Physiology & Behavior 68 (1999) 241–250

Brief Communication

Rapid mood change and human odors Denise Chen* and Jeannette Haviland-Jones Rutgers University Received 29 May 1998; received in revised form 22 March 1999; accepted 7 July 1999

Abstract We demonstrate an immediate effect of airborne chemicals on human moods. We collected six groups of underarm odors, respectively, from five prepubertal girls, five prepubertal boys, five college women, five college men, five older women, and five older men. In addition, we collected odors from homes of these donors, making them a seventh group of odor. Three hundred and eight odor observers ranked the seven groups of odors of little girls, little boys, college women, college men, older women, older men, and homes by their perceived pleasantness, intensity, perceived masculinity, and age of the donors, among other qualities. On a separate task, the same odor observers assessed their depressive, hostile, and positive moods twice, once before and once a few minutes after they sniffed one of the above seven groups of odors. Exposure to underarm odors for under 2 min led to significant, rapid, and small changes in the nonclinical depressive mood of the odor observers. The mood changes were independent of the observers’ perceptions of odor qualities. Odors perceived as unpleasant and intense were as likely to relieve a depressive mood as were pleasant odors. © 1999 Elsevier Science Inc. All rights reserved. Keywords: Airborne chemical communication; Mood; Odor judgment; Humans

1. Introduction Animals are known to produce airborne chemicals that elicit long-term physiological and endocrinological effects (e.g., estrous synchronization) [1,2] and immediate behavioral responses (e.g., approach, avoidance) [1] including mood changes (fear) [3,4,]. Human airborne chemicals also elicit long-term endocrinological effects (e.g., menstrual synchronization) [5]. Rudimentary olfactory identification (e.g., kin from nonkin, self from others, familiar from unfamiliar individuals) has been demonstrated in humans [6–9]. What has not been studied is whether mere exposure to such odors has a short-term effect on the behavior of the odor recipients, and whether the effect is contingent upon, or independent of, the recipients’ perceptions of the odor qualities and their inferences about the source of the odors. Research shows that synthetic odors have an effect on mood and memories [10–13] such that pleasant scents tend to have a positive effect, whereas unpleasant chemicals tend to have a negative effect. According to this hedonic congruency model, it seems likely that natural body odors perceived to be pleasant should affect people positively, and that body odors perceived to be unpleasant should affect people negatively. On the other

* Corresponding author. Monell Chemical Senses Center, 3500 Market Street, Philadelphia, PA 19104. E-mail address: [email protected]

hand, given the evidence that odors can affect people without their conscious awareness [5,14,15], it is also possible that the emotional impact of natural body odors may be independent of how the odors are consciously perceived. Animal [1] and dermatological literature [6,9] suggests that odors across different developmental stages vary in biological properties, making them possibly identifiable by age and gender. Research on human olfactory identification of gender, however, is inconclusive. The majority of the studies examined only the olfactory identification of the gender of young adults, and relied on the direct-questioning method of asking people to pick the right odor. Six out of the nine studies found evidence supporting human identification of the gender of young adults based on hand [16], breath [17], and T-shirt [8,18] odors while the three studies based on underarm odors [19] did not. One interpretation of these results is that what is identified is odor intensity/pleasantness, and not gender per se [6,19]. It remains unclear whether discrimination is possible in young adults and in other age groups such as prepubertal children and older adults. A recently published study showed that neither adults nor children themselves identified gender of 9-year-old children [20]. However, hygiene and soap usage in donor children was not controlled, which, as an adult study has suggested [21], could have hampered gender identification. Further, the direct questioning methods may have tapped only the more conscious level of discrimination.

