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

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Abstract

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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References

  • Ainsworth MDS, Bell SM (1970) Attachment, exploration, and separation: illustrated by the behavior of one-year-olds in a strange situation. Child Dev 41:49–67

    Article  CAS  PubMed  Google Scholar 

  • Albuquerque N, Guo K, Wilkinson A, Savalli C, Otta E, Mills D (2016) Dogs recognize dog and human emotions. Biol Lett 12:20150883

    Article  PubMed  PubMed Central  Google Scholar 

  • Ashida S (1972) Development changes in the basal and evoked heart rate in neonatal rats. J Comp Physiol Psych 78:368

    Article  CAS  Google Scholar 

  • Baldock NM, Sibly RM, Penning PD (1988) Behavior and seasonal variation in heart rate in domestic sheep, Ovis aries. Anim Behav 36:35–43

    Article  Google Scholar 

  • Bekoff M (2007) The emotional lives of animals: a leading scientist explores animal joy, sorrow, and empathy-and why they matter. New World Library, Novato

    Google Scholar 

  • Berns GS, Brooks AM, Spivak M (2012) Functional MRI in awake unrestrained dogs. PLoS ONE 7:e38027

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Berns GS, Brooks AM, Spivak M (2013) Replicability and heterogeneity of awake unrestrained canine fMRI responses. PLoS ONE 8:e81698

    Article  PubMed  PubMed Central  Google Scholar 

  • Berns GS, Brooks AM, Spivak M (2015) Scent of the familiar: an fMRI study of canine brain responses to familiar and unfamiliar human and dog odors. Behav Process 110:37–46

    Article  Google Scholar 

  • Candland DK, Taylor DB, Dresdale L, Leiphart JM, Solow SP (1969) Heart rate, aggression, and dominance in the domestic chicken. J Comp Physiol Psychol 67:70

    Article  CAS  PubMed  Google Scholar 

  • Custance D, Mayer J (2012) Empathic-like responding by domestic dogs (Canis familiaris) to distress in humans: an exploratory study. Anim Cogn 15:851–859

    Article  PubMed  Google Scholar 

  • D’Aniello B, Scandurra A (2016) Ontogenetic effects on gazing behavior: a case study of kennel dogs (Labrador retrievers) in the impossible task paradigm. Anim Cogn 19:565–570

    Article  PubMed  Google Scholar 

  • D’Aniello B, Scandurra A, Prato-Previde E, Valsecchi P (2015) Gazing toward humans: a study on water rescue dogs using the impossible task paradigm. Behav Process 110:68–73

    Article  Google Scholar 

  • D’Aniello B, Scandurra A, Alterisio A, Valsecchi P, Prato-Previde E (2016a) The importance of gestural communication: a study of human–dog communication using incongruent information. Anim Cogn 19:1231–1235

    Article  PubMed  Google Scholar 

  • D’Aniello B, Polese G, Luongo L, Scandurra A, Magliozzi L, Aria M, Pinelli C (2016b) Neuroanatomical relationships between FMRF-amide-immunoreactive components of the nervus terminalis and the topology of olfactory bulbs in teleost fish. Cell Tissue Res 364:43–57

    Article  PubMed  Google Scholar 

  • D’Aniello B, Alterisio A, Scandurra A, Petremolo E, Iommelli MR, Aria M (2017) What’s the point? Golden and Labrador retrievers living in kennels do not understand human pointing gestures. Anim Cogn 20:777–787

    Article  PubMed  Google Scholar 

  • Dantzer R, Baldwin BA (1974) Changes in heart rate during suppression of operant responding in pigs. Physiol Behav 12:385–391

    Article  CAS  PubMed  Google Scholar 

  • de Groot JH, Smeets MA, Kaldewaij A, Duijndam MJ, Semin GR (2012) Chemosignals communicate human emotions. Psychol Sci 23:1417–1424

    Article  PubMed  Google Scholar 

  • de Groot JH, Smeets MA, Rowson MJ, Bulsing PJ, Blonk CG, Wilkinson JE, Semin GR (2015) A sniff of happiness. Psychol Sci 26:684–700

    Article  PubMed  Google Scholar 

  • de Groot JH, Semin GR, Smeets MA (2017) On the communicative function of body odors: a theoretical integration and review. Perspect Psychol Sci 12:306–324

    Article  PubMed  Google Scholar 

  • Deputte BL, Doll A (2011) Do dogs understand human facial expressions? J Vet Behav 6:78–79

    Article  Google Scholar 

  • Eisermann K (1992) Long-term heart rate responses to social stress in wild European rabbits: predominant effect of rank position. Physiol Behav 52:33–36

