Chapter 18 Human Body Odour Individuality Pavlina Lenochova and Jan Havlicek Abstract Humans produce temporarily stable, genetically mediated odour signatures and possess the ability to recognise, discriminate and identify other people through the sense of smell. The capability of self, gender, kin and non-kin odour recognition plays a role in social interactions. It seems that despite the stability of olfactory cues, the hedonic quality of body odour may vary over time. 18.1 Introduction “It is the odour of a body what invites for love feast, not its beauty. . .” (Asklepiades from Erithrea, Greek philosopher and rhetorician, 124-60 BC) Human skin is covered with abundant apocrine, eccrine and sebaceous glands. The latter produces a fatty sebum over the whole body surface, especially on the chest, back, forehead, cheeks, scalp, breast areolae and external genitals. The highest incidence of eccrine glands occurs in axillae, palm, sole and forehead areas. In contrast, apocrine glands are only bound to tertiary hair and are to be found in the regions of axillae, external genitals, eyelids, nipples, around the umbilicus and in the ears and nose. Fresh secretion (fat sebum and sweat) of these glands is virtually odourless but the metabolic activity of skin bacteria transforms it to odourous compounds (Leyden, McGinley, Holzle, Labows and Kligman 1981). The characteristic odour of every human, called the “body odour signature”, is an essential source of information about the odour producer. Axillary area is the pivotal place of personal odour origin. Due to the upright posture in recent humans it is especially suitable for chemical communication. Axillary substances are potential cues of individuality, gender, reproductive status, age, health, diet, smoking habits, hygiene and so on. The main aim of this paper is to review studies dealing with different aspects of body odour individuality. We mainly focus on odour recognition of (1) gender specific cues, (2) self and sexual partner Pavlina Lenochova Charles University, Department of Anthropology and Human Genetics [email protected] J.L. Hurst et al., Chemical Signals in Vertebrates 11. C Springer 2008 189 190 P. Lenochova, J. Havlicek cues, (3) kin cues and (4) mother-infant cues. Subsequently, we discuss possible proximal causes of odour individuality. 18.2 Sex Differences It is probable that besides individual characteristics, some general olfactory features differentiate the two sexes. Resulting from these differences, people can distinguish between males and females through smell alone. After experiencing both male and female hand odours, a group of eight women and eight men, blindfolded, went through thirty trials trying to identify the source of odour as one of those introduced previously. During the session, the raters were informed of the correctness of their judgment, thus systematic learning of the target odours could occur (Wallace 1997). In another study a three-choice discrimination test was used while the subject’s own T-shirt, a strange male’s and strange female’s T-shirt was evaluated. A significant ability to discriminate the sexes on the basis of olfactory cues was found. Male odours were in most cases described as musky and female odours as sweet (Russell 1976). The capability of discrimination between male and female axillary odours was further shown in a cross-cultural study in 20% of Italian, 30% of German and 60% of Japanese raters. T-shirts worn for 7 consecutive nights were laid out in a separate room, then taken by the subject and evaluated for olfactory sex recognition and hedonic qualities, confirming the quality difference in the two sexes’ odour (Schleidt, Hold and Attili 1981). In most studies the female odours were evaluated as more pleasant and male odours as unpleasant (Doty, Green, Ram and Yankell 1982; Schleidt et al. 1981; Schleidt 1980). These ratings often negatively correlated with the odour intensity (Havlicek, Bartos, Dvorakova and Flegr 2006; Weisfeld, Czilli, Phillips, Gall and Lichtman 2003; Doty, Kligman, Leyden and Orndorff 1978). An inverse relationship between the perceived intensity and pleasantness of body odour has also been shown in a study where people tried to identify gender from oral odours. After sniffing breath scents from glass tubes (the donors were hidden behind plywood barriers), the judges assessed the male odours as more intense and less pleasant (Doty et al. 1982). Even if people only suppose some odour to be male, they tend to judge it as rather unpleasant (Schleidt 1980). The subjectively perceived qualitative variance between the two sexes’ odours may be attributed to different levels of sex steroid homornes. However, analytical studies did not discover any qualitative differences in male and female odours (Zeng, Leyden, Spielman and Preti 1996). Only variable levels of steroid substances, like androstenes, have been found (Gower et al. 1985). It has been shown that women’s body odour changes across their menstrual cycle (Havlicek et al. 2006; Singh and Bronstad 2001). Odours of women in the fertile phase were rated as the least intense and the most attractive. This may result in misidentification of women’s gender in some phases of their cycle (e.g. in menstrual phase). Another possible explanation is the fact that women have on average smaller apocrine glands than men and therefore produce less intense body odour 18 Human Body Odour Individuality 191 (Doty 1977). To sum up, men and women differ in their body odour, thus the two sexes can be discriminated but often the commonly perceived divergence in hedonic qualities of male and female body odour are likely to be a result of different intensity. 