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The purpose of this study is to investigate: (1) whether underarm odors from different age and gender groups have a differential impact on the mood of young adult men and women observers who smell the odors; and (2) whether the emotional responses to odors are contingent upon the observers’ perceptions of odor qualities (e.g., pleasantness, intensity) and inferences about odor source (e.g., donor age and gender). 2. Materials and methods 2.1. Participants and design 2.1.1. Odor donors Underarm odors were collected from 30 donors of six age-by-gender groups: (1) five little girls (mean 6 SD 5 5 6 1.48 years, specific age 5 3, 4, 5, 5, 7); (2) five little boys (mean 6 SD 5 6 6 1.22 years, specific age 5 5, 5, 6, 6, 8); (3) five college women (mean 6 SD 5 20 6 1.14 years, specific age 5 18, 19, 20, 20, 21); (4) five college men (mean 6 SD 5 23 6 3.28 years, specific age 5 19, 21, 21, 25, 27); (5) five older women (mean 6 SD 5 71 6 5.28 years, specific age 5 64, 68, 73, 76, 76); and (6) five older men (mean 6 SD 5 73 6 8.44 years, specific age 5 58, 74, 76, 78, 78). All were Caucasian, healthy, not on hormone treatment, and nonsmoking. The college women were not pregnant and reported regular menstrual cycles (i.e., between 27 to 33 days per cycle). All donors were recruited through ads from the New Brunswick, NJ area. The children were recruited from day care centers, young adults from a state university, and older adults from faculty/staff from the same university, and from a senior activity center. All received $10 and three T-shirts for their participation. 2.1.2. Odor observers The odor observers were 316 undergraduate students. All received course credit for their participation. They were screened for gross olfactory deficit at the end of the experiment. Eight out of the original 316 observers (2%, five women, three men) failed to meet the criteria and were excluded from subsequent analysis. The tests and criteria will be described later under Olfactory Screening Tests. The final odor observers consisted of 308 undergraduate students (154 men, 154 women) ages 17 to 29 (mean 6 SD 5 19 6 1.64 years). Fifty-two percent described themselves as Caucasian, 24% Asian, 9% Hispanic, 8% African-American, and 7% other. The majority of them (97%) were nonsmokers. None of the women reported that they were pregnant. 2.1.3. Design The experiment was a 7 (odor sources: little girls, little boys, college women, college men, older women, older men, home odors) 3 2 (observer gender) mixed-model design, with 22 observers in each cell. The percentage of White, African-American, Hispanic, Asian, and other odor observers were equally distributed across odor conditions (p 5 0.691).

2.2. Odor stimuli collection Adult donors were instructed not to use any fragrance/ antiperspirant nor to shave their underarms starting from 4 days prior to odor collection. Some used the fragrance-free deodorant provided by the experimenter up to the day prior to odor collection. Both child and adult donors were instructed not to eat any odorous food such as garlic and onion both on the day before and on the days of odor collection. A diet diary was kept during odor collections to check if dietary instructions were followed. Any strenuous activities by the donors on the days of odor collection were reported. Both child and adult donors took a bath/shower (or at least washed their underarm regions) on the evening before each odor collection with the fragrance-free soap and shampoo provided by the experimenter, taped a clean 4 3 40 gauze pad around each armpit the next morning, and kept them on for 8 to 10 h. This was repeated for 3 days. Following each day of collection, donors stored the pads in double plastic bags in their freezer. Each day of odor collection, donors wore a new T-shirt provided by the experimenter to avoid odor contamination from laundry detergent. Donors were instructed to leave open blank pads at home as controls for environmental influences. On average, pads were collected by the experimenter the same or the second day after the collection was over, separated by donor age, gender, and odor type, cut into 2 3 20 squares, placed in enclosed glass jars, and frozen at 280 8C until used in testing. Each donor contributed underarm sweat collected on a total of 24 pads (two arms 3 3 days 3 four squares per pad). Subsequent analyses revealed that donor diet, activity level, and the length of time the pads had been worn did not vary by odor conditions. The seven donors who reported to have consumed garlic- or onion-flavored food on the days of odor collection were evenly distributed in each age by gender group (i.e., one little girl, one college man, one older man, two college women, and two older women). Overall, the majority of children and older adult donors reported to be physically active such as engaging in play (children), or gardening or exercising in the gym (older adults). More young adults reported to engage in school-related work such as attending classes and reading. A repeated-measures ANOVA with the number of hours worn on Day 1, Day 2, and Day 3 of odor collection as a within-subjects factor, and with the seven odor conditions as a between-subject factor, found no significant difference in the number of hours the pads were worn on each day, F(2, 23) 5 0.794, p . 0.05, nor in the number of hours the pads were worn for each odor condition, F(10, 48) 5 1.448, p . 0.05. 2.3. Odor stimuli preparation Odor stimuli were defrosted to room temperature at least 40 min before testing. The seven groups of odor stimuli (six groups of underarm odors from little girls, little boys, college women, college men, older women, and older men, re-

