ArticlePublisher preview available
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.
1 3
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
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
... Interspecific odour communication of emotions has received increased attention in recent years [19,[40][41][42][43][44]. D'Aniello et al. [41] reported that dogs are able to recognise human emotions from body odour, as they displayed behaviours indicating stress only when being presented with human odour of fear. ...
... Interspecific odour communication of emotions has received increased attention in recent years [19,[40][41][42][43][44]. D'Aniello et al. [41] reported that dogs are able to recognise human emotions from body odour, as they displayed behaviours indicating stress only when being presented with human odour of fear. In a recent study, Sabiniewicz et al. [44] demonstrated that horses presented differential behaviours in response to human fear and non-fear odour samples, showing the ability of purely olfactory recognition of human emotions. ...
Full-text available
Mammalian body odour conveys cues about an individual’s emotional state that can be recognised by conspecifics. Thus far, little attention has been paid to interspecific odour communication of emotions, and no studies have examined whether humans are able to recognise animal emotions from body odour. Thus, the aim of the present study was to address this question. Body odour samples were collected from 16 two-year-old thoroughbred horses in fear and non-fear situations, respectively. The horse odour samples were then assessed by 73 human odour raters. We found that humans, as a group, were able to correctly assign whether horse odour samples were collected under a fear- or a non-fear condition, respectively. Furthermore, they perceived the body odour of horses collected under the fear condition as more intense, compared with the non-fear condition. An open question remains, which is whether humans could simply distinguish between little versus much sweat and between high intensity versus low intensity or were able to recognise horses’ fear and non-fear emotions. These results appear to fit the notion that the ability to recognise emotions in other species may present an advantage to both the sender and the receiver of emotional cues, particularly in the interaction between humans and domesticated animals. To conclude, the present results indicate that olfaction might contribute to the human recognition of horse emotions. However, these results should be addressed with caution in light of the study’s limitations and only viewed as exploratory for future studies.
... For example, in juvenile common ravens (i.e., Corvus corax), emotional contagion in the context of play could occur through a general mood state transfer resulting in increased locomotion and social play rather than through the reproduction of the same motor patterns (50). Human body odors produced in states of happiness and fear also stimulate animals emotionally and induce sympathetic and parasympathetic changes, suggesting an interspecies transfer of emotions through this means (i.e., autonomic mimicry) (51)(52)(53). Emotional contagion through vocalizations is also studied in different animal species (54,55) and shows compelling results (56,57). In particular, it is established that animals, like humans, have the ability to discriminate vocal expression of emotions (58). ...
Full-text available
The Integrative Model of Human-Animal Interactions (IMHAI) described herewith provides a conceptual framework for the study of interspecies interactions and aims to model the primary emotional processes involved in human-animal interactions. This model was developed from theoretical inputs from three fundamental disciplines for understanding interspecies interactions: neuroscience, psychology and ethology, with the objective of providing a transdisciplinary approach on which field professionals and researchers can build and collaborate. Seminal works in affective neuroscience offer a common basis between humans and animals and, as such, can be applied to the study of interspecies interactions from a One Health-One Welfare perspective. On the one hand, Jaak Panksepp's research revealed that primary/basic emotions originate in the deep subcortical regions of the brain and are shared by all mammals, including humans. On the other hand, several works in the field of neuroscience show that the basic physiological state is largely determined by the perception of safety. Thus, emotional expression reflects the state of an individual's permanent adaptation to ever-changing environmental demands. Based on this evidence and over 5 years of action research using grounded theory, alternating between research and practice, the IMHAI proposes a systemic approach to the study of primary-process emotional affects during interspecies social interactions, through the processes of emotional transfer, embodied communication and interactive emotional regulation. IMHAI aims to generate new hypotheses and predictions on affective behavior and interspecies communication. Application of such a model should promote risk prevention and the establishment of positive links between humans and animals thereby contributing to their respective wellbeing.
