Uncovering the Stinkin’ Truth Anne Kitchell, Sharon Lynn, Shiva Vafai A Taste of Smell 6 December 1995 Of the human senses, smell is perhaps the least appreciated, least understood, and most difficult to study. In fact, one study demonstrated that, of the people polled, “the least valued sense--the one people would be most willing to lose if they had to lose one--is smell.” (Synnott, 1994) In our search for a term project for A Taste of Smell, we quickly discovered that many commonly held ideas about the sense of smell are supported by little more than anecdotal evidence. So, we searched for scientific documentation which supports or refutes some of these widely accepted notions of smell. We elicited the help of our classmates, and our collaborative brainstorming effort resulted in numerous “smell myths.” The following ten questions summarize our research efforts, and provide a springboard for further investigation of this under-appreciated sense. 1. Do men and women differ in their capacity to detect odors?shiva 2. Does olfactory acuity decline with age?shiva 3. What role do odors play in the human menstrual cycle?a 4. Do human menstrual odors act as attractants? a 5. Can animals really smell fear?s 6. Do members of different cultures have characteristic body odors?s 7. Does smoking affect the sense of smell?ass 8. Do pregnant women experience a heightened sense of smell?ass 9. What role does hair color play in olfaction?ass 10. Do human pheromones exist? ass
Synnott, A (1994) Roses, coffee and lovers: the meanings of smell. in Compendium of Olfactory Research 1982-1994. pp. 117-128.
Do men and women differ in their capacity to detct odors? According to studies performed before the turn of the century (Bailey & Nichols, 1884; Bailey & Powell, 1885), it was believed that men possessed greater sensitivity to odors in threshold studies than did women. Albeit, these studies, both from the same laboratory, did not report the details of their experiments, except that twenty subjects of each gender participated. Neither the ages of the participants, the testing procedure, nor the number of replicates performed, if any, were reported. Since the publication of these studies, there has been no conclusive evidence in support of the findings of these experiments. In fact, the overwhelming evidence has provided support for the opposite contention, that women possess greater sensitivity to odorants. Koelega and Koster (1974) conducted experiments involving a modified method of constant stimuli of several hundred subjects, reporting lower female thresholds for the nine substances tested. Experimentally, threshold measures and sensitivity are considered to directly correspond. Koelega and Koster also found that prepubescent girls out performed prepubescent boys on a number of odor detection tasks. The substances involved in the experiment included amyl acetate, androstenone derivatives, exaltolide, xylene, and pyridine. The experiments of Toulous and Vaschide (1899), Le Magnen (1952), and Schneider and Wolf (1955) also support the notion that females possess greater sensitivity to odors in threshold studies. In addition to the well-documented superior female performance noted in these and more recent odor-identification studies (Doty, 1981), other studies reveal that the sex difference may be observed in all decades of life. This is in direct objection to the widely-accepted belief that sex differences in olfactory perception are due to differences in gonadal hormone levels (Doty & Snyder, 1981). It is not surprising that sex differences with regard to smell sensibility exist, especially in light of studies which reflect similar differences in performance between the sexes in vision, hearing, tactile, and kinesthetic experiments (McGuinness, 1976). The most extensive study heretofore conducted on odor perception on a large scale is the classic Smell Survey sponsored by the National Geographic in its September 1986 issue. The Smell Survey, comprised of a questionnaire and a set of six microencapsulated odorants, was distributed worldwide to 10.7 million members of the National Geographic Society. Of the 1.5 million surveys which were returned, the results of nearly 1.2 million United States respondents between the ages of 10 and 90 provide the basis for the conclusions herein discussed. Respondents characterized the odors, namely, androstenone (sweat), isomyl acetate (banana), galaxolide (musk), eugenol (cloves), mercaptans (natural gas warning agent), and a synthetic rose scent, according to a set of category descriptors. The huge sample size and broad range of the survey provides data which can be used to investigate further possible correlations with specific demographics of the sample population, including gender (Gilbert & Wysocki, 1987). Certain aspects of the sample surveyed are to be noted to prevent misapplication of the results bias (Wysocki & Gilbert, 1989). The data are not considered to be representative of the United States. More women than men participated in the survey, which may indicated a positive female response Additionally, it may be worthwhile to mention that the vast majority (95%) of the participants identified themselves as white. The average age of the respondent was 43.3 years. Though the gender differences were small, they were consistently evident in the survey results. Self-Rating: Throughout the nine-decade life span distribution, women thought they had better olfaction than men, and generally, they did. The smell-ability self-ratings declined for both sexes, though women's self-ratings increased until the fifth decade, at which point the self-ratings decreased, with accelerated decline in the eight decade; Men's smell-ability self-ratings declined more conistently across the age distribution, though the range of self-ratings for both sexes represented 11% of the entire rating scale. Insert graphs WYC and GIB p 16 Perception/Intensity: Women of all ages more frequently perceived androstenone and galaxolide. Both men and women generally detected the other four odors with equal degree of perception until the fifth decade, after which time women more frequently perceived the odors. Across the lifespan, women correctly identified all six odors more frequently than did men. Insert graphs WYC and GIB p 17 and 19 and 20 Pleasantness: In rating the quality of the odors, the responses of the participants divided according to sex for each odor, though the relationship between the sexes was inconsistent. Men found the androstenone, isomyl acetate, and mercaptans to be more pleasant, and women found eugenol and rose to be more pleasant. Women generally found Galaxolide to be more pleasant than did men, with slightly declining ratings after the fourth decade; men generally demonstrated a similar pleasantness rating distribution, except with a sharp increase in the ninth decade of life. Insert graphs WYC and GIB p 24 A microscale experiment was conducted in our classroom using the National Geographic Smell Survey. The raw data may be accessed from the “class.xls” file. Unfortunately, due to the small sample size and the disproportionate male - female ratio, we found it difficult to draw any conclusions as a whole from the data collected. However, a mini-questionnaire (modelled after the Smell Survey) and a spreadsheet may be found in the aforementioned “class.xls” file for use in future surveys