D. Chen and J. Haviland-Jones / Physiology & Behavior 68 (1999) 241–250

spectively, and one group of odors combined from the homes of each donor) were each covered up in a 150 3 20 mm glass Petri dish. Glass Petri dishes were chosen over plastic bottles because the latter gave off a plastic odor. They were chosen over glass jars because Petri dishes’ short, flat, and wide surfaces allowed the pads to be evenly spread out and allowed easier sniffing. Each dish of underarm odors contained five 2 3 20 pads representing each individual within that donor group. The home odor dish contained six pads, one randomly drawn from each donor group. The extra pad was hidden underneath the other five pads, so that the home odor dish did not appear different from the underarm odor dishes. Each set of five groups of pads was reused for an average of 7 days (mean 6 SD 5 6.62 6 2.50), and was tested on an average of 13 observers (mean 6 SD 5 13.12 6 3.94). The old pads were then discarded and new pads were used. The pads were changed a total of eight times (or cycles). Three sets of seven groups of odors were used at a cycle during the first seven cycles, and two sets of seven groups of odors were used during the last cycle. After being transferred into enclosed glass jars, the pads were refrozen in between the test days, as well as between sessions on a single test day if the two sessions were separated by more than 3 h. 2.4. Testing condition The experiment was described as a study of people’s reactions to various odors, and did not specify the source/type of any odors. The odor observers were instructed not to wear any fragrances or strongly scented deodorants to the experiment. The experiment was administered by a single experimenter who also did not use any of the above fragrances. On average, observers were either tested individually or two at a time in a room of approximately 6 meters long and 3 meters wide. The room had seven windows; all were opened in between the test sessions. When more than one subject was tested at a time, they were seated apart from one another, to ensure that they were not able to smell the target odor assigned to each other. The experiment consisted of three assessments, in their chronological order: (1) olfactory impact on mood, (2) olfactory impact on memory recollections (not reported here), and (3) odor judgment. Observers smelled only one group of odors on the olfactory-impact-on-mood task but smelled all seven groups of odors on the odor-judgment task. For the purpose of clarity, the odor-judgment task will be presented before the olfactory-impact-on-mood task. 2.5. Olfactory screening tests Two screening tests were given. One was a three-item scratch-and-sniff test (Sensonics, Inc.) in which subjects were asked to identify the correct name of a scent out of four available choices for a total of three scents that are familiar to most people who are raised in this country (i.e.,

243

grass, root beer, coconut). The other was an androstenone identification test. Androstenone is an odorous steroid believed to contribute to underarm odors [22,23]. Subjects were presented with three bottles, and asked to identify over two trials the only one bottle that contained an odor (5 mg of 99% pure 5a-androst-16-en-3-one purchased from Sigma). The order of the tests was random across subjects. Two different tests were used because a previous study [24] suggested that andronstenone sensitivity might not be directly related to overall olfactory sensitivity. Only subjects who made no more than one mistake on the scratch-andsniff test regardless of their performance on the androstenone test, or subjects who correctly identified androstenone on both trials regardless of their performance on the scratchand-sniff test, were included in the final analysis. Five women (one each from the little-girl, little-boy, collegewomen, college-men, and older-women odor condition) and three men (one each from the little-girl, college-women, and older-men odor condition) did not meet such criterion and were excluded. The criterion was arbitrary, and aimed at excluding individuals who were sensitive to neither common/familiar odors nor one of the odorous ingredients of sweat. Out of the final 308 observers who passed the screening tests, one-third of women (34% or 52 women) and over onefourth of men (27% or 42 men) performed correctly on both the scratch-and-sniff and the androstenone test. Sixty percent of women (92 women) and close to 50% of men (48% or 75 men) detected androstenone, compared with 56% of each gender (86 females, 87 males) who correctly identified the names of all three scents on the scratch-and-sniff test. 2.6. Experimental procedure 2.6.1. Odor judgment Observers had all seven odors presented to them. Each odor was ranked independently on perceived pleasantness, intensity, and familiarity, and on perceived erotic quality/ allure, dependency/neediness for care and protection, and perceived age and gender of the donor. The odors were resorted before each ranking. There was a minimum of a 1min interval in between each ranking to minimize the effects of odor adaptation. The order of the evaluations was random except for questions on age and gender, which always appeared last. 2.6.2. Olfactory impact on mood The Differential Emotion Scale IV (DES) [25] consists of 36 questions that assess how frequently observers experienced 12 emotions. Each question is rated on a scale from 1 (rarely or never) to 5 (very often). Observers’ mood was twice assessed on two different forms of the DES, once at the beginning of the experiment, and once about 2 min later, after they completed a brief demographic information form and sniffed one target odor. All observers sniffed only one type of odor. Neither observers nor the experimenter knew which odor was presented. The experimenter randomly selected one dish of odors from the seven dishes of odors. Be-