... When assessing canine stress during human-animal interactions, it is important to note that domestic dogs can detect human emotion through visual, auditory, and chemical channels (21)(22)(23). Dogs have been reported to use social referencing with their human companions, with the emotional reaction of the human influencing that of the dog (24); and emotional contagion between humans and dogs has been reported, especially in female dogs and with duration of the relationship playing a role (25). Research suggests that factors such as owner personality, human-animal interactions, and choice of training methods, particularly over extended time periods, can all impact companion animal behavior and welfare (26)(27)(28)(29)(30)(31)(32)(33)(34). ...
Full-text available
Negative stress due to human handling has been reported for a number of domestic animals, including dogs. Many companion dogs display significant stress during routine care in the veterinary clinic, risking injury to staff and potentially compromising the quality of care that these dogs receive. On the other hand, positive interactions with humans can have a beneficial effect on dogs, particularly in stressful situations such as animal shelters. Research has shown that dogs can detect human emotions through visual, auditory, and chemical channels, and that dogs will exhibit emotional contagion, particularly with familiar humans. This study investigated relationships between emotional states of dogs and unfamiliar human handlers, using simultaneous measures of cardiac activity and behavior, during two sessions of three consecutive routine handling sets. Measures of cardiac activity included mean heart rate (HR mean ), and two measures of heart rate variability (HRV): the root mean square of successive differences between normal heartbeats (RMSSD); and the high frequency absolute power component of HRV, log transformed (HF log ). We also assessed human handlers' emotional state during handling sessions following an intervention designed to reduce stress, compared with sessions conducted on a different day and following a control activity. Polar H10 cardiac sensors were used to simultaneously record cardiac activity for both canine and human participants, and behavioral data were collected via digital video. The strongest influence on the dogs' stress levels in our study was found to be increasing familiarity with the setting and the handler; HR mean and SI decreased, and HRV (as RMSSD) increased, significantly from the first to the third handling set. Canine HRV (as HF log ) was also highest in set 3, although the difference was not statistically significant. There were no strong patterns found in the human cardiac data across handling set, session, or by pre-handling activity. We did not find consistent support for emotional contagion between the dogs and their handlers in this study, perhaps due to the brief time that the dogs spent with the handlers. Recommendations for application to dog handling, and limitations of our methods, are described.
... Whereas several recent studies demonstrated that some animal species are able to recognize human emotions based on information from body odor [1][2][3][4], our study [5] was the first to demonstrate that the ability to recognize emotions from body odor cues of other species might be reciprocal between animals and humans. In their critical comment [6], Semin and colleagues suggest that the study's methodology should be changed. ...
... The argument rests on their report suggesting that humans could differentiate the chemosignals of horses experiencing fear from the chemosignals collected while they were not experiencing this emotion (control). We know of studies that have documented the communication of fear and happiness experiences via the body odors of human beings to pet dogs (Canis lupus familiaris) (e.g., D'Aniello et al., 2018; 2021) [3,4] and horses (Equus ferus caballus) (Semin et al., 2019;Sabiniewicz et al., 2020) [5,6]. Still, Sabiniewicz and her colleague's Field (2021) study is the first to show the reverse, namely, from horses to humans. ...
Full-text available
We illustrate the problematic nature of different assumptions guiding the examination of whether humans can detect the source of fear chemosignals (i.e., body odors) emitted by horses—a research question examined in an article recently published in Animals. A central issue is that the formulation of the question itself contains the answer to it. In this paper, we parse the problematic assumptions on which the analysis and methodology rely, leading to conclusions that are difficult to support. These assumptions constitute examples of methodological problems that should be avoided in research with animals and odors. The unique aspect of this paper is that it is a collaborative product, including the original contributor, in the pursuit of transparency in science.
... Mice can easily solve complex "olfactory cocktail party" problems, where a target odorant is mixed with complex and variable odor mixtures (41). Dogs are capable of discriminating between "happy," "fearful," and "neutral" emotions in humans, based on the odorants present in a test subject's sweat (42). More recently, a cohort of dogs has been trained to diagnose COVID-19 from the smell of a patient's secretions (43). ...
