ArticlePublisher preview available

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

Authors:
To read the full-text of this research, you can request a copy directly from the authors.

Abstract and Figures

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.
This content is subject to copyright. Terms and conditions apply.
Vol.:(0123456789)
1 3
Anim Cogn (2018) 21:67–78
https://doi.org/10.1007/s10071-017-1139-x
ORIGINAL PAPER
Interspecies transmission ofemotional information
viachemosignals: fromhumans todogs (Canis lupus familiaris)
BiagioD’Aniello1 · GünRefikSemin2· AlessandraAlterisio1· MassimoAria3·
AnnaScandurra1
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
Introduction
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
biagio.daniello@unina.it
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
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
... 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. ...
Article
Full-text available
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. ...
Chapter
Full-text available
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]. ...
Article
Full-text available
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 . ...
Article
Full-text available
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). ...
Article
Full-text available
Emotions are critical for humans, not only feeling and expressing them, but also reading the emotional expressions of others. For a long time, this ability was thought to be exclusive to people; however, there is now evidence that other animals also rely on emotion perception to guide their behaviour and to adjust their actions in such way as to guarantee success in their social groups. This is the case for domestic dogs, who have tremendously complex abilities to perceive the emotional expressions not only of their conspecifics but also of human beings. In this paper we discuss dogs' capacities to read human emotions. More than perception, though, are dogs able to use this emotional information in a functional way? Does reading emotional expressions allow them to live functional social lives? Dogs can respond functionally to emotional expressions and can use the emotional information they obtain from others during problem-solving, that is, acquiring information from faces and body postures allows them to make decisions. Here, we tackle questions related to the abilities of responding to and using emotional information from human expressions in a functional way and discuss how far dogs can go when reading our emotions. Social media summary: dogs recognise and infer emotional information from humans and use this information to regulate their own behaviour.
Chapter
In this chapter, I present a concept for a dog-assisted self-confidence training that I have developed and use for working with self-doubting individuals. First, I discuss general aspects of the target group as well as the duration and framework of the training, and then introduce the concept of self-confidence in the following section. Subsequent explanations are given as to why self-confidence can be trained so well with dogs, and how exactly self-confidence is expressed when dealing with a dog. Afterwards, I will introduce the specific course of the training using examples from practice. Finally, I will highlight possible difficulties in the course of the dog-assisted self-confidence training.
Article
The olfaction is not a degraded sense, but it plays an important function not only in survival but also in human senses, emotions, memories, and social functions. It is a complex and difficult characteristic of the olfaction that has only recently been scientific development. Although interest has increased recently, the characteristics and functions of human olfactory function are not well known, and medical research are also focused on disease. In fact, interest in medical aspects such as the cause of olfactory diseases, olfactory function tests, treatments, and olfactory rehabilitation has only recently grown, and other odors, olfactory characteristics, functions, and humanities have little interest. Therefore, beyond the medical perspective on human olfaction and smell, we intend to increase our understanding and interest in the olfaction, which has been underestimated in importance, through humanistic considerations. The olfaction is also a sense of a person, and its value should be paid attention again. It’s never an inferior sense. Understanding the functions of the underrated human olfaction and re-discovering the lost olfaction and smell culture will enrich life.
Article
Humans can communicate their emotions to others via volatile emissions from their bodies. Although there is now solid evidence for human chemical communication of fear, stress and anxiety, investigations of positive emotions remain scarce. In a recent study, we found that women's heart rate and performance in creativity tasks were modulated by body odors of men sampled while they were in a positive vs. neutral mood. However, inducing positive emotions in laboratory settings remains challenging. Therefore, an important step to further investigate the human chemical communication of positive emotions is to develop new methods to induce positive moods. Here, we present a new mood induction procedure (MIP) based on virtual reality (VR), that we assumed to be more powerful than videos (used in our previous study) to induce positive emotions. We hypothesized that, consequently, given the more intense emotions created, this VR-based MIP would induce larger differences between the receivers' responses to the positive body odor versus a neutral control body odor, than the Video-based MIP. The results confirmed the higher efficacy of VR to induce positive emotions compared with videos. More specifically, VR had more repeatable effects between individuals. Although positive body odors had similar effects to those found in the previous video study, especially faster problem solving, these effects did not reach statistical significance. These outcomes are discussed as a function of the specificities of VR and of other methodological parameters, that may have prevented the observation of such subtle effects and that should be understood more in-depth for future studies on human chemical communication.