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cause the identification number was written on the bottom of the dish, the experimenter did not know which odor it was. The identification was only uncovered and recorded before the odor-judgment task. At the end of the day, the experimenter recorded the number of subjects in each odor condition. If one condition was filled, subjects were assigned odors from the remaining conditions. With the exception of the last few subjects, the experimenter did not know which condition the subjects were assigned to. The perceived intensity of the target odor was defined as the ranked intensity of that odor relative to the six other odors. Other perceived qualities of the target odor were similarly defined, based on how the target odor was ranked relative to the other odors on the odor judgment task. When presented with the target odor, observers were instructed to first sniff all five pads in the dish one by one to get an idea of what each smelled like. They were then instructed to take three quick sniffs followed by three long sniffs of all the pads at once. This was done to ensure that all subjects would smell the stimuli in a similar fashion, and that each individual odor within the donor group was smelled. 2.7. Statistical analyses 2.7.1. Odor judgment To determine observers’ perceptions of odor qualities, repeated-measures ANOVAs were conducted with rank within each judgment category (for perceived pleasantness, intensity, perceived masculinity and age of the odor donors, respectively) as a within-subjects factor, and with observer gender as a between-subjects factor. To investigate whether observers on the odor-judgment task might rank the target odor that they had been exposed to earlier on the mood task to be less intense than observers who had not been exposed to it, seven ANOVAs were performed, with the rank of the perceived intensity for each target odor group relative to the other odors as a dependent variable, and with odor condition (observers in that target odor condition versus those who were not) as an independent variable. Results indicate that observers in a particular target odor condition did not rate the intensity of the target odor any differently than those who were not in the condition except that observers who had been exposed to the odors of college men on the mood task rated those odors to be less intense than did observers who had not been exposed to such odors (mean 5 5.77 versus 6.40, F(1, 304) 5 11.26, p , 0.005). Consequently, ranked intensity for odors of college men by observers in that odor condition was adjusted such that any rank less than 4 was increased by 4 (e.g., on a scale where the maximum intensity ranking is 7, an intensity ranking of 1 of college men’s odors by a subject in the college men’s odor condition was adjusted to 5). This brought the mean intensity rank for odors of college men by observers in that condition equivalent to the same as those not in that condition (mean 5 6.30 versus 6.40).

2.7.2. Olfactory impact on mood Mood scores before and after the odor exposure were separately analyzed by Principal Components Analysis (PCA) with varimax rotation. Principal Components Analysis, similar to factor analysis, is a data reduction method widely used in the social sciences. PCA successively extracts a small number of components that account for a large amount of variance while varimax rotation makes the components easier to interpret [26]. Three mood factors were revealed based on the scree plot for both preodor mood and postodor mood scores: depressive mood (like other measures of depression, includes sadness, inward hostility, disgust, and anxiety associated with fear, shame, shy, and guilt), hostile mood (anger and contempt), and positive mood (interest, joy, and surprise). Factor loadings are presented in Table 1. Questions 4 and 31 had low loadings on both mood tests. Question 31 also loaded on different factors on the second mood test. Consequently, both were excluded from subsequent analyses. The three-factor mood structure in the present study was consistent with the threefactor structure found by Stapley and Haviland [27]. No ethnicity difference was found in mood changes or in odor judgment; therefore, subsequent analyses combined observers across different ethic backgrounds. To investigate the relative predictive value of odors on mood above and beyond observers’ preodor mood state, six hierarchical multiple regression analyses were conducted, two for each mood factor. The following variables were entered as predictors in step 1: preodor mood, perceived intensity of the target odor, odor conditions, and observer gender. Odor conditions either appeared as individual odors (dummy coded into six variables), or were grouped by donor age (dummy coded into two variables) and donor gender. Two-way interactions between observer gender and odor conditions were entered as predictors in step 2. Any three-way interactions were entered in step 3. As one of the purposes of the study was to investigate whether mood scores changed as a function of the target odor, the dependent variable was changes in mood (defined as a preodor mood factor subtracted from its postodor mood factor). The seven perceived odor qualities (perceived intensity, erotic quality, pleasantness, familiarity, donor dependency, donor age, and gender) were not entered simultaneously in the same regression because they were significantly correlated with one another. Instead, separate regressions were conducted as above, each controlling for one of the six remaining odor qualities. The same hierarchical multiple regression analyses were also conducted with the adjusted perceived intensity as one of the predictors. The ability to detect androsterone was not entered as a predictor in the regression because it was not significantly correlated with observed mood changes (point-biserial correlation 5 20.029, 20.069, 0.011 with depressive, hostile, and positive mood changes, respectively, p . 0.05), nor was it correlated with observers’ accuracy at identifying the age and gender of the odors (point-biserial correlation 5 0.067, p . 0.05).