Full-text available
In the mammalian brain, sensory circuits are usually organized in a topographical way, meaning that, for a given brain region, neighboring neurons respond to stimuli close to each other in their sensory space. Olfaction is a notable exception to this rule; projections to the olfactory system are sparse and dispersed, leading to no apparent topography. Here, we assessed the presence of a topographical map in the mouse olfactory cortex, using a previously generated online dataset of neuronal recordings. The dataset consisted of about 1,800 olfactory cortical neurons collected from 10 mice, stimulated with a panel of 15 odorants. If there is no odor topography in the olfactory cortex, there should be no correlation between the chemical composition of odorants and their evoked neuronal response. To test this hypothesis, we first calculated odor similarity between each pair of odorants, using their chemical traits. Then, for each odor pair, we computed the similarity between their evoked neuronal responses. Finally, we assessed the relationship between odor similarity and neuronal response similarity. We found little to no correlation between the two variables (R2 averaged across all mice tested: 0.015), which suggests the lack of topography in the murine olfactory cortex and opens new questions into what other variables might play a role in odorant distinction.
Our relationship with dogs runs thousands of years deep. Today, we might know dogs intimately as members of our human family, but we can also know and consider dogs on their own terms, as members of Canis familiaris , with a unique evolutionary history and species‐specific characteristics and needs. This chapter is a resource for all types of dog knowers and caretakers. It relies heavily on empirical research to anchor readers in the foundations of canine behavior—such as dog behavioral development, normal dog behavior, factors influencing behavior, and relationships with people—and considers how these topics affect dogs of all ages and backgrounds who find themselves in the shelter environment.
Results achieved by man trailers/trackers is often accepted as evidence in courts. To be used as such, the results should be founded on scientific proof. With respect to the uniqueness of human individual scent, there is sufficient scientific foundation, but with respect to animal learning and cognition we now know that great care must be taken to ensure animals are responding to the intended cue. A review of man trailing studies indicate that these do not prove the essential question: are the dogs responding to the individual human odor cue when matching a scent article to a track? A suggestion ismade for testing individual dogs based on guidelines set by the Scientific Working Group on the use of Dogs and Orthogonal Detector Guidelines. Finally, points that should be addressed when assessing such evidence in courts are provided.
Full-text available
Behavioural reactions towards a dead conspecific have been observed rarely in wild canids and there is no documented scientific evidence of grief in pet dogs. A quantitative analysis of grief-related responses in both dogs and owners was conducted, using the validated online Mourning Dog Questionnaire. The survey was completed by 426 Italian adults who had owned at least two dogs, one of whom died while the other was still alive. This research aims to explore whether, how and what a dog may experience over the loss of a companion dog. Multiple logistic regression indicates that both a friendly or parental relationship between two dogs but also the fact that dogs used to share food and the owner’s grief and anger are principal predictors of negative behavioural changes. According to dog owners’ answers, the surviving dog after the death of the companion dog changed both in terms of activities (“playing”, “sleeping”, and “eating”) and emotions (fearfulness), which occurred as a function of the quality of the relationship between the two animals. By contrast, the time the two dogs had spent together had no effect on the behaviours of surviving dog. Owner perceptions about their dog’s reactions and emotions were not related to the memory or suffering of the event that tended to diminish over time. These findings indicate that a dog may show grief-related behavioural and emotional patterns when a close conspecific dies, with aspects of the latter possibly related to the owner’s emotional status.
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.
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.
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.
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.
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.
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.
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.
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.
Previous studies have reported striking asymmetries in the nostril use of dogs during sniffing at different emotive stimuli. Here we report, for the first time, that this asymmetry is also manifested during sniffing of both human and canine odours collected during different emotional events. Results showed that during sniffing of conspecific odour collected during a stressful situation (e.g. an “isolation” situation in which a dog was isolated from its owner in an unfamiliar environment) dogs consistently used their right nostril (right hemisphere). On the other hand, dogs consistently used the left nostril to sniff human odours collected during fearful situations (emotion-eliciting movies) and physical stress, suggesting the prevalent activation of the left hemisphere. The opposite bias shown in nostril use during sniffing at canine versus human odours suggests that chemosignals communicate conspecific and heterospecific emotional cues using different sensory pathways.