of this nature. In conclusion, it is suggested by the literature available that there exists slightly superior female performance in odor-identification studies, a trend observed consistently in all ages of life. However, due to the difficulty in testing and quantifying olfactory acuity, the experimental data from which conclusions have been made are not as scientific in their method or in their accuracy as would be ideal; neither are the data as dependable as the information available from sex-differences studies in regard to the other senses. It is hoped that future investigation in the field of olfaction may lead to more precise tools and methods with which to test the hypothesis that women possess greater olfactory prowess. References Bailey, E.H.S. and Nichols, E.L. Preliminary notes on the delicacy of the special senses. New York Medical Journal, 40:325, 1884, cited in Doty, R.L. Mammalian Olfaction, Reproductive Processes, and Behavior, 1976. Bailey, E.H.S. and Powell, L.M. Some special tests in regard to the delicacy of the sense of smell. Transactions of the Kansas Academy of Science, 9:100-101, 1885, cited in Doty, R.L. Mammalian Olfaction, Reproductive Processes, and Behavior, 1976. Doty, R.L. Chemical Senses, 6:351, 1981. Doty, R.L. et al., Journal of Comparative Physiological Psychology, 95:45, 1981. Gilbert, A.N. and Wysocki, C.J., The Smell Survey Results, National Geographic, 122:514-525, 1987. Koelega, H.S. and Koster, E.P. Some experiments on sex differences in odor perception. Annals of t he New York Academy of Sciences, 237:234-246, 1974, cited in Doty, R.L. Mammalian Olfaction, Reproductive Processes, and Behavior, 1976. Le Magnen, J. Les phenomenes olfacto-sexuels chex l'homme. Archives des Sciences Physiologiques, 6:125-160, 1952, cited in Doty, R.L Mammalian Olfaction, Reproductive Processes, and Behavior, 1976. McGuinness, D. Exploring Sex Differences, pp 123-156, 1976. Schneider and Wolf, R.A. and Wolf, S. Olfactory perception thresholds for citral utilizing a new type olfactorium. Journal of Applied Physiology, 8:337-342, 1955, cited in Doty, R.L. Mammalian Olfaction, Reproductive Processes, and Behavior, 1976. Toulouse, E. and Vaschide, N. Mesure de l'odorat chex l'homme et chez la femme. Comptes Rendue des Sceances de la Societe de Biologie et de Ses Filiales, 51;381-383, 1899, cited in Doty, R.L. Mammalian Olfaction, Reproductive Processes, and Behavior, 1976. Wysocki, C.J. and Gilbert, A.N. The National Geographic Smell Survey: Effects of age are heterogenous. Annals of the New York Academy of Sciences, 561:12-28, 1989. Does olfactory acuity decline with age? Unlike well-documented evidence collected in studies of vision and hearing loss with aging, most smell-perception studies are not standardized, some are contradictory, and few are broad enough in scope and depth to offer clear and irrefutable conclusions. A smell survey conducted by National Geographic, however, provides valuable information in the study of age-related change in smell perception (Gibbons, 1986). The Smell Survey, comprised of a questionnaire and a set of six microencapsulated odorants, was distributed worldwide to 10.7 million members of the National Geographic Society. Of the 1.5 million surveys which were returned, the results of nearly 1.2 million United States respondents between the ages of 10 and 90 provide the basis for the conclusions herein discussed. Respondents characterized the odors, namely, androstenone (sweat), isomyl acetate (banana), galaxolide (musk), eugenol (cloves), mercaptans (natural gas warning agent), and a synthetic rose scent, according to a set of category descriptors. The huge sample size and broad range provided data which demonstrates continuous trends according to age measured in decades of life (Gilbert and Wysocki, 1987). Wysocki and Gilbert (1989) discuss in great detail the results of the survey, but for our purpose, let it be noted that an analysis of the data showed a decline of odor perception with age for each of the six odors, though the loss of the sensibility was unequal across the odors. Generally, the intensity of the odors was perceived to decline with age, supporting previously-documented studies of suprathreshold odors involving elderly participants (Van Toller and Dodd, 1987). In addition to declining smell perception, aged participants demonstrated declining smell identification capability. These differences may not be solely due to sensory perception, as Wysocki and Pelchat (1993) point out, but to cognitive perceptions as well, including skills such as active encoding, retrieval and use of labels (Schemper, 1981). Insert graphs WYC and GIB p 17, 19 It is interesting to note that younger participants rated themselves as having better smell sensibility than did older participants. However, those participants who performed very poorly on the survey, indicating poor olfaction, considered themselves to have average to better olfaction. Insert graphs WYC and GIB p 16 If there does exist a general decline of smell sensibility with age, it may be logical to investigate an anatomic or physiological deterioration or change which may occur in the olfactory system over time. As has been studied by Liss and Gomez (1958), senile changes may be observed to correspond with degenerative changes in the central nervous system, including extensive degeneration of the olfactory epithelium with subsequent degeneration of the olfactory bulb. Correlations have been made between the similarities of amyloid bodies seen in the olfactory bulb and nerve fiber degeneration in the optic nerve. As the causes of the morphological changes in aging olfactory bulbs are unknown, the evidence is only circumstantial that regressive bulbs may be involved in inducing diminished smell perception (Doty et al., 1984). With age there is noted, in addition to atropy of olfactory receptors, increased exposure to olfactory-unfriendly chemicals in the environment, and increased probability of complications arising from other age-related diseases and from their medications (Bhatnagar et al., 1987). Unlike studies dealing with the other senses, olfaction studies cannot directly measure smell perception, but must rely instead on indirect methods such as magnitude estimation ("How strongly did you smell the odor?"), threshold determinations (i.e.: at what strength was the odor perceptible), and association judgements ("What did the odor smell like?"). As there exist various and sundry other factors which may take a role in the perception of smells, including psychological, physiological, and experiential factors, it is impossible to correlate a direct relationship between any one factor, such as age, and smell sensibility. Factors which may contribute to age-related sensory decline are presumed to be not singular, and therefore potentially interacting, and probably complex. That is to say, there does not exist evidence to support the contention that age-related deficiency in olfactory sensation occurs uniformly with age, across odors and concentrations. The effects of aging with regard to the sense of olfaction are heterogeneous given the evidence which has heretofore been collected, albeit a general decline of sensory perception and identification is noteworthy with age, as the results of the Smell Survey clearly indicate. References Bhatnagar, K.P. R.C. Kennedy, G. Baron & R.A. Greenberg,. Anatomical Record 218:73-87, 1987. Doty, R.L. , P. Shaman, S.L. Applebaum, R. Giberson, L. Sikorski & L. Rosenberg, Science 226: 1441-1443, 1984. Gibbons, B. 1986. The Intimate Sense of Smell/National Geographic Smell Survey, National Geographic 170:324-361. Gilbert, A.N. and C.J. Wysocki. 