D. Chen and J. Haviland-Jones / Physiology & Behavior 68 (1999) 241–250

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Table 1 Item content and factor loadings (Varimax rotation) of the pre-odor and post-odor mood scores Item content on Izard’s original scale

Preodor Components

23. Feel bashful, embarrassed 28. Feel sick about yourself 35. Feel afraid 14. Feel mad at yourself 21. Feel sad and gloomy, almost like crying 5. Feel you can’t stand yourself 22. Feel like you did something wrong 34. Feel discouraged, like you can’t make it, nothing’s going right 7. Feel unhappy, blue, downhearted 10. Feel shy, like you want to hide 19. Feel fearful, like you are in danger, very tense 26. Feel like people laugh at you 6. Feel embarrassed when anybody sees you make a mistake 2. Feel sheepish, like you don’t want to be seen 1. Feel regret, sorry about something you did 12. Feel scared, uneasy, like something might harm you 27. Feel like things are so rotten they could make you sick 30. Feel like you ought to be blamed for something 36. Feel like people always look at you when anything goes wrong 24. Feel disgusted, like something is sickening 31. Feel the way you do when something unexpected happens 9. Feel like somebody is a low-life, not worth the time of day 16. Feel like somebody is “good for nothing” 33. Feel angry, irritated, annoyed with somebody 13. Feel mad at somebody 29. Feel like you are better than somebody 20. Feel like screaming at somebody or banging on something 4. Feel like somthing stinks, puts a bad taste in your mouth 15. Feel happy 3. Feel glad about something 25. Feel joyful, like everything is going your way, everything is rosy 18. Feel amazed, like you can’t believe what’s happened, it was so unusual 17. Feel so interested in what you’re doing that you’re caught up in it 32. Feel alert, curious, kind of excited about something 11. Feel like what you’re doing or watching is interesting 8. Feel surprised, like when something suddenly happens you had no idea would happen

0.680 0.667 0.648 0.645 0.645 0.637 0.624 0.612 0.603 0.596 0.591 0.585 0.584 0.583 0.572 0.562 0.559 0.520 0.508 0.503 0.397

Depressive Hostile

0.421

Postodor Components Positive Depressive Hostile

0.490 0.332 0.778 0.774 0.668 0.641 0.544 0.505 0.480

0.348

0.793 0.677 0.718 0.712 0.678 0.740 0.749 0.725 0.626 0.757 0.636 0.681 0.679 0.748 0.622 0.637 0.611 0.635 0.608 0.637 0.427

0.434 0.705 0.667 0.646 0.575 0.568 0.555 0.542 0.516

Positive

0.488 0.830 0.838 0.727 0.724 0.591 0.644 0.440 0.623 0.658 0.613 0.691 0.647 0.667 0.673 0.650

Principal Components Analysis is used as the extraction method. Loadings on both components are displayed if the same item loads on two components and their loading difference is less than 0.19.

Corrections for inclusion of multiple tests were taken to protect the alpha levels. For example, to ensure that the significance level for the variable of odor condition was 0.05, the significance level of each of the six dummy variables to represent the seven categories of odor condition had to be less than 0.0083 to be considered significant. To ensure that the significance level for the variable of donor age was 0.05, the significance level of each of its two dummy variable had to be less than 0.025 to be considered significant. The effect size d is reported. It is calculated at t times the square root of the sum of one over the first sample size and one over the second sample size. According to Cohen, d 5 0.20 indicates a small effect size, d $ 0.50 indicates a medium effect size, and d $ 0.80 indicates a large effect size [28].

measures ANOVAs were performed for perceived intensity and perceived pleasantness respectively with the rank of the seven groups of odors as a within-subjects factor and with the cycle of the pads as a between-subjects factor. Although there was a significant rank by cycle interaction, F(39, 1689) 5 2.254 and F(38, 1649) 5 2.438, p , 0.0001, for pleasantness and intensity, respectively. Scheffe post hoc analyses showed that none of the pairwise comparison reached significance after the significance level for each pair was adjusted. There were a total of 56 (seven odors 3 eight cycles) pairs of comparisons. The significance level for each pair needed to be less than 0.0009 in order to achieve an overall significance level of 0.05. Thus, we conclude that the perceived odor pleasantness and intensity respectively did not differ by cycle.

