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Interspecies transmission of emotional information via chemosignals: from humans to dogs (Canis lupus familiaris)

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We report a study examining interspecies emotion transfer via body odors (chemosignals). Do human body odors (chemosignals) produced under emotional conditions of happiness and fear provide information that is detectable by pet dogs (Labrador and Golden retrievers)? The odor samples were collected from the axilla of male donors not involved in the main experiment. The experimental setup involved the co-presence of the dog’s owner, a stranger and the odor dispenser in a space where the dogs could move freely. There were three odor conditions [fear, happiness, and control (no sweat)] to which the dogs were assigned randomly. The dependent variables were the relevant behaviors of the dogs (e.g., approaching, interacting and gazing) directed to the three targets (owner, stranger, sweat dispenser) aside from the dogs’ stress and heart rate indicators. The results indicated with high accuracy that the dogs manifested the predicted behaviors in the three conditions. There were fewer and shorter owner directed behaviors and more stranger directed behaviors when they were in the “happy odor condition” compared to the fear odor and control conditions. In the fear odor condition, they displayed more stressful behaviors. The heart rate data in the control and happy conditions were significantly lower than in the fear condition. Our findings suggest that interspecies emotional communication is facilitated by chemosignals.
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Anim Cogn (2018) 21:67–78
Interspecies transmission ofemotional information
viachemosignals: fromhumans todogs (Canis lupus familiaris)
BiagioD’Aniello1 · GünRefikSemin2· AlessandraAlterisio1· MassimoAria3·
Received: 10 July 2017 / Revised: 19 September 2017 / Accepted: 4 October 2017 / Published online: 7 October 2017
© Springer-Verlag GmbH Germany 2017
Keywords Dogs· Human emotional smell· Interspecies
emotional transfer· Emotional communication· Dog’s
heart rate· Dog–human bond
Body odors constitute chemical signals that have evolved
for species-specific communication (e.g., McClintock 2000;
Stevenson 2009; Wyatt 2015). Research has shown that in
humans, chemosignals can carry compound information
ranging from genetic relatedness (Jacob etal. 2002), gender
(Penn etal. 2007), to emotional states (e.g., de Groot etal.
2012; Mujica-Parodi etal. 2009; Prehn etal. 2006; Zhou and
Chen 2009; Mutic etal. 2015) and more (see de Groot etal.
2017). The transmission of olfactory information related to
emotional states occurs without the requirement of com-
municative intent (Semin and de Groot 2013) and is below
the threshold of consciousness (Pause 2012). Nevertheless,
such transmission induces in the receiver a partial affective,
behavioral, perceptual, and neural reproduction of the state
of the sender (Semin 2007). The question we addressed here
was about interspecies transmission of emotional informa-
tion. To this end, we employed an experimental paradigm
used in our previous research (e.g., de Groot etal. 2012),
whereby the signal was human body odor that was pro-
duced while the donors were experiencing experimentally
induced emotional states (i.e., happy, fear). The receivers of
the human chemosignals were pet dogs (Labrador retrievers
and Golden retrievers). Thus, the communication paradigm
we employed exposed pet dogs to chemosignals produced by
humans and analyzed the dogs’ reactions. In the following,
we provide an overview of the relevant research to date with
dogs and then outline the current study.
Abstract We report a study examining interspecies emo-
tion transfer via body odors (chemosignals). Do human
body odors (chemosignals) produced under emotional con-
ditions of happiness and fear provide information that is
detectable by pet dogs (Labrador and Golden retrievers)?
