cycle length and occurrence of ovulation being a more finely tuned index of male exposure. Certainly, this effect if replicated, has implications in terms of its adaptive values controlling women's fertility. Further work is called for to determine the underlying mechanism of this phenomenon.
REFERENCES I. Birch, M. C. Pheromones. New York: American Elsevier, 1974. 2. Comfort, A. Likelihood of human pheromones. Nature 230: 432-433. 1971.
3. Cowley, J. J., A. L. L. Johnson and B. W. L. Brooksbank. The effect of two odorous compounds on performance in an assessment-of-people test. Psychonettroendocrinology 2: 159--165, 1977.
MALE INDUCED OVULATION
IN WOMEN
4. Gleason, K. K. and J. H. Reynierse. The behavioral significance of pheromones in vertebrates. Psychol Bull 71: 58-73, 1969. 5. Lanson, L. From Woman to Woman. New York: Alfred A. Knopf, 1978. 6. McClintock, M. Menstrual synchrony and suppression. Nature 229: 244-245, 1971. 7. McClintock, M. K. Estrous synchrony and its mediation by airborne chemical communication (Rattus norvegicus). Horm Behav 10: 264-276, 1978. 8. Michael, R. P. Role of olfaction in sexual response. Med Asp Hum Sex 6: 63-69, 1972. 9. Michael, R. P., R. W. Bonsall and P. Warner. Human vaginal secretion: Volatile fatty acid content. Science 186: 1217-1219, 1974. 10. Rogel, M. J. A critical evaluation of the possibility of higher primate reproductive and sexual pheromones. Psychol Bull 85: 810-830, 1978.
315 11. Russell, M. J. Human olfactory communication. Nature 260: 520-522, 1976. 12. Russell, M. J., G. M. Switz and K. Thompson. Olfactory influences on the human menstrual cycle. Pharmacol Biochem Behav 13: 737-738, 1980. 13. Shorey, H. H. Animal Communication by Pheromones. New York: Academic Press, 1976. 14. Thiessen, D. and M. Rice. Mammalian scent gland markings and social behavior. Psychol Bull 83: 505-539, 1976. 15. Whitten, W. K. Modification of the estrous cycle of the mouse by external stimuli associated with the male: Changes in the estrous cycle determined by vaginal smears. J Endocrinol 17: 307-313, 1958. 16. Whitten, W. K. Occurrence of anestrous in mice caged in groups. J Endocrinol 18: 102-107, 1959.