1987. The Smell Survey Results, National Geographic 122:514- 525. Liss, L. and Gomez, F. 1958. The nature of senile changes of the human olfactory bulb and tract, Arch. Otolaryngol. (Stockh) 67:167. Schemper, T., Voss, S. and Cain, W.S. 1981. Odor identification in young and elderly persons: sensory and cognitive limitations, J. Gerontol., 36:446, 1981. Van Toller, S. and G.H. Dodd. 1987. Presbyosmia and olfactory compensation for the elderly, Br. J. Clin. Pract. 41:725. Wysocki, C.J. and A.N. Gilbert. 1989. The National Geographic Smell Survey: Effects of age are heterogenous. Annals of the New York Academy of Sciences, 561:12-28. Wysocki, C.J., and Pelchat, M.L.. 1993. The Effects of Aging on the Human Sense of Smell and Its Relationship to Food Choice, in Critical Reviews in Food Science and Nutrition, 33(1):63-82. What role do odors play in the human menstrual cycle? Do human menstrual odors act as attractants? Blood-Scented Perfume Through no fault, nor choice, of their own, women are “blessed” monthly with the outward expression of their inner femininity, that internal cycle of fertility-- intimately characterized by intense hormonal explosions, physiological “expectations” of ensuing life, and emergency trips to particular grocery aisles that men tend to avoid. There one can find shelf upon shelf of products by Kotex, Tampax, Playtex, Always... an infinite demand supplied by a market delicately labeled FEMININE PROTECTION. Heavy or light, thick or thin, disposable, cardboard/ plastic applicator, fresh scent, winged-teen-maxi-supreme all are available to the lucky ladies of the 20th century. Lucky schmucky. In dealing with menstruation, women have to worry about wearing white, watching embarrassing douche commercials about beach walks with mom, and smelling like blood and dead fish. Even worse is the common rhetoric defining PMS which generally includes emotional rollercoasters and hyper-bitchiness. Instead of being respected as necessary evils associated with being the propagators of all humankind, the insufferable menstrual unpleasantries women endure, unfortunately, are viewed and accepted by society as physical and mental limitations. A woman can’t be trusted to make decisions because every four weeks she becomes completely irrational. A woman can’t fly a fighter because at the first of every month she becomes uncontrollably trigger-happy. No women astronauts or sailors are allowed; there is a problem with the disposal of certain FEMININE PROTECTION in space and sea, and no one wants to be trapped in an enclosed area with an hysterical PMSer. Women can’t go swimming during menstruation because the sharks will attack, and definitely NO HIKING-- the bears will come out of the woods drawn to dinner (or maybe a mate) by Jane’s blood-scented perfume. Whatever! Some husband who didn’t want his poker-playing, beer-drinking, dirty-joke telling camping trip with the buddies spoiled by the presence of his “shackle” made that up! Sound scientific documentation supporting such anecdotal, gender-biased malarkey is hard to find; actually one is more likely to run across studies concluding quite the opposite. ... UNBEARABLE ... Such a study was published in the Journal of Wildlife Management in 1991 in answer to concerns regarding black bears’ attraction to menstrual odors and subsequent attacks on female hikers. The death of two menstruating women attacked by grizzlies in Glacier National Park in 1967 apparently prompted the government to print brochures warning women to avoid bear country during periods of active menstruation. However, the examination of factors surrounding hundreds of grizzly and black bear attacks produced neither evidence that supported a causal relation between human menstruation and attacks nor revealed any published records concerning black bear responses to menstrual blood. The U.S. Forest Service conducted a series of experiments (Rogers et al., 1991) which tested the responses of both male and female black bears to human menstrual odors. The first experiment involved the spin-cast introduction of 15 used tampons (in clusters of 5) to adult male black bears foraging in a garbage dump. Each presentation, therefore, gave the bears a choice between the garbage and tampons. If the bears ate (like they did the garbage), closely sniffed, or rolled on the tampons, then they were considered to have paid attention to the tampons. Of 22 presentations, the bears ignored the used tampons 20 times (twice casual sniffs were observed), effectively preferring the garbage in every instance. In a second experiment, seven bears feeding on piles of corn were offered groups of six used tampons. Six of the bears sniffed the tampons and then returned to their piles of corn. A yearling male tasted one of the tampons, quickly dropped it and returned to the corn. A third experiment placed four used tampons, an unused tampon, a tampon soaked in non-menstrual human blood, and a tampon containing rendered beef fat in the middle of a heavily traveled bear path with the used tampons interspersed among the others. Ten out of ten bears ate only the tampons soaked in beef fat. In a fourth experiment, women on different days of their period accompanied and contacted bears who were accustomed to human interaction and were known to investigate attractive odors. Eleven encounters involved women wearing tampons and one crazy woman wearing clothing through which her menstrual blood was soaking. Of the twelve encounters with the women, the ten bears did not pay any attention to the lower torsos of the women. Another woman wearing external pads during two of her menstrual cycles hand-fed four female bears and walked within two meters of adult male bears during bear mating season and did not receive any attention. Rogers et al. (1991) concluded that the lack of interest of the bears to menstrual odors does not prove that such odors are never attractive to bears (similar experiments resulted in tampon feasts by polar bears lacking attractive buffets); however, menstrual odors essentially were ignored. References Rogers, L L., G.A. Wilker, and S.S. Scott. 1991. Reactions of black bears to human menstrual odors. J. Wildl. Manage. 55(4):632-634. See also Cushing, B. 1983. Responses of polar bears to human menstrual odors. Int. Conf. Bear Res. and Manage. 5:270-274. Herrero, S. 1974. Conflicts between man and grizzly bears in the national parks of North America. Int. Conf. Bear Res. and Manage. 3:121-145. -------. 