18.3 Self-Recognition and Sexual Partner’s Odour The ability to recognize one’s own body odour was tested for the first time by Russell (1976). The participants had to pick out their own T-shirt from a group of three placed in wax-coated cardboard buckets with a small hole for sniffing. Thirteen of the sixteen males and nine of the thirteen females answered correctly. Raters in a different study had a much harder choice. Only one-third of the subjects identified their own odour correctly, but this time their own odour was one among another nine T-shirts (Hold and Schleidt 1977). These results were however still significantly better from chance. The shirts were laid out randomly in a row in a separate experimental room without any external covering and the raters were tested simultaneously, thus the actual proportion of subjects able to recognize their own sample could be underestimated as a consequence of touching the samples and interfusion of odours. The quality of own scents was evaluated more often as being pleasant in women and more often unpleasant in men (Schleidt et al. 1981; Hold and Schleidt 1977). Elsewhere, a comparison of self-odour hedonic evaluation was made between a group of people who had a strictly prescribed hygienic treatment and participants without any restrictions, who followed their usual personal hygienic routine (i.e. using perfumes). In the former, men rated their odour as unpleasant, unlike the latter group, where men assessed their odour as predominantly pleasant. Women in both groups described their scents as mainly pleasant (Schleidt 1980). Different results were found when after three hours of sampling axillary secretions the participants tried to find their own gauze in a group of five vials and evaluated all samples for the hedonic quality. 59.4% of females, but only 5.6 % of males were able to identify their self-odour. At the same time, women tended to rate their own secretions as significantly less pleasant than males (Platek, Burch and Gallup 2001). Apart from the self-odour, another scent which one would expect to be relatively familiar with—due to frequent contact with naked skin—is body odour of a sexual partner. Twenty-four couples were recruited for the study of Hold and Schleidt (1977). Their T-shirts, worn for seven consecutive nights, were used for the experiment with nine other samples. Correct identification of the partner’s Tshirt on the basis of individual odour qualities were found in one third of the subjects. The odour of the partner was judged as predominantly pleasant (Hold and Schleidt 1977). In another study, no hygienic restrictions were demanded in the group of participants while odour sampling. Even though they could use any perfumes and deodorants, the partner’s body odour recognition was comparable to that in the previous study (Schleidt 1980). From the cross-cultural point of view, the sexual partners’ body odours were evaluated more often as pleasant in German 192 P. Lenochova, J. Havlicek females than in Italian and Japanese females, while in men no cross-cultural differences were found (Schleidt et al. 1981). On the whole, it seems that humans are able to recognize their own body odour and women mostly tend to assess it as pleasant and men mostly as unpleasant. The significant results from experiments dealing with the question of the sexual partner’s body odour recognition indicate that humans can learn their partner’s olfactory cues, probably through their mutual intimacy. 18.4 Kin Recognition Most likely, specific olfactory cues (genetically based similarities in body odours) are perceivable among all family members. During human evolution, the ability of distinguishing kin from non-kin might have played an important role in kin altruism and inbreeding avoidance. Individuals with the advantage of discerning a kin member could have had higher levels of survival, successful reproduction and consequently higher fitness. Olfactory kin recognition was tested for the first time by Porter and Moore (1981). A T-shirt of one child was sniffed in a two-choice test, together with a T-shirt worn by an unfamiliar, age-matched individual, by the child’s mother and by a sibling. Mothers and siblings alike were able to discriminate their relative’s scent (Porter and Moore 1981). The possibility that the sibling’s odour is discernable simply due to shared environmental cues, was dismissed by Porter et al. (1986). Siblings who had lived a long time apart rated the odours of their brother or sister and a control person of the same sex and age. Twenty-seven of the forty subjects correctly identified the shirt worn for three nights by their sibling. This significant result supports the probable existence of family olfactory cues (Porter, Balogh, Cernoch and Franchi 1986). Recognition of kin is expected to fluctuate according to the level of consanguinity. The closer the family members are the more similar olfactory signatures