    Article  CAS  PubMed  Google Scholar 

  • Essner A, Sjöström R, Ahlgren E, Lindmark B (2013) Validity and reliability of Polar® RS800CX heart rate monitor, measuring heart rate in dogs during standing position and at trot on a treadmill. Physiol Behav 114:1–5

    Article  PubMed  Google Scholar 

  • Fox MW, Andrews RV (1973) Physiological and biochemical correlates of individual differences in behavior of wolf cubs. Behavior 46:129–139

    Article  CAS  Google Scholar 

  • Fukuzawa M, Mills DS, Cooper JJ (2005) More than just a word: non-semantic command variables affect obedience in the domestic dog (Canis familiaris). Appl Anim Behav Sci 91:129–141

    Article  Google Scholar 

  • Gácsi M, Gyoöri B, Virányi Z, Kubinyi E, Range F, Belényi B, Miklósi Á (2009) Explaining dog wolf differences in utilizing human pointing gestures: selection for synergistic shifts in the development of some social skills. PLoS ONE 4:e6584

    Article  PubMed  PubMed Central  Google Scholar 

  • Hamilton J, Vonk J (2015) Do dogs (Canis lupus familiaris) prefer family? Behav Process 119:123–134

    Article  Google Scholar 

  • Hare B, Tomasello M (2005) Human-like social skills in dogs? Trends Cogn Sci 9:439–444

    Article  PubMed  Google Scholar 

  • Hare B, Brown M, Williamson C, Tomasello M (2002) The domestication of social cognition in dogs. Science 298:1634–1636

    Article  CAS  PubMed  Google Scholar 

  • Hepper PG (1988) The discrimination of human odor by the dog. Perception 17:549–554

    Article  CAS  PubMed  Google Scholar 

  • Huber A, Barber AL, Faragó T, Müller CA, Huber L (2017) Investigating emotional contagion in dogs (Canis familiaris) to emotional sounds of humans and conspecifics. Anim Cogn 20:703–715

    Article  PubMed  PubMed Central  Google Scholar 

  • Izuma K, Saito DN, Sadato N (2008) Processing of social and monetary rewards in the human striatum. Neuron 58:284–294

    Article  CAS  PubMed  Google Scholar 

  • Jacob S, McClintock MK, Zelano B, Ober C (2002) Paternally inherited HLA alleles are associated with women’s choice of male odor. Nat Genet 30:175–179

    Article  CAS  PubMed  Google Scholar 

  • Jonckheer-Sheehy VS, Vinke CM, Ortolani A (2012) Validation of a Polar® human heart rate monitor for measuring heart rate and heart rate variability in adult dogs under stationary conditions. J Vet Behav 7:205–212

    Article  Google Scholar 

  • Knutson B, Adams CM, Fong GW, Hommer D (2001) Anticipation of increasing monetary reward selectively recruits nucleus accumbens. J Neurosci 21:RC159

    CAS  PubMed  Google Scholar 

  • MacLean EL, Herrmann E, Suchindran S, Hare B (2017) Individual differences in cooperative communicative skills are more similar between dogs and humans than chimpanzees. Anim Behav 126:41–51

    Article  Google Scholar 

  • Marshall DA, Moulton DG (1981) Olfactory sensitivity to α-ionone in humans and dogs. Chem Senses 6:53–61

    Article  Google Scholar 

  • McClintock MK (2000) Human pheromones: primers, releasers, signalers, or modulators? In: Wallen K, Schneider JE (eds) Reproduction in context. MIT Press, Cambridge, pp 355–420

    Google Scholar 

  • Merola I, Prato-Previde E, Marshall-Pescini S (2012) Social referencing in dog–owner dyads? Anim Cogn 15:175–185

    Article  CAS  PubMed  Google Scholar 

  • Merola I, Marshall-Pescini S, D’Aniello B, Prato-Previde E (2013) Social referencing: water rescue trained dogs are less affected than pet dogs by the stranger’s message. Appl Anim Behav Sci 147:132–138

    Article  Google Scholar 

  • Miklósi Á (2007) Human–animal interactions and social cognition in dogs. In: Jensen P (ed) The behavioral biology of dogs. CAB International, Wallingford, pp 205–222

    Google Scholar 

  • Miklósi Á, Topál J (2013) What does it take to become ‘best friends’? Evolutionary changes in canine social competence. Trends Cogn Sci 17:287–294

    Article  PubMed  Google Scholar 

  • Mitro S, Gordon AR, Olsson MJ, Lundström JN (2012) The smell of age: perception and discrimination of body odors of different ages. PLoS ONE 7:e38110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Montague PR, Berns GS (2002) Neural economics and the biological substrates of valuation. Neuron 36:265–284