Chapter
Full-text available
Wie sprechen Menschen mit nicht-menschlichen Entitäten, wie über sie? Wie versprachlichen wir die Beziehungen und Unterschiede zwischen Menschen, Tieren und Maschinen? Wie wird die Grenze zwischen Menschlichem und Nicht-Menschlichem genutzt, um soziale Auf- und Abwertung zu kommunizieren? Der Band bringt linguistische und benachbarte Disziplinen zusammen, um sprachliche Praktiken an und jenseits der Außengrenze des Humanen auszuleuchten.
Article
Full-text available
In many studies that have investigated whether dogs' capacities to understand human pointing gestures are aspects of evolutionary or developmental social competences, family-owned dogs have been compared to shelter dogs. However, for most of these studies, the origins of shelter dogs were unknown. Some shelter dogs may have lived with families before entering shelters, and from these past experiences, they may have learned to understand human gestures. Furthermore, there is substantial variation in the methodology and analytic approaches used in such studies (e.g. different pointing protocols, different treatment of trials with no-choice response and indoor vs. outdoor experimental arenas). Such differences in methodologies and analysis techniques used make it difficult to compare results obtained from different studies and may account for the divergent results obtained. We thus attempted to control for several parameters by carrying out a test on dynamic proximal and distal pointing. We studied eleven kennel dogs of known origin that were born and raised in a kennels with limited human interaction. This group was compared to a group of eleven dogs comparable in terms of breed, sex and age that had lived with human families since they were puppies. Our results demonstrate that pet dogs outperform kennel dogs in their comprehension of proximal and distal pointing, regardless of whether trials where no-choice was made were considered as errors or were excluded from statistical analysis, meaning that dogs living in kennels do not understand pointing gestures. Even if genetic effects of the domestication process on human-dog relationships cannot be considered as negligible, our data suggest that dogs need to learn human pointing gestures and thus underscore the importance of ontogenetic processes.
Article
Full-text available
Emotional contagion, a basic component of empathy defined as emotional state-matching between individuals, has previously been shown in dogs even upon solely hearing negative emotional sounds of humans or conspecifics. The current investigation further sheds light on this phenomenon by directly contrasting emotional sounds of both species (humans and dogs) as well as opposed valences (positive and negative) to gain insights into intra- and interspecies empathy as well as differences between positively and negatively valenced sounds. Different types of sounds were played back to measure the influence of three dimensions on the dogs’ behavioural response. We found that dogs behaved differently after hearing non-emotional sounds of their environment compared to emotional sounds of humans and conspecifics (“Emotionality” dimension), but the subjects responded similarly to human and conspecific sounds (“Species” dimension). However, dogs expressed more freezing behaviour after conspecific sounds, independent of the valence. Comparing positively with negatively valenced sounds of both species (“Valence” dimension), we found that, independent of the species from which the sound originated, dogs expressed more behavioural indicators for arousal and negatively valenced states after hearing negative emotional sounds. This response pattern indicates emotional state-matching or emotional contagion for negative sounds of humans and conspecifics. It furthermore indicates that dogs recognized the different valences of the emotional sounds, which is a promising finding for future studies on empathy for positive emotional states in dogs.
Article
Full-text available
By 2.5 years of age humans are more skilful than other apes on a set of social, but not nonsocial, cognitive tasks. Individual differences in human infants, but not chimpanzees, Pan troglodytes, are also explained by correlated variance in these cooperative communicative skills. Relative to nonhuman apes, domestic dogs, Canis familiaris, perform more like human infants in cooperative communicative tasks, but it is unknown whether dog and human cognition share a similar underlying structure. We tested 552 dogs in a large-scale test battery modelled after similar work with humans and nonhuman apes. Unlike chimpanzees, but similarly to humans, individual differences in dogs were explained by correlated variance in skills for solving cooperative communicative problems. Direct comparisons of data from all three species revealed similar patterns of individual differences in cooperative communication between human infants (N = 105) and domestic dogs (N = 430), which were not observed in chimpanzees (N = 106). Future research will be needed to examine whether the observed similarities are a result of similar psychological mechanisms and evolutionary processes in the dog and human lineages.
Chapter
This book provides an up-to-date description of the behavioural biology of dogs. It is written for students of animal behaviour or veterinary medicine at advanced levels and dog owners. This book is divided into 4 parts and 14 chapters. The first part (chapters 1-3) focuses on the evolution and development of the dog. The second part (chapters 4-8) deals with the basic aspects of animal behaviour with particular emphasis on dogs. The third part (chapters 9-12) places the modern dog in its present ecological framework in the niche of human coexistence. A broad overview of the behavioural aspects of living close to humans is given. The fourth part (chapters 13 and 14) focuses on behavioural problems, their prevention and cure.