with more family cues they could have. Varying degrees of consanguinity were observed in a study of Porter et al. (1986), where newborn babies’ fathers, grandmothers and aunts, who were exposed to its odour before testing, identified correctly the odour of donor infant. Later on, the odour was described by fathers as similar to their own or the newborn mother’s body odour. Positive results in relatively distant relatives (i.e. aunts and grandmothers) can be explained by the fact of a prior knowledge about the aim of study and consequent possibility of self-training. Thus, level of consanguinity did not show an effect on ability to recognise relative newborn baby. Different levels of consanguinity were the main topic of another study in which preadolescent children identified their full siblings (first-degree relatives) but not half siblings or step-siblings (further relatives) by the odour (Weisfeld et al. 2003). In the same study, twenty-two Canadian university students were tested for the ability to discriminate the odours of their mother, father, a brother, a sister, a familiar but unrelated person, a stranger, and themselves. Kin members were rarely confused with non-kin and the participants remarked that even though the scent very often 18 Human Body Odour Individuality 193 resembled a familiar one, they were not sure to which target person it belonged to. Close relatives of one species seem to have a similar but individually distinguishable odour signature. Discrimination between kin and non-kin is also connected with the phenomenon of inbreeding avoidance and incest taboo. The combination of related genes might mean a lower probability of viability of the offspring. Hedonic evaluations of kin members’ odours provide good support for these suggestions. People recognized their relatives’ odour but described it as less pleasant than the odour of a non-kin person in general. A mutual father-daughter and brother-sister aversion was found as most significant in tests of preferences of odours in the nuclear family (Weisfeld et al. 2003). These relationships are the examples of the greatest danger of incest. The exact mechanism of kin recognition is not yet fully explained, but there are two main theories. Firstly, odour association may be an important factor in individual odour discrimination based on olfactory imprinting during the sensitive period of life (“sensitive period phenomenon”). Thus, the recognition of sibling’s odour could be strengthened through exposure to a sibling during childhood (e.g. Porter et al. 1986). Secondly, the family member cue provides support for the mechanism of “phenotypic matching”. On the basis of similar features in the odour signature, the individuals may discriminate between the stimuli of known kin and those of possible kin. For example, T-shirts of mothers and their children were correctly matched by non-kin raters on the basis of perceivable similarities (Porter, Cernoch and Balogh 1985). 18.5 Mother-Infant Recognition The special case in kin recognition studies is mutual recognition of mothers and newborn infants. Presumably, olfaction plays a crucial role in the mother-infant first contact and the linking-up of their mutual relationship. In a study testing the olfactory phenotype matching theory (see above), a child’s garment together with garments worn by unfamiliar children were presented in cardboard buckets and mothers were asked to decide which one belonged to their own baby. It was found that newly-parturient mothers can identify their own infants based on body odour within the first six days postpartum (Porter, Cernoch and McLaughlin 1983). To test whether mothers are especially sensitive for infant recognition, a group of non-mothers was also asked to participate. After 45 minutes of cradling a baby, women tested its undershirt. Unexpectedly, it was found that there was no difference between mothers and non-mothers in this task (Kaitz and Eidelman 1991). The authors concluded that both mothers and non-mothers can learn an infant’s odour features and they do so without intention during the course of routine interactions. Another experiment using pre-exposure to the target odours came to similar conclusions: no improved ability of infant odour identification was found amongst mothers than non-mothers (Fleming, Corter, Surbey, Franks and Steiner 1995). These authors suggest that mothers are not uniquely primed to recognize the infant 194 P. Lenochova, J. Havlicek odours. In the second part of the study, the authors focused on factors associated with the successful recognition. They discovered that the amount of time spent with the child in the first day after the delivery positively influences the mother’s success in odour recognition. In addition, mothers who were able to recognize their infant’s odour differed from mothers who were not in having a shorter interval to first breast-feeding, more nurturing attitudes and closer nasal interactions with the child. A newborn’s ability to recognise its mother is the other side of the coin. First contact with maternal olfactory stimuli occurs in utero. The child is in an environment poor in external visual and auditory stimuli and olfaction might have an outstanding role in perception of the surroundings. A rich range of chemical information probably