3. Results

3.1. Odor judgment

To examine whether pads from differ cycles varied in their perceived pleasantness and intensity, two repeated-

Odor observers ranked the seven odors on qualities such as perceived pleasantness, intensity, and perceived gender

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and age of the donors (Figs. 1 and 2). Home odors and odors of children were perceived to be most pleasant, least intense, most feminine, and youngest in age among the seven target odors. The odors of college men followed closely by odors of older women were perceived as most unpleasant, intense, most masculine, and oldest in age. Odors of college women and older men were in the middle. The finding that odors of older women were judged more similar to odors of college men than to odors of college women and that odors of older men were judged more similar to odors of college women than to odors of college men could be due to the change in the hormonal profile in older women and men. The estrogen/testosterone ratio has been found to decrease in postmenopausal women [29,30] and increase in older men [30–32]. Although apocrine gland activities are believed to stop in old age [9], the strong underarm odors found in older women in this study seem to indicate otherwise. There have been claims that people can discriminate gender from the hand, breath, and T-shirt odors of young adult men and women [8,16–18], but such results may have been biased by age restrictions in the samples. When we added an older adult sample, we found neither gender nor age identification was consistently accurate. Our results support Doty and colleagues’ findings [6,19] that such discrimination might have been based on observers’ perceptions of odor intensity and pleasantness. The more intense and unpleasant an odor, the older and more masculine the donors were judged to be. This stereotypic rule led observers to misidentify little boys as little girls, and to misidentify both college men and older women as old men. Older men, whose odor was judged moderate on most scales, might be classified as any age or gender. Odors of college women were identified as female, but their low intensity caused them to be easily confused with children’s odors.

Fig. 1. Average rank of perceived odor pleasantness, intensity, and perceived masculinity and age of the donors by odor conditions. Vertical bars represent standard errors about the means. This is based on repeated measures ANOVAs, F(6, 301) 5 125.14, 266.24, 77.17, and 46.17, respectively, p , 0.0001.

Fig. 2. Average rank of perceived erotic quality, intensity, familiarity, and perceived dependency of the donors by odor conditions. Vertical bars represent standard errors about the means. This is based on repeated measures ANOVAs, F(6, 301) 5 88.82, 266.24, 14.84, and 9.70, respectively, p , 0.0001.

3.2. Olfactory impact on mood The regression results for depressive mood are presented in Tables 2 and 3, and mean changes in depression by odor conditions are presented in Fig. 3. Based on research on the effect of synthetic odors on mood and behavior [10–13], we had predicted that mild and pleasant odors, such as the underarm odors of children, would have an uplifting effect on the mood of the observers, whereas intense and unpleasant odors, such as the underarm odors from men, would increase the hostile and depressive moods of the observers. However, we actually found that even after preodor depressive mood and perceived odor intensity had been controlled, observers still reported lower ratings of depression when presented with odors of older adults in contrast to younger adults, and odors of women in contrast to men (b 5 20.166 and 20.144, p , 0.02, d 5 0.36 and 0.29, respectively, small effect size). Identical results were obtained after the perceived intensity had been adjusted for habituation (b 5 20.167 and 20.145, p , 0.02, d 5 0.36 and 0.29). In particular, observers reported significantly lower ratings of depression when presented with odors of older women than when presented with odors of college men (b 5 20.287, p , 0.0001, d 5 0.82, large effect size). Again, identical results were obtained after the perceived intensity had been adjusted for habituation (b 5 20.290, p , 0.0001, d 5 0.81). ANCOVAs for each mood factor with the preodor mood and perceived odor intensity as covariates, with odor conditions and observer gender as independent variables, and with the mood change as the dependent variable, yielded the same result as the regression analyses. Regression analyses respectively controlling for perceived odor pleasantness, erotic quality, familiarity, and donor dependency, age, and gender yielded results that are

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Table 2 Hierarchial multiple regressiona of preodor depressive mood, perceived odor intensity,b observer gender, and odor conditions (for individual odors) on changes in depressive moodc Variable Step 1 Preodor depressive mood Perceived odor intensity Observer gender (w 5 1, m 5 0) Odor 1 (girlse 5 1, rest 5 0, cm 5 reference)f Odor 2 (boys 5 1, rest 5 0, cm 5 reference) Odor 3 (cw 5 1, rest 5 0, cm 5 reference) Odor 4 (ow 5 1, rest 5 0, cm 5 reference) Odor 5 (om 5 1, rest 5 0, cm 5 reference) Odor 6 (home 5 1, rest 5 0, cm 5 reference) Step 2 Observer gender 3 odor 1 Observer gender 3 odor 2 Observer gender 3 odor 3 Observer gender 3 odor 4 Observer gender 3 odor 5 Observer gender 3 odor 6