1985. Bear attacks. Nick Lyons Books, New York, N.Y. 287pp. Insert bear picture Darwin’s Sexy Nose Bear attacks, among other less-desired responses to a woman’s menstrual perfume, do not seem to be frequent consequences of the olfactory influences involving human menstruation. Many scientific journals suggest that human males, on the other hand, respond to vaginal cyclic scents. Doty et al. (1975) described a study which concluded that “the odors of human vaginal secretions vary in both intensity and pleasantness across the stages of the menstrual cycle.” Men were asked to rate both the intensity and pleasantness of odors arising from used tampons from consecutive phases of the menstrual cycle. It was found that even though there was considerable variation across cycles from the same donor, men claimed secretions from pre-ovulatory and ovulatory stages were less intense and more pleasant than during the other phases. Data fell short of providing substantial support to the idea that particular staged menstrual odors were “attractive” to men, and due to heterogeneity of results it “is unlikely that humans can use vaginal odors reliably to determine the general time of ovulation.” “Unlikely” does not mean impossible, and the logical jump made (before or after) with studies such as the aforementioned is to attempt to bridge some evolutionary gap between man and ape, providing a reasonable explanation as to the importance of menstrual olfactory cues in communicating courtship rituals and defining timed mating behaviors in early man. In the December 1974 edition of Science, scientists from Emory University of Medicine published the volatile fatty acid content as determined by gas chromatography of 682 vaginal samples from human females. They noted that fatty acid content “increased during the late follicular phase of of the menstrual cylce and declined progressively during the late luteal phase.” The same volatile aliphatic acids found in the human samples (i.e. acetic, propanoic, methylpropanoic, butanoic, methylbutanoic, and methylpentanoic) have been found ubiquitously in the vaginal secretions of many primate species such as the rhesus monkey, anubis baboon, patas monkey, pigtail monkey, crab-eating monkey, and squirrel monkey. Although scant information is available on the importance of these compounds in humans, say Michael et al. (1974), “The same substances possess sex-attractant properties in other primates.” Interestingly, it was noted that similar attraction reactions resulted when human vaginal secretions where exposed to rhesus monkeys, and that women on oral contraceptives had lower acid amounts and showed no rhythmic changes during their cycle. There is evidence to suggest in rhesus monkeys that other odorous, non-aliphatic compounds present in vaginal secretions serve as distinct cues to males during the preovulatory phase of the menstrual cycle (Goldfoot, 1981). So did man at one time in his early development use scent, like today’s primates, as an important reproductive communicator? Acceptance of the arguement further implicates that somewhere along the evolutionary line of man, menstrual olfactoy cues became obsolete. The subsequent weakening of human’s conscious attraction to vaginal odors resulted in the degeneration of sense of smell found in humans today. Of course, whether one makes the leap connecting primate olfactory cues to early man’s equally intrinsic ability to detect estrous of Cro-magnon Jane or not, it must be accepted that supportive, documented science just does not exist in a less correlative form. References Doty, R.L., M. Ford, G. Preti, and G.R. Huggins. 1975. Changes in the intensity and pleasantness of human vaginal odors during the menstrual cycle. Science 190: 1316- 1317. Goldfoot, D.A. 1981. Olfaction, sexual behavior, and the phermone hypothesis in rhesus monkeys: A critique. Am. Zool. 21(1): 153-164. Michael, R.P., R.W. Bonsall, and P. Warner. 1974. Human vaginal secretions: Volatile fatty acid content. Science 186: 1217-1219. see also Bieber, I. 1959. Am. J. Psychother. 13: 851. Michael, R. P. 1972. Acta. Endocrinol. Suppl. 166: 322. Michael, R.P., E.B. Keverne, and R.W. Bonsall, 1971. Science 172: 964. Rogers, J. and G. Beauchamp, in Mammalian Olfaction, Reproductive Processes and Behavior, R.L. Doty, Ed. (Academic Press, New York, 1974). Stinkin’ Synchin’ The menstrual cycle not only produces odors, rumored to serve as attractive cues, but reacts to external odors as well. One often hears of females living in close proximity undergoing the synchronization of their menstruation onset times. In an article published by Russell et al. (1980), it was stated that “menstrual synchrony is not due to changes in food, awareness of menstrual timing or lunar cycles, and [it is] suggested that the only significant factors seem to be the amount of time the women spend together and the lengths of their cycles.” They conducted a really cool experiment in an attempt to demonstrate if the olfactory cues of one very “regular” woman could influence the timing of menstrual onset in other women. Eleven women, with mean age was 28.5 years, none of whom were lesbians or were taking oral contraceptives, volunteered to have an odor placed on their upper lip three times a week during a four month period. The odor was extracted from the axillary region (the armpit!) of a female donor with a history of a very regular menstrual cycle. She did not use underarm deodorant or perfumed soap, nor was she allowed to wash under her arms during the odor gathering period. Odor collection involved having the donor wear 4X4 cotton pads under her arms for 24 hours. The subjects had the pads rubbed on their upper lips and asked not to wash their faces for six hours. The group of control subjects received the same treatment, with the exception that they did not receive the odor. Test subjects and control subjects had no knowledge as to which group they belonged. The results indicated with statistical significance of p < 0.01 that ododrs from one woman can influence the the mensrtual cycle of another. The mean difference in days between the menstrual onset of tested subjects and the donor at the beginning of the experiment was 9.2 days. This average decreased to 3.4 days by the end of the experiment with four of the five subjects synchronizing to within one day of the donor’s onset. The control group avearged 8.0 days from the donor’s onset in the pre-treatment month and 9.2 days in the post-treatment month. Difference (in Days) Between Menstrual Onset of Donor and Subjects Insert graphs Russell (1980) p 738 Fig 1 Figure 1: Recreated by extrapolation from Russell et al. (1980), these graphs represent the difference (in days) between each subject’s onset of menstruation with that of the donor. Each line represents one individual. The possibility was noted that “the mechanism of [odor] transfer did not involve the nose at all, but diffusion of chemical compounds through the skin which may occur when the sample was placed on the subject’s upper lip.” If compounds placed under the nose were volatile and the subject unaware of their presence, then can one properly use the term “odor” anyway? The olfactory influences on the menstrual cycle of crab-eating monkeys (Macaca fascicularis) have been studied along the same lines as human synch experiments. Wallis et al. (1986) placed twelve female monkeys in adjacent cages allowing for the occurrence of physical contact. Only one of the females had a history of regularly-timed menstruation. A control set was established in the same manner with the exception that cages were situated far enough apart so no physical contact was possible. Within the course of the six month study, the experimental subjects with irregular flow tended to normalize, although cycle synchronization was not observed as a trend. In the control group, irregular subjects continued to experience abnormally long cycles. The authors suggested, “Close physical contact may serve to transmit chemical and/or hormonal cues that can normalize the menstrual cycle of crab-eating monkeys.” References Russell, M.J., G.M. Switz, and K. Thompson. 