stimulates fetal chemoreceptors via the flow of the amniotic fluid through the nasal passages of the baby (Davis and Porter 1991). The odour of amniotic fluid itself was a main interest in several previous studies. It is supposed that there are characteristic familiar cues in the odour of the amniotic fluid. The study of Schaal and Marlier (1998) showed that both mothers and fathers are able to discriminate and accurately identify the odour of amniotic fluid from their own infant at a betterthan-chance level. The scent of amniotic fluid was described as similar to the body odour of the mother, especially at the end of gestation (Schaal and Marlier 1998). The individually unique quality of amniotic fluid is confirmed by the newborn infant’s own responsiveness to its odour. Own amniotic fluid and a control stimulus were presented to 2 day old newborns. Most frequently, infants turned their head to a gauze pad scented with their own amniotic fluid odour (Schaal, Marlier and Soussignan 1995). Neither differences between breast-fed and bottle-fed neonates nor between the two sexes were found. The authors interpret the amniotic fluid preference as a consequence of its odour similarity to lacteal secretions, which might help while breast-feeding. The uniqueness of olfactory cues in amniotic fluid has also been shown in several other studies. Immediately after parturition, the newborn was washed and one nipple of the mother was moistened with a small amount of amniotic fluid. The baby was then laid between the mother’s breasts and, during the initial attempt to locate the mother’s nipple, spontaneous choice of the nipple scented with amniotic fluid occurred (Varendi, Porter and Winberg 1996). In the study of Marlier et al. (1997), however, 2 day old breast-fed children did not show preferential reaction to amniotic fluid or to lacteal secretions. At four days of age, they preferred odour of milk (Marlier, Schaal and Soussignan 1997). On the contrary, one year later the same research team found somewhat different results. Two and four day old bottle-fed neonates were exposed to the odours of their amniotic fluid, formula milk and distilled water as a control sample. Both 2 and 4 day old infants preferred the amniotic fluid to the odour of formula milk (Marlier, Schaal and Soussignan 1998a). A discrepancy between these two studies can be explained by different development of preferences in breast fed and bottle fed infants. Positive attraction to amniotic fluid was also found in the work of Schaal et al. (1998). At the age of three days, both breast-fed and bottle-fed neonates preferred their familiar amniotic fluid, when presented together with a non-familiar one, and a familiar or non-familiar amniotic fluid when presented with the control stimulus (Schaal, Marlier and Soussignan 1998). Another study by Marlier et al. (1998b) convinc- 18 Human Body Odour Individuality 195 ingly documents the fluent transition of preferences from amniotic fluid to lacteal odours. When the reactions of 2 day old breast-fed neonates to presented pairs of stimuli (amniotic fluid, colostrum or control) were compared, the amniotic fluid was favoured at this age. On the other hand, 4 day old children preferred milk to amniotic fluid and the control. It seemed that with increasing age and exposure to feeding cues, infants display greater attraction to their mothers’ lacteal odour than to their own amniotic fluid odour (Marlier, Schaal and Soussignan 1998b). The last study to be mentioned here examined whether the odours of amniotic fluid, mother’s breast or a control stimulus influence the crying of the newborn infant. After the first breast-feed, at the moment of the first distance of crying, the infants were exposed to one of the odourous samples. Infants exposed to amniotic fluid cried significantly less than other exposed to the other stimuli (Varendi, Christensson, Porter and Winberg 1998). Despite the fact that the opportunity for breast odour sampling was no more than two hours, which could explain the lack of ameliorative effect of breast odour, the importance of familiar amniotic fluid smell is obvious. To sum up, the attraction to amniotic fluid odour may reflect foetal exposure to that substance. The human foetus can detect and store the unique chemosensory information available in the prenatal environment and thus prenatal experience might influence the earliest odour preferences. In the last three decades, the question of discernible uniqueness of mother’s odour for its newborn baby has been tested repeatedly. It is thought that, early in life, the key olfactory cues are produced by the mother’s nipple and areola region, which may support the first successful suckling (Schaal, Doucet, Sagot, Hertling and Soussignan 2006). In the first, second and sixth week after delivery, the mostly sleeping children smelled cotton pads impregnated with an odourless substance, then pads worn for three hours in the breast area of their mother and another lactating mother (Russell 1976). There was no difference between the one and 2 week old newborns’ responses. At the age of six weeks, 6/10 of infants identified their mother’s odour from the non-mother’s. The author suggests the possibility that this effect could be explained by the infant’s own scent contaminating the odour of the