R2

DR2

0.086

0.086

3.034**

0.112 0.011 0.139* 20.136 20.136 20.136 20.287*** 20.108 20.202*

0.095

0.009

0.475

0.026 20.069 0.051 20.016 0.028 20.090

Incremental F

Betad

R 5 0.308, R2 5 0.095, F(15, 285) 5 1.991, p , 0.02, for the total equation. Perceived odoar intensity 5 Ranked intensity of the target odor relative to the six other odors. The ranks were obtained from the odor judgment task. c Changes in depressive mood 5 postodor depressive mood 2 preodor depressive mood. d Beta weights are for the simultaneous entry of variables. Beta is the standardized multiple regression coefficient that allows comparisons of the relative effects of the predictor variables. It indicates the predicted change (in standard deviation units) in the dependent variable of a mood difference for a standard deviation change in a particular predictor, when all other predictor variables are held constant [39]. e Girls 5 little girls, boys 5 little boys, cw 5 college women, cm 5 college men, ow 5 older women, om 5 older men, home 5 home odors, w 5 women, m 5 men. f Each level of odor condition and each level of gender by odor condition is counted as significant only if p , 0.0083. *p , 0.05, **p , 0.005, ***p , 0.0001. a

b

Table 3 Hierarchial multiple regressiona of preodor depressive mood, perceived odor intensityb, observer gender, and odor conditions (by donor age and donor gender) on changes in depressive moodc Variable

R2

DR2

Incremental F

Step 1 Preodor depressive mood Perceived odor intensity Observer gender (w 5 1, m 5 0) Donor gender (w 5 1, m 5 0) Donor age 1 (ce 5 1, rest 5 0, ya 5 reference)f Donor age 2 (oa 5 1, rest 5 0, ya 5 reference) Step 2 Observer gender 3 donor gender Observer gender 3 donor age 1 Observer gender 3 donor age 2 Donor gender 3 donor age 1 Donor gender 3 donor age 2 Step 3 Observer gender 3 donor gender 3 donor age 1 Observer gender 3 donor gender 3 donor age 2

0.081

0.081

3.701***

Betad 0.131* 20.001 0.160*** 20.144** 20.090 20.166**

0.094

0.013

0.711 0.046 20.074 20.038 0.133 20.051

0.097

0.003

0.362 0.073 20.066

R 5 0.311, R2 5 0.097, F(13, 245) 5 2.018, p , 0.03, for the total equation. Perceived odor intensity 5 ranked intensity of the target odor relative to the six other odors. The ranks were obtained from the odor judgment task. c Changes in depressive mood 5 postodor depressive mood 2 preodor depressive mood. d Beta weights are for the simultaneous entry of variables. Beta is the standardized multiple regression coefficient that allows comparisons of the relative effects of the predictor variables. It indicates the predicted change (in standard deviation units) in the dependent variable of a mood difference for a standard deviation change in a particular predictor, when all other predictor variables are held constant [39]. e C 5 children, ya 5 young adults, oa 5 older adults, w 5 women, m 5 men. f Donor age 1 and donor age 2 are counted as significant only if p , 0.025 for each. *p , 0.05, ** p , 0.02, ***p , 0.01. a

b

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Fig. 3. Changes in depressive mood by odor conditions. Vertical lines represent standard errors about the mean. The part below zero indicates the amount of reduction in depression after the observers smelled the target odor. This is based on an ANCOVA with changes in depressive mood as the dependent variable, observer gender, and odor condition as independent variables, and with preodor depressive mood and perceived intensity of the target odor as covariates, F(6, 285) 5 2.771, p , 0.02.

identical to the regression analyses reported above that controlled for perceived odor intensity. Namely, even after preodor depressive mood and perceived odor qualities (e.g., pleasantness, erotic quality, familiarity, dependency, donor age, donor gender) had been controlled, observers still reported significantly lower ratings of depression when presented with odors of older adults in contrast to younger adults (b 5 20.166 to 20.17, p , 0.016 to 0.018), and odors of women in contrast to men (b 5 20.144 to 20.154, p , 0.013 to 0.019. Rapid exposure (i.e., around 2 min) to odors also led to a nonsignificant change in the positive mood consistent with that found in the depressive mood. That is, when depression was significantly lightened, positive moods were nonsignificantly elevated. There was no change in the hostile moods. Mean changes in depressive, hostile, and positive mood, are presented in Table 4. Although women reported higher ratings of depression than did men (b 5 0.139, p , 0.02, d 5 0.28, small effect size and identical results were obtained after perceived intensity had been adjusted for habituation), there was no interaction. 4. Discussion To summarize, our data demonstrate that airborne chemicals produced by humans can modulate the moods of other humans independent of perceived odor intensity and pleasantness, and independent of the attributions of the donors’ age and gender. In particular, exposure to underarm odors of older women, women, and older adults, led to a greater reduction in depressive mood than exposure to underarm