The odor samples were collected from the axilla of male
donors not involved in the main experiment. The experi-
mental setup involved the co-presence of the dog’s owner,
a stranger and the odor dispenser in a space where the dogs
could move freely. There were three odor conditions [fear,
happiness, and control (no sweat)] to which the dogs were
assigned randomly. The dependent variables were the rel-
evant behaviors of the dogs (e.g., approaching, interacting
and gazing) directed to the three targets (owner, stranger,
sweat dispenser) aside from the dogs’ stress and heart rate
indicators. The results indicated with high accuracy that the
dogs manifested the predicted behaviors in the three condi-
tions. There were fewer and shorter owner directed behav-
iors and more stranger directed behaviors when they were
in the “happy odor condition” compared to the fear odor and
control conditions. In the fear odor condition, they displayed
more stressful behaviors. The heart rate data in the control
and happy conditions were significantly lower than in the
fear condition. Our findings suggest that interspecies emo-
tional communication is facilitated by chemosignals.
* Biagio D’Aniello
1 Department ofBiology, University ofNaples “Federico II”,
Via Cinthia, Naples80126, Italy
2 William James Center forResearch, ISPA - Instituto
Universitário, Lisbon, Portugal
3 Department ofEconomics andStatistics, University
ofNaples “Federico II”, Naples, Italy
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... The recent interest in intraspecies communication has inspired pioneering work on interspecies communication. It has been shown that human emotional chemosignals shape the behaviors of other species, particularly dogs (D'Aniello et al. 2018(D'Aniello et al. , 2021Semin et al. 2019;Siniscalchi et al. 2016), mice, cows (Destrez et al. 2021), and horses (Lanatà et al. 2018;Sabiniewicz et al. 2020). ...
... Another plausible scenario is that puppies do not reveal any of the systematic responses that the two types of chemosignals activate, suggesting that the regular and robust patterns observed with adult dogs (D'Aniello et al. 2018) are the result of an extended socialization process. The opportunity to learn from humans during ontogenesis and thus shape (D'Aniello et al. 2015;Scandurra et al. 2015) and improve social-communicative skills, including chemosignal sensitivity, could be the result of the proximity between puppies and their owners (D'Aniello et al. , 2017. ...
... Odor collection was performed as reported in our earlier papers (D'Aniello et al. 2018(D'Aniello et al. , 2021. Heterosexual male donors were students at ISPA University, Lisbon (average age 21 years) (de Groot et al. 2012(de Groot et al. , 2015 who watched 25-min fear or happiness-inducing videos in two sessions separated by a week. ...
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We report an observational, double-blind, experimental study that examines the effects of human emotional odors on puppies between 3 and 6 months and adult dogs (one year and upwards). Both groups were exposed to control, human fear, and happiness odors in a between subjects' design. The duration of all behaviors directed to the apparatus, the door, the owner, a stranger, and stress behaviors was recorded. A discriminant analysis showed that the fear odor activates consistent behavior patterns for both puppies and adult dogs. However, no behavioral differences between the control and happiness odor conditions were found in the case of puppies. In contrast, adult dogs reveal distinctive patterns for all three odor conditions. We argue that responses to human fear chemosignals systematically influence the behaviors displayed by puppies and adult dogs, which could be genetically prefigured. In contrast, the effects of happiness odors constitute cues that require learning during early socialization processes, which yield consistent patterns only in adulthood.
... Importantly, beyond artificial scents, the question of how human body chemosignals ("human body odors; HBOs") may modulate emotional processing is reaching great attention. Typically, HBOs are collected by axillary sweat of individuals who are exposed to an emotional elicitation procedure via, for example, videos eliciting happiness or fear [19]. The donors are usually asked to rate how their feelings according to concrete emotions (e.g., angry, fearful, sad, happy, disgusted, neutral, surprised, calm, and amused) and/or affective dimensions (valence and arousal) on a numerical Likert scale. ...
