No effects of exposure to women's fertile window body scents on men's hormonal and psychological responses. James R. Roney et al. Evolution and Human Behavior, March 22 2023. https://doi.org/10.1016/j.evolhumbehav.2023.03.003
Abstract: Do men respond to women's peri-ovulatory body odors in functional ways? Prior studies reported more positive changes in men's testosterone and cortisol after exposure to women's scents collected within the putative fertile window (i.e., cycle days when conception is possible) compared to comparison odors, and also psychological priming effects that were differentially larger in response to the fertile window odors. We tested replication of these patterns in a study with precise estimation of women's ovulatory timing. Both axillary and genital scent samples were collected from undergraduate women on six nights spaced five days apart. Here, we tested men's responses to a subset of these samples that were chosen strategically to represent three cycle regions from each of 28 women with confirmed ovulation: the follicular phase prior to the start of the fertile window, the fertile window, and the luteal phase. A final sample of 182 men were randomly assigned to each smell one scent sample or plain water. Saliva samples were collected before and after smelling to assess changes in testosterone and cortisol, and psychological measures of both sexual priming and social approach motivation were assessed after stimulus exposure. Planned comparisons of fertile window to other stimuli revealed no statistically significant effects for any dependent variable, in spite of sufficient power to detect effect sizes reported in prior studies. Our findings thus failed to replicate prior publications that showed potentially adaptive responses to women's ovulatory odors. Discussion addresses the implications of these findings for the broader question of concealed ovulation in humans.
Keywords: Scent attractivenessConcealed ovulationTestosteroneCortisolHuman mating
4. Discussion
As a general summary, we found no compelling evidence that men exhibit differential hormonal or psychological responses to women's body odors collected near ovulation relative to their responses to body odors from other cycle regions (or to plain water). The nonsignificant findings occurred despite our study having sufficient power to detect effect sizes that have been reported in the prior literature. Furthermore, Bayes factors computed for each of our dependent variables suggested that the observed data were about 10 to 13 times more likely under null models than under models including the fertile window contrast, and Bayes factors in this range have been argued to provide strong evidence in favor of the null hypothesis (see Schonbrodt & Wagenmakers, 2018).
4.1. Hormone responses to scent stimuli
Our results did not replicate prior findings of more positive testosterone or cortisol changes after exposure to scents collected near ovulation relative to comparison scents (Cerda-Molina et al., 2013; Miller & Maner, 2010). Our findings for testosterone were more similar to those of Roney and Simmons (2012), who reported no significant differences in hormone changes after exposure to peri-ovulatory scents vs. after exposure to plain water. Among prior studies, only Cerda-Molina et al. (2013) measured differential cortisol responses to women's peri-ovulatory body odors, and they reported a complex pattern whereby cortisol rose above basal concentrations at 15 min post-exposure for peri-ovulatory stimuli and for luteal vulvar stimuli at post 30 min., but fell below baseline concentrations for luteal axillary stimuli at 15 and 60 min. post-exposure. Our results at 15 min. post-exposure did not replicate those patterns.
What may account for differences between results of the current study and those of prior studies that have reported significant hormone responses to women's peri-ovulatory body scents? Miller and Maner (2010) used whole T-shirts as scent stimuli as opposed to our use of gauze pads; although Cerda-Molina et al. (2013) employed similar collection methods to those in the present study, we cannot rule out the possibility that hormone responses may be more reliable in response to shirt stimuli. A possible limitation of our method was the longer time that we stored frozen samples before use in testing (up to a year, as opposed to samples being used within a week in Miller and Maner (2010) and Cerda-Molina et al. (2013)), although studies that have varied length of storage have provided evidence that responses to human body scents are not affected by long freezing times (Gomes et al., 2020; Lenochova et al., 2009). We estimated ovulatory timing more precisely via use of LH tests than did Miller and Maner (2010) who used highly error-prone counting methods (see Gangestad et al., 2016), and this should have increased our probability of finding true effects. Cerda-Molina et al. (2013) cited two factors that might explain discrepancies between their results and the null effects reported by Roney and Simmons (2012)—the longer stimulus collection time in their study and evidence that men in their study were aware that they were smelling women—but both of these differences were eliminated in the present study in which women collected scents overnight and male participants were explicitly told that they were smelling odors from women.
A salient difference between our methods and those of Cerda-Molina et al. (2013) was their use of a nebulizer containing scent stimuli (or plain air) in order to forcefully project odors into participants' nasal passages. It is possible that this method produces hormone responses in perceivers that are absent after taking deep sniffs from jars containing scent stimuli. The ecological validity of the nebulizer delivery method is uncertain. On the one hand, it may deliver stimuli of supra-normal intensity that are not encountered under real-world conditions. On the other hand, it is possible that this method approximates the greater intensity of odor exposure that might occur during some forms of sexual contact. In any case, this difference in scent delivery method presents a possible reason for the discrepancy in findings across the two studies.
It is also possible that prior positive findings for men's hormone responses to women's peri-ovulatory body odors were false positive results. The patterns described in Cerda-Molina et al. (2013) were particularly striking in that men generally responded with testosterone increases after smelling peri-ovulatory stimuli but testosterone decreases after exposure to luteal stimuli. That pattern suggested that men's hormone responses might be strong enough that they could accurately diagnose women's ovulatory timing from scent cues alone. The current findings shed at least some doubt on the robustness of those findings. Future research would ideally provide additional evidence.