odors of young men, men, and young adults. This could indicate a subtle effect of airborne chemicals on human mood. Even though the effect of airborne chemicals on mood is very small, though significant, we believe that the rapid mood change is impressive, given that observers smelled the target odor for under 2 min, and given that the two mood tests were only separated by 2 or 3 min. Longer exposure or repeated exposure may show significant cumulative effects on individual and group moods. In addition, results of this study suggest that people may differentially react to differences between odors of different ages and gender, but may not be able to articulate them on a simple discrimination task. For example, although underarm odors of older women and of young men had different effects on observers’ depressive moods, both were perceived to be intense, unpleasant, masculine, and aging on odor judgment tasks. This could be because the mood assessment task provided a relatively meaningful and self-relevant context, whereas the simple discrimination task did not. Context may be important to process olfactory information. This is consistent with observations that meaningful scents trigger emotional memories [33,34]. Van Toller and Kendal-Reed [35] made the distinction between an olfactory experience that lends itself to linguistic description (e.g., naming or labeling an odor) versus an olfactory experience that is intuitive and nonlinguistic (e.g., emotional relationship with one’s grandmother evoked by the smell of lavender water). Perhaps the mood task used in this work provided such a social linguistic environment for people to describe something that may be social but may not be intrinsically linguistic. The hedonic congruency effect was found in previous studies but not in the present study. This could be due to a number of reasons. One of them could be that natural body odors carry biologically significant information that impacts on people differently from the way artificial fragrances or chemical irritants do. Another reason could be due to differences in analyses. The present study controlled for differences due to subjects’ perceived odor intensity/pleasantness,

Table 4 Mean changes in depressive, hostile, and positive mood by types of odor Depression

Hostility

Positive

Types of odor

Mean

SE

Mean

SE

Mean

SE

Little girls Little boys College women College men Older women Older men Home odor

22.062 22.078 22.020 20.0543 24.213 21.688 23.093

0.768 0.788 0.764 0.852 0.792 0.758 0.799

20.317 20.408 20.876 20.418 20.774 20.908 20.295

0.307 0.311 0.308 0.343 0.317 0.303 0.317

20.892 21.147 20.842 21.955 20.924 20.859 21.624

0.378 0.383 0.374 0.419 0.390 0.381 0.389

Children Young adults Older adults

22.072 21.002 22.934

0.597 0.568 0.561

20.400 20.629 20.820

0.229 0.221 0.217

21.008 21.385 20.876

0.295 0.281 0.281

Women’s odors Men’s odors

22.766 21.239

0.455 0.454

20.658 20.576

0.175 0.175

20.874 21.305

0.224 0.226

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whereas previous studies did not. In addition, the intensity/ pleasantness of the odors in the present study was measured relative to one another, and not in the absolute sense. We found in this study that underarm odors differentially impacted on the depressive mood but not on the positive mood. One possible explanation is that almost all existing mood tests have more items on negative than on positive moods, a potential bias that might have made the tests more sensitive to detecting negative than positive changes. Another plausible explanation is that the observed olfactory impact on negative moods reflected a primordial impression of men and young adults. In many species, including humans [36], males and young adults tend to be more aggressive then females and older adults. There are several important limitations of this study. For one thing, target odors were not judged individually but were judged as a group. It is possible that individual differences exist within each donor group. However, the experimenter observed that at least three of the five college men and two of the five older women had strong odors. Thus, it was not simply the odor of one individual within the group that biased the judgment of the entire group. Nevertheless, future studies may want to evaluate the odors both on an individual as well as on a group basis. Secondly, a number of studies have indicated that the olfactory sensitivity in women varies by the different phases of their menstrual cycles [37,38]. However, menstrual cycles of female observers were not recorded in this study, largely because the olfactory screening tests would already discriminate between the olfactorily more sensitive observers from those who were not. In conclusion, the findings of the present work replicate and extent past research on olfactory identification of gender. This work examines olfactory identification of gender in conjunction with age from a developmental perspective, and examines the effects of body odors from different ages and genders on peoples’ mood. It demonstrates for the first time that body odors carrying social-biological information differentially bias odor recipients’ moods. This finding may have an important implication for existing research on human perception and interaction. Acknowledgments We are grateful to Dr. Erich Labouvie for helpful discussions. We are also grateful to Drs. Julie Mennella, Mort Bart, and Paul Vincenti for discussions, to Dr. Terry McGuire for comments on the first draft, Dr. Pamela Dalton for comments and suggestions on a later draft, and to the anonymous reviewers for comments and suggestions. We thank all our participants. This research was supported in part by Tova Dissertation Fellowship from the Olfactory Research Fund. References [1] Brown RE, Macdonald DW. Social Odors in Mammals, vols 1 & 2. Oxford: Clarendon Press, 1985.

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