1980. Olfactory influences on the human menstrual cycle. Pharmacol, Biochem., & Behav. 13: 737-738. Wallis, J. 1986. The effest of female proximity and social interaction on the menstrual cycle of crab-eating monkeys (Macaca fascicularis). Primates 27(1): 83-94. Doty, R.L. 1981. Olfactory communication in humans. Chem. Senses 6(4): 351-376. see also: McClintock, M.K. 1971. Menstrual synchrony and suppression. Nature 229: 244-245. Can animals really smell fear? In everyday speech, the sense of smell is commonly used as a catch-all category meant to represent perception in general. For example, during the course of a day, one might hear the phrases, “I smell a rat,” or, “Something smells fishy” Each of these statements is rarely taken literally--if someone has proclaimed that he smells a rat, the chances are slim that he indeed can detect the odor of a small nocturnal rodent. Instead, he is probably suggesting that he has perceived that something is inappropriate or strange about a specific situation. Likewise, the statement that “something smells fishy” generally suggests that the speaker perceives a reason to be suspicious about a situation. In both utterances, smell is used as the active verb, but is not necessarily relevant to the sentence’s intended message. Instead, smell is used to suggest perception through any or several of the senses. Additionally, the statement that “animals can smell fear” is often heard, and can even be found in current popular literature. Taken literally, this statement seems absurd. Fear is an emotion, an internal response which is generated by an animal’s nervous system when the animal encounters a situation it perceives to be dangerous. It is not a volatile substance. One definition of “smell” given by the American Heritage Dictionary is, “A distinctive quality enveloping or characterizing something.” This gives some validity to such phrases as the “smell of success,” and the “smell of victory.” Likewise, the existence of a “smell of fear” seems slightly less ridiculous when it is considered in the context of such a broad (and non-olfactory) definition of smell. Therefore, it is likely that the statement “animals can smell fear” developed from the idea that animals can sense that a nearby animal is acting strangely, perhaps as a result of an alarm response. It is well-documented that the fear response in most animals includes a series of visual, acoustic, and possibly olfactory stimuli which may alert a potential predator or attacker (Pruitt and Burghardt, 1977; Lorenz and Leyhausen, 1973). Therefore, while it is not possible for an animal to literally smell fear, an individual’s response to fear may include the release of certain odoriferous substances which can be detected by a nearby animal. For example, in humans, the autonomic nervous system is responsible for enacting a stress response. This response is thought to function in preparing the body for immediate protective action. Characteristic physiological changes comprising the fear response in humans include (1) an increased hear rate, (2) an increase in blood supply to the muscles and to the brain, (3) release of glucose into the bloodstream, (4) dilation of the pupils, (5) increased breathing rate, and (6) an increase in sweat gland activity (Janis et al., 1983). In particular, the increase in sweat gland activity which accompanies a stress response in humans may contribute to an olfactory “fear” signal. The human body has two types of sweat glands. The first is the eccrine, or sudoriferous, gland, which is a coiled structure responsible for the regulation of body temperature through evaporation of sweat from the body surface. The second type of sweat gland is called the apocrine gland. Apocrine glands are localized to specific areas of the body with the highest concentrations occurring in the region of the axillary organs (armpits) and the groin area (Stoddart, 1990). In response to emotional stress and sexual stimulation, apocrine glands release secretions through hair follicles. The secretions contain cellular material that is broken down by bacteria, and thus body odor is produced (Memmler et al., 1992). The human stress response may therefore result in the production or intensification of one’s natural body odor which is detectable to a nearby animal. Thompson (1988) suggests that human thermoregulatory responses to stress or fear may provide a valid measure of the intensity of emotion, but do not provide much specific information about which emotion an individual is experiencing. Thus, if a person becomes fearful in the presence of an animal, that animal may be able to detect a new odor, and may therefore be alerted to the person’s presence. it is, however, unlikely that such an olfactory cue provides the animal with enough information to detect that the person is fearful. Additionally, it is unlikely that such an olfactory cue acts alone to incite aggression in the animal. Certain non-human animals may also produce a scent as a result of fear or emotional stress. Fox and Cohen (1977) suggest that, in mammals, the production of odors may render the rank and the emotional state of an animal identifiable. Many mammalian species deposit various odors when they are alarmed. For animals which typically scent mark objects, such as cats and dogs, odors produced as a result of emotional stress are not usually deposited at a specific marking spot. However, the composition of the secretions which are deposited on a traditional or specific marking spot may actually be changed as a result of alarm reactions (Fox and Cohen, 1977). Studies have demonstrated that fear and emotional stress are conditions which may be communicated by odors in mice and rats, as well (Valenta and Rigby, 1968). One study also suggests that the genital scent glands of two prosimian primates are involved in producing a fear scent (Manley, 1974). Chemical signals produced under stress, however, are thought to function in alerting conspecifics of danger, rather than in eliciting aggression in an intruder. Therefore, taken literally, “the smell of fear” might be more appropriately termed “the smell of danger,” and may function as a warning to others after danger has been encountered, rather than being the cause of a dangerous encounter. The use of pheromones to alert conspecifics or members of a social group to the presence of an intruder or a potential attacker is common in many animal species. For example, in the presence of an intruder, several species of social hymenoptera secrete pheromones which cause defensive behavior among conspecifics (Maschwitz, 1966). This “alarm pheromone” is thought to have two effects: (1) it alerts conspecifics to the threat of danger, and (2) it acts as a chemical repellent to the intruder. In this manner, the “fear scent” produced by a honeybee worker does not provoke aggression by a predator, but instead functions in hive protection. If an individual worker detects an intruder to the hive, the bee will release an alarm pheromone. Detection of a foreign odor by a honeybee worker may even be enough to elicit an alarm secretion. This alarm pheromone excites workers in or near the hive, and attracts them to the source, and thus to the intruder. The secretion itself does not cause an attack--the