4.2. Psychological responses to scent stimuli
Our results also failed to replicate prior findings suggesting the priming of sexual concepts after exposure to peri-ovulatory scent stimuli relative to comparison stimuli. For two dependent variables, we employed measures verbatim from Miller and Maner (2011): the word stem completion task, and a measure of attribution of sexual arousal to the scent donor. A difference in data analysis between studies was the addition of the Chemical Sensitivity Scale (CSS; Nordin, Millqvist, Lowhagen, & Bende, 2003) to the data analyses in Miller and Maner (2011). The scale measures participants' conscious awareness of odors in their environment. For the word stem task, Miller and Maner (2011) added controls for main and interaction effects for scores on this scale in the model testing effects of scent exposure condition. For the sexual arousal attribution task, they reported no main effect of scent exposure condition but a significant interaction between scent condition and CSS scores such that only among men with high smell sensitivity was greater sexual arousal attributed to the peri-ovulatory scents relative to luteal scents. We did not administer this scale, and this difference in method could help to explain discrepant findings for these variables. However, simulation data show that the addition of covariates and testing for interactions with individual difference variables are practices that can inflate type I error rates (Simmons, Nelson, & Simonsohn, 2011), which adds some doubt to the positive findings for the word stem and arousal attribution variables. Furthermore, if sexual priming effects were specialized adaptations for responding to cues of women's ovulatory timing, one would not expect their expression to be restricted only to men with highly sensitive senses of smell. Thus, the overall data pertaining to these variables—including the non-significant findings in the present study—appear to provide weak evidence for adaptations that produce sexual priming effects in response to ovulatory scent cues.
As a more direct measure of sexual priming, we also queried how much sexual desire men felt after exposure to scent cues. There were no significant effects of cycle phase for this variable (see Table 1 and Fig. 4c). Cerda-Molina et al. (2013) administered an “an interest in sex” scale and reported higher scores after exposure to peri-ovulatory scent stimuli, but the scale was quite heterogeneous and included trait-like items (e.g., “[how high do] you think that your sexual desire normally is?”) in addition to measures of current states. As with the hormone responses, it is possible that a nebulizer delivery of scents would produce stronger fertile window effects on men's self-reported sexual desire than those found here.
We did find a main effect of stimulus type on sexual desire such that men who smelled the armpit stimuli reported higher desire than those who smelled the pantyliner stimuli. Additional data analyses supported subjective scent attractiveness ratings as mediating this effect of stimulus type. The positive correlation between scent attractiveness ratings and sexual desire supports the possibility that desire responds to odor attractiveness in general even if it does not respond reliably to scents produced during the fertile window. Odor attractiveness may be related to variables like health (e.g., Olsson et al., 2014) or immune compatibility (e.g., Thornhill et al., 2003), and thus responding to it with desire may have functions aside from ovulation detection.
We also administered a custom social approach motivation scale but scores on it were not differentially higher after exposure to scents from the fertile window (see Table 1 and Fig. 4d). Tan and Goldman (2015) used an indirect behavioral measure to provide evidence that men exposed to peri-ovulatory scents were motivated to sit closer to women, and it is possible that our findings would have differed with such a measure. Oren and Shimone-Tsoory (2019) provided evidence that single but not paired men exhibited greater social perception abilities after exposure to peri-ovulatory scents. Although we did not measure social perception, we did assess the possible moderating influence of relationship status for the effects of cycle phase on our dependent measures, in part motivated by the findings of the social perception study. Results presented in SOM provide no compelling evidence that hormonal or psychological responses to fertile window stimuli were consistent with prior positive findings in the subset of single men.
4.3. Implications for concealed ovulatory timing
Our findings argue against the possibility that human ovulatory timing is detectable from body odors. Mei et al. (2022) recently used signal detection analyses to show that increased scent attractiveness during the fertile window was not substantial enough to reliably diagnose ovulatory timing. That finding left open the possibility that diagnostic cues of ovulatory timing might be revealed via adaptive patterns of responses to scents, such as reactive hormone changes. The present results failed to detect any such putatively adaptive responses, however, and thus argue against that possibility.
The present study addressed only odor cues of ovulatory timing. Cues from other sensory modalities could in principle provide more information, or a combination of cues across modalities could prove more diagnostic. With respect to the latter possibility, Miller and Maner (2011) provided evidence that men who interacted in person with a woman confederate were more likely to mimic her movements and to increase their risk-taking when her estimated conception risk was higher. Perhaps in cases like that, a combination of odor, voice, face, and behavioral cues might more accurately cue fertile window timing.
The strongest tests of multi-modal cuing of ovulatory timing should in principle come from studies that measure the responses of women's long-term romantic partners to the women's cycle phases. Such partners should have the most intimate and detailed information regarding changes in any perceptible stimuli, and would also have clear functional reasons to respond to cues of ovulatory timing for the purpose of ensuring paternity confidence. A recent study of nearly 400 couples with preregistered data analyses and many thousands of observations found no significant effects of women's estimated fertile window timing on male partners' ratings of the women's attractiveness, sexual desire for their partners, feelings of jealousy, or levels of attention to and desire to have contact with the women (Schleifenbaum et al., 2022). Those findings corroborate earlier studies that have generally found that men's rates of sexual initiation are flat across phases of their partners' menstrual cycles (Adams, Gold, & Burt, 1978; Caruso et al., 2014; Van Goozen, Wiegant, Endert, Helmond, & VandePoll, 1997; cf. Harvey, 1987). Likewise, and pertinent to the hormonal responses tested in the current study, studies have failed to find significant shifts in men's testosterone concentrations across different phases of their romantic partners' menstrual cycles (Ström, Ingberg, Druvefors, Theodorsson, & Theodorsson, 2012; Ström, Ingberg, Slezak, Theodorsson, & Theodorsson, 2018). Collectively, these patterns are unexpected if women's body odors provide diagnostic information regarding their ovulatory timing, or if multi-modal stimulus cues jointly reveal fertile window timing.