mother’s skin during earlier contacts (Russell 1976). However, the value of odours produced by the lactating woman’s breast was confirmed in the Makin and Porter study (1989). A group of full-term, 2 week old, healthy but bottle-fed neonates was exposed to three samples: a breast sample of an unrelated non-parturient female, a breast sample of an unrelated lactating mother and an axillary odour sample of the same unrelated female. In a series of two-choice tests, children oriented preferentially to the breast sample of the lactating woman without any previous exposure to her odour, indicating the attractiveness of the areolar odour for newborns in general (Makin and Porter 1989). Varendi et al. (1994) provided another supportive study confirming the extraordinary importance of breast odour. They washed one randomly chosen breast of mothers immediately after delivery, placed the newborn between her breasts and observed that the most children spontaneously chose the unwashed one, grasped a nipple and started to suckle (Varendi, Porter and Winberg 1994). Additionally, preference for familiar axillary odours has been tested. Two week-old breast-fed newborns sniffed their own mother’s axillary odour for a longer time than samples 196 P. Lenochova, J. Havlicek of control women (Cernoch and Porter 1985). No similar preference for the father’s odour was found. A different reaction was found in bottle-fed newborns of the same age. They were not able to recognize the odour of their mother, which indicated the lack of familiarization of the mother’s unique olfactory signature, presumably because of reduced contact with her naked skin. This same effect could also explain the lack of preference for father’s odours. 18.6 Stability of Odour Quality The origin of odour individuality could be at least partly explained by genetic factors. This is supported by several twin studies. As monozygotic twins possess the same genotype, it is supposed that their olfactory signatures would resemble each other. The hand odours of two female monozygotic twins, having been on the same diet for three days, and two female twins on a different diet, were judged by nine women. The number of correct discriminations between the two twins was better than chance in both groups. The hand odours of twins on different diets were significantly easier to recognize (Wallace 1977). In another study, cotton pads worn for one night in the axillae of twins living apart were gathered and presented to subjects who tried to match the odours of the twins together (Roberts, Gosling, Spector, Miller, Penn and Petrie 2005). Scents of identical twins were matched by raters better than could be expected by chance and with higher frequency than odours of dizygotic twins. Duplicate odour samples of the same individual were correctly matched with the same frequency as matching the identical twins scents. This suggests high odour similarity in pairs of twins which can be perceived by human nose, even if the siblings live apart. Influence of genetic factors on the odour signature predicts its relative stability throughout life. On the other hand, body odour can be shaped by a number of environmental factors as well, including diet and reproductive or health status (for review see Havlicek and Lenochova in this issue). It was shown by Porter et al. (1985) that environmental influences alone cannot produce sufficiently similar body odours to enable matching of two unrelated individuals. They asked spouses who lived together to wear T-shirts, and then asked unfamiliar raters to match the spouses according to their smell. Raters were not able to match odours of spouses at rates different from chance. Thus, genetic factors seem to be crucial for individual or kin recognition 18.7 Conclusions The main aim of this paper was to document in which social contexts human body odour individuality may be functionally important. There is clear evidence that humans can recognize other people and discriminate or identify their body odour. Contrary to traditional thinking, smell therefore has the potential to be an integral 18 Human Body Odour Individuality 197 part of nonverbal behaviour and plays a role in social interactions and establishment of relationships. Olfactory communication appears highly important in very early human development, potentially facilitating the mutual mother-infant relationship. The majority of studies are based on conscious and verbally declared recognition. We suggest that this approach might in fact underestimate the significance of odour cues. It is expected that odour perception partly runs on the subconscious level. Presumably, humans perceive the unique body odour of other individuals and evaluate its hedonic quality being not always fully aware of it. This is supported by some studies based on EEG (Electroencephalography) (e.g. Pause, Krauel, Sojka and Ferstl 1998). However, it still presents a field to be explored. Although the olfactory signature seems to be genetically mediated and consequently stable over the time, our data indicate that its quality could oscillate, possibly due to environmental factors. Acknowledgments We were funded by the Josef, Marie and Zdenka Hlavka Foundation, grants no. GAUK 393/2005 and GACR 406/06/P377. 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