attack-producing stimuli come from the intruder, whose behavior usually guides the attack (Maschwitz, 1966). Therefore, if a person approaches a honeybee hive, his body odor (because it is foreign to the hive) may be sufficient to excite and attract the bees. If the person becomes afraid, and moves erratically, he is likely to be attacked by the bees. So, while smell does play a role in hive defense, the odor which the bees detect is not “the smell of fear,” but more likely is “the smell of something foreign.” And, ultimately, it is visual cues which drive the bees to attack the intruder. Another example of the role that olfactory cues play in communicating alarm among animals is found in carnivorous mammals of the family Mustelidae. Mustelids are distinctive among mammals in their defensive use of anal scent glands to produce olfactory warning signals. All mustelids are characterized as having well developed anal scent glands. In particular, weasels, wolverines, and skunks have been documented to release a repellent odor from these glands when alarmed (Pruitt and Burghardt, 1977). Additionally, during traumatic experiences, the domestic cat and the sand cat are known to void their anal scent glands. The result is a pungent, unpleasant odor, which probably functions in defense as well (Pruitt and Burghardt, 1977). Thus, olfactory signals play a role in the alarm response of these mammals. These olfactory cues, however, appear to function in repelling an opponent rather than in inciting aggression in that opponent. However, if a stressed animal produces a scent which actually causes predators to attack, it is likely that animal will not survive for very long. Thus, it seems that natural selection would quickly act to eliminate animals which produce a “smell of fear” that does not function in some defensive or protective capacity as well. Fear is motivating, and the fear response in most animals includes behavior modification. Therefore, in addition to the production of a “fear scent” by certain mammals (for which evidence does not abound), the fear response in animals includes a series of behaviors which can incite an aggressive response in a potential attacker. Even slight behavioral signs of fear which result from an animal’s detection of a nearby predator might make it more vulnerable to attack. For example, the unusual or irrational movements which result from a fear response can immediately catch a predator’s attention, and result in instantaneous attack (Curio, 1976l). For predatory cats, seeing a small object running away is considered to be the stimulus for chasing (Lorenz and Leyhausen, 1973). Therefore, a cat can quickly detect a panic-stricken mouse through visual stimuli alone. Many police departments and search-and rescue squads use trained dogs to track both suspects and victims through olfactory cues. Usually, the dog is presented with an item on which the object of a search’s odor may be detected, and the dog then follows a scent trail which will presumably lead to the person. The role of a possible “fear scent” in directing a trained dog to a suspect is not well documented. One contributor to the K-9 Academy for Law Enforcement Trainer’s Resource Centers Web page suggests that, “If you want to train your canine to pick out all the people who are afraid, you can do that . . . a guilty persons odor is coming out like a smoke bomb and smells of ‘fear’.” However, evidence which supports this claim remains anecdotal1,2, as systematic study in this area is difficult. Nonetheless, Sigma Pseudochemicals does offer vials of human “fear scent” to those purchasers who are interested. In the strictest sense, it is doubtful that animals can smell fear. Some animals have been documented to release a scent in response to stress. Such a “fear scent” may play some role in alerting a potential attacker. However, it is more likely that an animal will become aggressive towards a fearful individual as a result of a combination of multiple sensory and behavioral cues. While odor may play a significant role in attack behaviors among animals, olfactory cues probably do not function alone to incite aggression in mammals. Notes 1 Morris R. Atwell related a personal training experience: My dogs are trained for cadaver search using both pseudo corpse and the real thing. There was a pseudo scent called ‘fear and trauma’ introduced to them at a training session. The very first alert on this scent was very interesting to me. Each dog reacted slightly different but both alerts were different for a normal cadaver find. You could tell when the dog came into the scent cone. One dog stopped smelled the wind, and took a more timid ‘sneak up’ approach on where this scent material was buried. He was very tentative in his approach and scratching at the area. He approached the area with body lower to the ground and did a very tentative initial investigation. I guess once he discovered nothing was going to jump out and attack - he did finally give a few barks. The second dog reacted differently. When she came into the scent cone - she immediately turned toward the scent. Body seemed to swell up and she became more stiff legged on her approach. Her approach was more straight to the scent. When she got to the area of the buried scent, she looked all around, sniffed the air, then went into her sniffing, barking alert. This only happened the first time they were exposed to the ‘fear and trauma’ scent material. Now they alert to it just like they do for all cadaver work. 2 Heather E. Houlahan related an anecdote: The one time my older dog, Lilly, was searching for (and found) a person who was alive and terrified, she alerted to him from an extraordinary distance -- almost a mile by air scent -- and was highly agitated while working out the scent. That said, there are two alternative explanations for what happened (1) the lost person had been in place overnight -- longer than a “practice victim” will stay out for us, and thus his scent had been dispersing far and wide and (2) members of the search party, including me, were afraid that this person had committed suicide -- we were undoubtedly telegraphing anxiety by our voices, body language, etc. References Curio, E. 1976. Zoophysiology and Ecology: The Ethology of Predation. Vol 7. New York: Springer-Verlag. Fox, M.W. and J.A Cohen. Canid Communication, in Sebeok. 1977. How Animals Communicate. Bloomington: Indiana University Press. Janis, I. P. Defares, and P. Grossman. 1983. Seyle’s Guide to Stress Research. (H. Seyle, ed.) Vol 3, pp. 1-42. New York: Scientific and Academic Editions. Lorenz, K. and Leyhausen, P. 1973. Motivation of Human and Animal Behavior: An Ethological View. New York: D. Van Norstrand. Manley, G. H. Functions of the external genital glands of Perodicticus and Arctocebus. In Doty, R. L. 1976. Mammalian Olfaction, Reproductive Processes, and Behavior. New York: Academic Press. Maschwitz, U. W. 1966. Alarm substances and alarm behavior in social insects. Vitamins Hormones. 24: 267-290. Memmler, R. L., B. J. Cohen, and D. L. Wood. 1992. The Skin, in Structure and Function of the Human Body. Edition 5. Philadelphia: J. B. Lippincott Company. Pruitt, C. H. and G. M. Burghardt. Communication in Terrestrial Carnivores: Mustelidae, Procyonidae, and Ursidae, in Sebeok. 