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Human sensory systems are capable of encoding emotion-related signals during social interactions (e.g., fearful or happy facial expressions). In this regard, many emotion elicitation procedures have been reported within the scope of social signal processing research. Most of these procedures rely on socially relevant stimuli, such as emotional face images, videos, and, more recently, virtual reality (VR) scenes. Unfortunately, procedures involving cross-modal interactions beyond visual and acoustic stimuli, such as olfaction, are still scarce. In this sense, neuroscience supports a close link between the olfactory and affective systems. Moreover, experimental research has reported faster appraisals of emotional face images when congruent valence-laden artificial scents were presented (e.g., positive scent-happy face; negative scent-fearful face). Interestingly, recent findings indicate that emotion-related human-body odors (HBOs) might also modulate affective appraisals during a neutral virtual reality experience. However, whether and how emotion-related HBOs modulate affective VR experiences requires further examination. Here, an approach to this research question is proposed from a Virtual Reality-based Behavioral Biomarker (VRBB) experimental framework. Concretely, in the first place, a novel affective elicitation procedure based on social-emotional VR is introduced, wherein electro-dermal activity (EDA), heart-rate variability (HRV), electroencephalography (EEG), and affective appraisals, will be accounted for. In a second step, the modulating role of HBOs will be investigated regarding those measures. This work presents the envisioned model, details of the devised VEs, and a research design to test concrete hypotheses.KeywordsHuman Body Odors (HBO)EmotionVirtual Environmentsocial signal processing
... When the situation was positive and there was indirect access to food, dogs spent more time sniffing the demonstrators, so sniffing might be an exploratory behaviour associated with acquisition of emotional information. In fact, studies show that the olfactory system plays an important role in detecting emotional cues of happiness and fear via human chemosignals [24]. ...
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Dogs are good models for studying behaviour and cognition as they have complex social capabilities. In the current study, we observed how human emotional valences (positive, neutral and negative) affected aspects of dogs’ behaviour. We expected that dogs would exhibit more approaching behaviours in the positive condition and more signs of avoidance in the negative one. We analysed videos of 70 adult pet dogs of various breeds taken from an experiment in which one of two actors expressed an emotion and dogs could freely explore the environment for 30 s. Our results show that dogs exhibit differential behaviour when presented with different emotional valences. Two behaviours arose that might be linked to a reciprocal positive emotional state in dogs: tail raised between 90° and 180° and physical contact during sniffing. These behaviours are associated with an active search for information. In the positive conditions, dogs were more willing to explore the social environment and gather information from the actors.
... These receptors could be present in horses, either as a result of domestication or by inheritance from a common mammalian ancestor. As several other species of domestic mammals seem to perceive these compounds (namely, dogs, cattle and mice 29,31,32 ), the first hypothesis would entail multiple appearances of such receptors during the domestication of each of these species. However, olfaction is the most ancient and universal sense, and the cerebral structures that process odors evolved very early in mammals 1 . ...
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Animals are widely believed to sense human emotions through smell. Chemoreception is the most primitive and ubiquitous sense, and brain regions responsible for processing smells are among the oldest structures in mammalian evolution. Thus, chemosignals might be involved in interspecies communication. The communication of emotions is essential for social interactions, but very few studies have clearly shown that animals can sense human emotions through smell. We used a habituation-discrimination protocol to test whether horses can discriminate between human odors produced while feeling fear vs. joy. Horses were presented with sweat odors of humans who reported feeling fear or joy while watching a horror movie or a comedy, respectively. A first odor was presented twice in successive trials (habituation), and then, the same odor and a novel odor were presented simultaneously (discrimination). The two odors were from the same human in the fear or joy condition; the experimenter and the observer were blinded to the condition. Horses sniffed the novel odor longer than the repeated odor, indicating they discriminated between human odors produced in fear and joy contexts. Moreover, differences in habituation speed and asymmetric nostril use according to odor suggest differences in the emotional processing of the two odors.
... Dogs have been empirically shown to be particularly sensitive to human emotions (Kujala, 2018;Albuquerque, 2017). They discriminate and show differential responses to emotional cues expressed through body postures, facial expressions, vocalisations and odours (Vás et al., 2005;Müller et al., 2015;Albuquerque et al., 2016;Caeiro et al., 2017;D'Aniello et al., 2017), and emotional cues can influence their behaviour (e.g. Merola et al., 2012a;Albuquerque et al., 2021;Bremhorst et al., 2021). ...
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