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Why Do Monkeys Smell Their Fingers

8. When humans sniff their hands, they are also smelling who their hands touched

After observing the extent of human hand-sniffing, it occurred to us that this behaviour may provide information not only regarding one’s own body, but also regarding the bodies of others. Indeed, in the previously described extensive hand-sniffing in primates (figure 10c), the animals typically mix between merely sniffing their own hands spontaneously, or sticking their fingers within bodily orifices (often the nostrils) of conspecifics and then carefully sniffing their own hand [19]. Humans obviously touch each other within the context of close relationships, but they also touch complete strangers: handshaking is a common introductory greeting ritual in the West and beyond [20,21]. We therefore set out to test in our previous study [12] the hypothesis that handshaking subserves social chemosignalling. We first used gas-chromatography mass-spectrometry (GCMS) to test whether the brief contact of a handshake is sufficient to transfer volatile organic compounds from one hand to another and found evidence for extensive transfer of several molecules from skin (figure 8).

We then covertly recorded and quantified hand-to-nose contact before and after handshaking with an experimenter within a fixed paradigm. What we view as the most significant result of this effort was the astonishingly high baseline rate of hand-sniffing, as reported above (figure 1). However, we also observed that this behaviour was significantly impacted by handshaking. Participants significantly increased sniffing of the shaking hand (right) after within-sex handshakes, yet increased sniffing of the non-shaking hand (left) after cross-sex handshakes. In other words, handshaking impacts ensuing hand-sniffing. Moreover, to again verify the olfactory origins of this behaviour, in a separate control experiment with 63 participants, we artificially tainted the body-odour of the experimenter. Here the experimenter wore a device on his/her wrist that covertly emitted one of three odourants during handshake. We found that we could selectively increase or decrease hand-sniffing in participants as a function of the odourant we used to taint the experimenter, and all this despite using subliminal levels of odour (figure 9a). This further verifies the olfactory origins of this behaviour and, in our view, serves not only to mitigate, but potentially to reverse our initial concern regarding this merely being a reflection of displacement behaviour. In using the term ‘reverse’, we mean that not only do we think that the behaviour we observed is chemosignalling and not displacement behaviour, but moreover, we suspect that many of the previous reports of displacement behaviour may in fact reflect chemosignalling. As to the counterintuitive within-sex versus cross-sex dissociation, it was very powerful (ANOVA, three-way interaction: F1,77 = 37.79, p < 0.0001), yet we have no strong theoretical hypothesis for it. We speculate that whereas sniffing the shaking hand provides information about the conspecific in question, sniffing the non-shaking hand provides comparative information on self (more about this in §9). We do not know, however, why one would want to increase this type of information on same-sex conspecifics rather than on cross-sex conspecifics and can only speculate that the sex interaction may reflect context specificity: although participants increased sniffing the within-sex shaking hand in the context of our experiment, they may opt to increase sniffing cross-sex hands in other behavioural settings. This remains a question for investigation.

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Amusingly, the handshake effect has been ‘replicated’ in live recreations on several popularized science television shows around the world (electronic supplementary material, figure S1 and video S2), and we have now replicated the handshake effect in one additional published study. Given our overarching working hypothesis that social chemosignalling is a big part of human social interaction, we therefore hypothesized that social chemosignalling will be altered in disorders of social behaviour. A particularly relevant condition is autism spectrum disorder (ASD). With this in mind, we replicated the handshake paradigm in 18 cognitively able adult men with ASD [22]. The effect replicated in the ASD cohort as a group, and moreover, four members of the ASD cohort stood out with hand-sniffing behaviour that was inordinately persistent and explicit (figure 9b). After handshake, three of the four practically did not remove their hand from their nose for the duration of the recorded session. Their behaviour reflected explicit careful olfactory investigation. In turn, the fourth participant carefully sniffed his hand for much of the baseline, but then never brought it back to his nose after handshake. In other words, consistent with other measures [23], the variability in the ASD cohort was higher than in controls. In conclusion, this result in ASD replicates the effect of increased face-touching after handshake, but the limited size of the cohort prevents us from determining whether this increase is greater in ASD than in controls, despite a trend to that effect. This dovetails with reports on excessive olfactory social investigation in ASD. In fact, the observation that initially drove us to investigate social olfaction in ASD in the first place was from a newspaper weekend magazine story in the leading Israeli newspaper Haaretz. This was the story of Ayala, a 51-year-old woman, who was one of the first in Israel to be diagnosed with autism (the English translation of the story is currently viewable at: http://www.haaretz.com/weekend/magazine/eternal-child-1.342756). Ayala is non-verbal, and her primary avenue of social investigation always was, and still is, her sense of smell. Ayala uses her nose to investigate all individuals. The following is a quote from the story:

When Ayala was four, her mother took her to preschool and stayed with her there. ‘I thought that if she heard children talking she’d pick something up’, she explains. ‘The children really loved her, but she didn’t cooperate with them. The most important thing to her, even then, was smell. She would smell the children. If she liked the smell, you were her friend. If not, you couldn’t come near her’.

This overt pattern of olfactory social investigation, or social sniffing, is repeated often in more detailed case-report depictions of behaviour in ASD (e.g. Stephen Wiltshire in [24]).

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