    Article  CAS  PubMed  Google Scholar 

  • Morisaki A, Takaoka A, Fujita K (2009) Are dogs sensitive to the emotional state of humans? J Vet Behav 4:49

    Article  Google Scholar 

  • Mujica-Parodi LR, Strey HH, Frederick B, Savoy R, Cox D, Botanov Y, Tolkunov D, Rubin D, Weber J (2009) Chemosensory cues to conspecific emotional stress activate amygdala in humans. PLoS ONE 4:e6415

    Article  PubMed  PubMed Central  Google Scholar 

  • Mutic S, Parma V, Brünner YF, Freiherr J (2015) You smell dangerous: communicating fight responses through human chemosignals of aggression. Chem Senses 41:35–43

    Article  PubMed  Google Scholar 

  • Nagasawa M, Murai K, Mogi K, Kikusui T (2011) Dogs can discriminate human smiling faces from blank expressions. Anim Cogn 14:525–533

    Article  PubMed  Google Scholar 

  • Nelson NL, Russell JA (2013) Universality revisited. Emot Rev 5:8–15

    Article  Google Scholar 

  • Palestrini C, Prato-Previde E, Spiezio C, Verga M (2005) Heart rate and behavioral responses of dogs in the Ainsworth’s strange situation: a pilot study. Appl Anim Behav Sci 94:75–88

    Article  Google Scholar 

  • Palmer R, Custance D (2008) A counterbalanced version of Ainsworth’s strange situation procedure reveals secure-base effects in dog–human relationships. Appl Anim Behav Sci 109:306–319

    Article  Google Scholar 

  • Panksepp J (2004) Affective neuroscience: the foundations of human and animal emotions. Oxford University Press, New York

    Google Scholar 

  • Pause BM (2012) Processing of body odor signals by the human brain. Chemosens Percept 5:55–63

    Article  PubMed  Google Scholar 

  • Penn DJ, Oberzauche E, Grammer K, Fischer G, Soini HA, Wiesler D, Novotny MV, Novotny MV, Dixon SJ, Xu Y, Brereton RG (2007) Individual and gender fingerprints in human body odor. J R Soc Interface 4:331–340

    Article  PubMed  Google Scholar 

  • Pinelli C, Rastogi RK, Scandurra A, Jadhao AG, Aria M, D’Aniello B (2014) A comparative cluster analysis of nicotinamide adenine dinucleotide phosphate (NADPH) diaphorase histochemistry in the brains of amphibians. J Comp Neurol 522:2980–3003

    Article  CAS  PubMed  Google Scholar 

  • Pongrácz P, Molnár C, Miklósi Á (2009) Dog barking: a specific way of dog–human communication. J Vet Behav 4:54

    Article  Google Scholar 

  • Prato-Previde E, Custance DM, Spiezio C, Sabatini F (2003) Is the dog–human relationship an attachment bond? An observational study using Ainsworth’s strange situation. Behavior 140:225–254

    Article  Google Scholar 

  • Prehn A, Ohrt A, Sojka B, Ferstl R, Pause BM (2006) Chemosensory anxiety signals augment the startle reflex in humans. Neurosci Lett 394:127–130

    Article  CAS  PubMed  Google Scholar 

  • Racca A, Guo K, Meints K, Mills DS (2012) Reading faces: differential lateral gaze bias in processing canine and human facial expressions in dogs and 4-year-old children. PLoS ONE 7:e36076

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rehn T, McGowan RT, Keeling LJ (2013) Evaluating the strange situation procedure (SSP) to assess the bond between dogs and humans. PLoS ONE 8:e56938

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rilling JK, Gutman DA, Zeh TR, Pagnoni G, Berns GS, Kilts CD (2002) A neural basis for social cooperation. Neuron 35:395–405

    Article  CAS  PubMed  Google Scholar 

  • Scandurra A, Prato-Previde E, Valsecchi P, Aria M, D’Aniello B (2015) Guide dogs as a model for investigating the effect of life experience and training on gazing behavior. Anim Cogn 18:937–944

    Article  PubMed  Google Scholar 

  • Scandurra A, Alterisio A, D’Aniello B (2016) Behavioral effects of training on water rescue dogs in the Strange Situation Test. Appl Anim Behav Sci 174:121–127

    Article  Google Scholar 

  • Scandurra A, Alterisio A, Marinelli L, Mongillo P, Semin GR, D’Aniello B (2017) Effectiveness of verbal and gestural signals and familiarity with signal-senders on the performance of working dogs. Appl Anim Behav Sci 191:78–83