1977. How Animals Communicate. Bloomington: Indiana University Press. Stoddart, D. M. 1990. The Scented Ape: The Biology and Culture of Human Odor. New York: Cambridge University Press. Thompson, J. G. 1988. The Psychobiology of Emotions. New York: Plenum Press. Valenta, J. G. and M. K. Rigby. Discrimination of the odor of stressed rats. In Doty, R. L. 1976. Mammalian Olfaction, Reproductive Processes, and Behavior. New York: Academic Press. Do Members of Different Cultures Have Characteristic Body Odors? Post-Darwinian anthropology developed the idea that different races or ethnic groups have characteristically different body odors (Corbin, 1986). However questionable some may seem, such claims are not difficult to uncover: “Negrids have strong and disagreeable odours, irrespective of the amount of axillary washing.” (Stoddart, 1990). “When white men and black men bathe together in the ocean, the black men, who smell more strongly than the white, are more susceptible to the ferocity of sharks.” (Lacepede, in Budker, 1971). “Australids have an odor of ‘phosphoric character’; central African women a slight ‘gout de noisette’” (Ellis, in Stoddart, 1990). “[The specific odor] of the Caribs is reminiscent of kennels.” (Virey, in Stoddart, 1990). Regardless of the possible validity of such claims, the concept that specific odors characterize different races was probably propagated as a means of setting certain races and cultures apart from others. Notice that each of these comments seems to be a derogatory assessment of the body odors emanated by members of other groups. This suggests that the idea of culturally specific odors may be a product of racially separatist ideals. While Classen (1994) states that there is no validity to claims that different races differ in their characteristic body odors, a physiology textbook last revised in 1968 claims, “In humans, there are characteristic racial smells” (Davson and Eggleton, 1968). The paragraphs that follow describe possible mechanisms by which human social groups may develop characteristically different body odors. Each individual is thought to have a genetically determined odortype, or personal odor, which is determined by genes located in the major histocompatability complex (Stoddart, 1990; Wysocki, pers. comm.) This genetically determined odortype may be affected by certain factors. Several such factors include an individual’s diet, sweat gland distribution and activity, and application of scented products to the body. For example, the types of food which are consumed by an individual may affect that person’s body odor (Wysocki, pers. comm.) Typical food items consumed may vary among cultures. Food consumption may contribute to a characteristic odor exuded by members of cultures or social groups in which all members share a common diet. For instance, the body odors of groups whose diet consists of very spicy foods may be recognizably different from the odors of a social group whose diet consists of bland foods. However, there can be immense variation in the types of food consumed both within a culture and within a region. For evidence of this, one only has to look as far as central South Carolina alone, which both vegans and hard-core “meat-and-potatoes” advocates call home. Clearly, it is unlikely that these individuals, though they may be members of a common culture, have similar body odors based on diet. However, among cultures or social groups which are wedded to a generally unchanging diet staple that differs from that of other groups, such a claim may be valid. For example, Corbin (1986) writes that in nineteenth century France, “Regional populations exhaled specific odors . . . as a result of the kind of food they ate.” Classen et al. (1994) also write of Amazonian rain forest tribes: The Deseana, who are hunters, are said to exude the musky smell of the game which they eat. Their neighbors, the Tapuya, on the other hand, live by fishing and are thought to smell of fish. The nearby Tukano are agriculturalists and they, in turn, are said to smell of the roots, tubers and vegetables which they grow in their fields. Such characteristic odors, however, may also be the result of the food preparations undertaken by members of each tribe. Fishermen, for example, are likely to smell of the fish they catch and handle; likewise, hunters may aquire the smell of the game they hunt as a result of preparing the animal after a kill. Another potential factor affecting human body odor is the scent-producing glands found in the skin. Variation among cultures and geographic regions in the number, arrangement, and activity of scent-producing sweat glands has been suggested (Stoddart, 1990; Davson and Eggleton, 1968). Like most mammals, humans have two types of sweat glands. One type is the eccrine, or sudoriferous, glands, which serve a cooling function. The sweat secretions which pass through the lumen of eccrine glands are never accompanied by cell secretions. Thus, scent-producing substances which are byproducts of cell metabolism are not secreted by these glands (Stoddart, 1990; Davson and Eggleton, 1968). The second type of sweat gland found in humans, called apocrine glands, are responsible for the production of body odor. Portions of secretory cells found near these glands enter the gland’s lumen along with the sweat secretions. These cells secrete a substance which contains fats and proteins. When apocrine sweat, combined with cell secretions, reaches the skin’s surface, the normal flora of the skin act on the sweat to produce body odor (Davson and Eggleton, 1968). While eccrine glands are distributed more or less uniformly across the skin, the densest collections of apocrine glands in the human body occur in the axillary organs (armpits). Clusters of apocrine glands are also found in the suprapubic region, circumanal region, perineum, face, scalp, and umbilical region of the abdomen. It has been suggested that distribution and abundance of apocrine glands within the axilla of different races produces a characteristic racial body odor (Stoddart, 1990; Davson and Eggleton, 1968). One study generalized that among Africans and Europeans, axillary organs are quite large and well-developed, with highly active apocrine glands. Mongolians, conversely, have weakly developed axilla. This study estimated that one-half of the Korean population has no apocrine glands in its axillary organs, and of the half that does, the glands are quite sparse. This study also estimates that ten percent of Japanese and only two to three percent of Chinese have an axillary odor (Stoddart, 1990). In his treatment of this subject, however, Stoddart (1990) points out that most of the data supporting this claim appears to have been collected before 1930. Perhaps lack of attention to this topic in recent years is an indication that the search for physical characteristics which set races of people apart is no longer as important as it has been in the past. Furthermore, individual odor is affected by the types of scented products an individual applies to his or her body. Use of scented products may also vary among cultures; members of cultures which use scented products liberally are likely to smell differently than members of cultures who rarely apply such products to their bodies. Clearly, personal body odor is affected by any of several factors. The types of food consumed, use of scented products, and even the distribution and abundance of scent-producing glands in the skin may vary from culture to culture. The interplay of these factors may result in a body odor which is specific to a culture or geographic region. However, the variation of each of these factors within a culture or geographic region can be tremendous. Likewise, descriptions of body odors remain somewhat subjective. As a result, systematic study of such a phenomenon is difficult to attain. References Budker, P. 1971. The Life of Sharks. New York: Columbia University Press. Corbin, A. 1986. The Foul and the Fragrant: Odor and the French Social Imagination. Cambridge: Harvard University Press. Classen, C., D. Howes, and A. Synnott. 