Article
Despite an increasing focus on the neural basis of human decision making in neuroscience, relatively little attention has been paid to decision making in social settings. Moreover, although human social decision making has been explored in a social psychology context, few neural explanations for the observed findings have been considered. To bridge this gap and improve models of human social decision making, we investigated whether acquiring a good reputation, which is an important incentive in human social behaviors, activates the same reward circuitry as monetary rewards. In total, 19 subjects participated in functional magnetic resonance imaging (fMRI) experiments involving monetary and social rewards. The acquisition of one's good reputation robustly activated reward-related brain areas, notably the striatum, and these overlapped with the areas activated by monetary rewards. Our findings support the idea of a "common neural currency" for rewards and represent an important first step toward a neural explanation for complex human social behaviors.
Article
We assessed how highly trained dogs respond to gestural versus verbal signals when their handlers or an unfamiliar person asked them to perform an obedience task. Dogs were requested to perform four different actions (“Sit”, “Down”, “Stay” and “Come”) upon receiving congruent (only gestural or only verbal) or incongruent signals (gestural and verbal signals contradict each other). The dogs’ performance measures were the frequency of correct responses and their response latency. Generalized Estimation Equation models were used to determine whether the type of signal, the coherence of the signals and familiarity with the signaler influenced dogs’ responses. Our results show that the probability of dogs expressing the requested behaviour was lower when the stranger gave verbal signals, than in any of the other conditions. In the incongruent condition, the probability that dogs expressed the behaviour indicated by the verbal signal was lower for signals provided by the stranger than for signals provided by the owner. The reverse was observed for gestural signals. In general, longer latencies to perform the “Come”, “Down” and “Sit” behaviours were observed in response to the stranger’s verbal signals than when the stranger gave gestural or incongruent signals. Additionally, the response latency to the stranger’s verbal stimuli took longer than verbal stimuli were provided by the owner in the case of “Come” (P = 0.002) and “Sit” (P < 0.001) actions. Our data support the argument that for highly trained dogs, gestural signals are less dependent upon signal-giver familiarity, whereas verbal signals are less effective when they are given by an unfamiliar person.
Article
Reports of variability in the social behavior of the domestic dog (Canis lupus familiaris) are common across populations, breeds, and individuals. This has often been considered a challenge for characterizing the nature and origins of the domestic dog’s social cognition. Here, we propose that this variability might be explained by social plasticity, a trait that could contribute to the success of the domestic dog and facilitate the dog-human bond. Additional research specifically aimed at investigating population and individual variation in canine social behavior, such as attachment-style research, may provide important insight into domestic dogs’ biological success, as well as knowledge that could benefit both dogs and humans in a wide range of applied settings.
Article
Humans use multiple senses to navigate the social world. Among these, our sense of smell is arguably the most underestimated one. One intriguing function of the sense of smell is its social communicative function. Research has shown that human odors can convey information about a range of states (e.g., emotions, sickness) and traits (e.g., individuality, gender). Yet, what underlies the communicability of these states and traits via smell? We aim to fill this explanatory gap by furnishing a framework that highlights the dynamic and flexible aspects of human olfactory communication. In particular, we explain how multiple-message body odors, associative learning (i.e., the systematic co-occurrence of certain odorants with state- or trait-related information), and top-down contextual influences could interact to shape human odor perception. Not only does our model help to integrate past research on human olfactory communication, but it also opens new avenues for future research on this fascinating, yet to date poorly understood field.
Article
We assessed how water rescue dogs, which were equally accustomed to respond to gestural and verbal requests, weighted gestural versus verbal information when asked by their owner to perform an action. Dogs were asked to perform four different actions (“sit”, “lie down”, “stay”, “come”) providing them with a single source of information (in Phase 1, gestural, and in Phase 2, verbal) or with incongruent information (in Phase 3, gestural and verbal commands referred to two different actions). In Phases 1 and 2, we recorded the frequency of correct responses as 0 or 1, whereas in Phase 3, we computed a ‘preference index’ (percentage of gestural commands followed over the total commands responded). Results showed that dogs followed gestures significantly better than words when these two types of information were used separately. Females were more likely to respond to gestural than verbal commands and males responded to verbal commands significantly better than females. In the incongruent condition, when gestures and words simultaneously indicated two different actions, the dogs overall preferred to execute the action required by the gesture rather than that required verbally, except when the verbal command “come” was paired with the gestural command “stay” with the owner moving away from the dog. Our data suggest that in dogs accustomed to respond to both gestural and verbal requests, gestures are more salient than words. However, dogs’ responses appeared to be dependent also on the contextual situation: dogs’ motivation to maintain proximity with an owner who was moving away could have led them to make the more ‘convenient’ choices between the two incongruent instructions.