1994. Aroma: The Cultural History of Smell. New York: Routledge Press. Classen, C. D. 1994 in Compendium of Olfactory Research 1982-1994. Davson, H. and M. G. Eggleton. 1968. Principles of Human Physiology. Philadelphia: Lea and Febiger. Stoddart, D. M. 1990. The Scented Ape: The Biology and Culture of Human Odor. New York: Cambridge University Press. Does smoking affect the sense of smell? The 1986 National Geographic Smell Survey indicated that, of the people polled, smokers rated the intensity of androstenone, cloves, and gas as weaker than those of nonsmokers, while banana and musk were perceived as stronger by smokers. However, smokers and nonsmokers did not differ in their detection of the rose scent. Additionally, smokers were less confident in their own ability to detect odors. As expected, smokers’ responses to the survey demonstrated a lowered sensitivity to odor quality. Smokers found the odors rated as unpleasant by nonsmokers to be less offensive, and indicated a decreased appreciation of the pleasant odors, as well. (Gilbert and Wysocki, 1987). In an additional study conducted at the University of Indiana, 100 students were asked to use their noses to locate their own shirts from an assortment of shirts. Seventy-four of the 100 students were able to correctly identify their own shirts by scent alone. However, of participants that smoked more than ten cigarettes per day, almost half were unable to correctly identify their own shirts (Lord and Kasprazak, 1989). References Gilbert, A. N. and C. J. Wysocki. 1987. The Smell Survey Results. National Geographic. October. pp. 514-525. Lord, T. and Kasprzak, M. 1989. Identification of self through olfaction. Perceptual and Motor Skills. 69(1): 219-224. Do pregnant women experience a heightened sense of smell? Anecdotal evidence suggests that women experience a heightened sense of smell during pregnancy. Data collected from 13,610 pregnant women and 277,228 non-pregnant women during the 1986 National Geographic Smell Survey suggests that this may not be the case. The survey results indicated that pregnant women rated their own olfactory abilities lower than women who were not pregnant, although the two groups did not differ significantly in their abilities to perceive the odors tested. Although the data are not statistically significant, pregnant women more often found the odors tested to be unpleasant and were less likely to indicate that they would ingest the odors. Additionally, pregnant women did not experience scent-induced memories as commonly as non-pregnant women (Gilbert and Wysocki, 1991). References Gilbert, A. N and C. J. Wysocki. 1991. Quantitative assessment of olfactory experience during pregnancy. Psychosomatic Medicine. 53: 693-700. What role does hair color play in odor and olfaction? This was a tough one. But, here are a couple of interesting quotes: Alain Corbin, in The Foul and The Fragrant (1986), writes of nineteenth century France: Oddly, medical discourse concerned itself little with the specific relation of smell to temperament, the color of hair, or complexion. The odor peculiar to irascible personalities and the smell of redheads were noted, but without emphasis, as if they were self evident. He later adds, “redheads were always pungent, both putrid and fascinating, as if their cycle had broken down and put them in a continuous state of menstruation.” We also found this interesting tidbit on the Net: There is a study done by a scientist which states that the color of a canine has a direct effect on the scenting ability. For instance, a white canine does not possess the same ability to scent as does a canine which is darker in color. That is one of the reasons you will never see a white canine in police service in foreign countries. The pigment of the canine’s skin or hair has a direct effect on his ability to smell. (Bill Syrotuk) Do human pheromones exist? According to an article printed in the Seattle Times, the Athena Institute for Women’s Wellness in Haverford, Pennsylvania has patented a chemical copy of “the human pheromone,” synthesized from a chemical found in sweat. The journalist states, “Like all animal pheromones, [the pheromone] is believed to stimulate response to the opposite sex.” Thirty-eight men participated in the company’s study testing the chemical. Seventeen used an aftershave to which a drop of the chemical was added, and twenty-one used untreated aftershave. The men were asked to document all sexual activities for the duration of the experiment. Results indiated that all of the “pheromone” users “turned out to be busier, sexually,” than the twenty-one controls. Based on these results, the researchers concluded that, “Human pheromones caused a statistically significant and distinct increase in those romantic behaviors in which a woman plays a major role . . . Thus, human pheromones affect the sexual attractiveness of men to women.” If you’re interested, you can pick up a vial for a mere $99.50 by mail order. (The State, 1995) With the expectation that 5-a-androst-16en-3a-on, the main component of male body odor, might be a human male pheromone, an additional study rated the responses of 289 women to the chemical’s odor. The women’s responses to the quality of the odor differed, depending on the stage of their menstrual cycle. During ovulation, women rated the odor as neither attractive nor unattractive. However, during other phases of their menstrual cycles, women rated the scent as uanttractive. An evolutionary consequence might be the facilitation of female choice during ovulation (Grammer, 1993). Additionally, the Results of the 1986 National Geographic Smell Survey indicate that women were more sensitive to the smell of androstenone than were men. References Gilbert, A. N. and C. J. Wysocki. 1987. The Smell Survey Results. National Geographic. October. pp. 514-525 Grammer, K. 1993. 5-a-androst-16en-3a-on: A male pheromone? A brief report. Ethology and Sociobiology. 14(3):201-207. “Nothing attracts the opposite sex like the odor of perspiration.” The State. October 15, 1995. In Conclusion Lucid answers to many of these questions cannot be extracted from this text; a simple function of not every myth having a definable reality. What we have presented, though, is a smidgen of what the literature says. We ask you neither to accept these statements as fact nor reject them as folly. We would, however, like for you to take from this an insight we ourselves have gained: Our sense of smell, however unappreciated and unconsciously devalued it seems, has permeated into the intergral matrix of man’s social existence. It manipulates our languages, our emotions, our reactions, and our physiology. We, as humans, unknowingly define ourselves through smell, and we always, always follow our noses.