    Article  Google Scholar 

  • Schoon GA, De Bruin JC (1994) The ability of dogs to recognize and cross-match human odors. Forensic Sci Int 69:111–118

    Article  CAS  PubMed  Google Scholar 

  • Schultz W, Dayan P, Montague PR (1997) A neural substrate of prediction and reward. Science 275:1593–1599

    Article  CAS  PubMed  Google Scholar 

  • Semin GR (2007) Grounding communication: Synchrony. In: Kruglanski AW, Higgins ET (eds) Social psychology: handbook of basic principles. Guilford Press, New York, pp 630–649

    Google Scholar 

  • Semin GR, de Groot JH (2013) The chemical bases of human sociality. Trends Cogn Sci 17:427–429

    Article  PubMed  Google Scholar 

  • Siniscalchi M, Sasso R, Pepe AM, Dimatteo S, Vallortigara G, Quaranta A (2011) Sniffing with the right nostril: lateralization of response to odor stimuli by dogs. Anim Behav 82:399–404

    Article  Google Scholar 

  • Siniscalchi M, Pergola G, Quaranta A (2013) Detour behavior in attack-trained dogs: left-turners perform better than right-turners. Laterality 18:282–293

    Article  PubMed  Google Scholar 

  • Siniscalchi M, d’Ingeo S, Quaranta A (2016) The dog nose “KNOWS” fear: asymmetric nostril use during sniffing at canine and human emotional stimuli. Behav Brain Res 304:34–41

    Article  PubMed  Google Scholar 

  • Stevenson RJ (2009) The psychology of flavour. Oxford University Press, Oxford

    Book  Google Scholar 

  • Sümegi Z, Oláh K, Topál J (2014) Emotional contagion in dogs as measured by change in cognitive task performance. Appl Anim Behav Sci 160:106–115

    Article  Google Scholar 

  • Svartberg K (2006) Breed-typical behavior in dogs—historical remnants or recent constructs? Appl Anim Behav Sci 96:293–313

    Article  Google Scholar 

  • Tarvainen MP, Niskanen JP, Lipponen JA, Ranta-Aho PO, Karjalainen PA (2014) Kubios HRV–heart rate variability analysis software. Comput Methods Programs Biomed 113:210–220

    Article  PubMed  Google Scholar 

  • Thesen A, Steen JB, Doving KB (1993) Behavior of dogs during olfactory tracking. J Exp Biol 180:247–251

    CAS  PubMed  Google Scholar 

  • Topál J, Miklósi Á, Csányi V, Dóka A (1998) Attachment behavior in dogs (Canis familiaris): a new application of Ainsworth’s (1969) Strange Situation Test. J Comp Psychol 112:219

    Article  PubMed  Google Scholar 

  • Topál J, Gergely G, Erdőhegyi Á, Csibra G, Miklósi Á (2009) Differential sensitivity to human communication in dogs, wolves, and human infants. Science 325:1269–1272

    Article  PubMed  Google Scholar 

  • Udell MA, Brubaker L (2016) Are dogs social generalists? Canine social cognition, attachment, and the dog–human bond. Curr Dir Psychol Sci 25:327–333

    Article  Google Scholar 

  • Udell MA, Wynne CD (2008) A review of domestic dogs’ (Canis familiaris) human-like behaviors: or why behavior analysts should stop worrying and love their dogs. J Exp Anal Behav 89:247–261

    Article  PubMed  PubMed Central  Google Scholar 

  • Udell MA, Wynne CD (2010) Ontogeny and phylogeny: both are essential to human-sensitive behavior in the genus Canis. Anim Behav 79:e9–e14

    Article  Google Scholar 

  • Udell MA, Dorey NR, Wynne CD (2010) What did domestication do to dogs? A new account of dogs’ sensitivity to human actions. Biol Rev 85:327–345

    Article  PubMed  Google Scholar 

  • Van der Ploeg HM (1980) Validity of the Zelf-Beoordelings-Vragenlijst (A Dutch version of the Spielberger State-Trait Anxiety Inventory). Ned Tijdschr Geneeskd 35:243–249

    Google Scholar 

  • Weisbard C, Graham FK (1971) Heart-rate change as a component of the orienting response in monkeys. J Comp Physiol Psychol 76:74

    Article  CAS  PubMed  Google Scholar 

  • Wyatt TD (2015) How animals communicate via pheromones. Am Sci 103:114

    Article  Google Scholar 

  • Wynne CD, Udell MA, Lord KA (2008) Ontogeny’s impacts on human–dog communication. Anim Behav 76:e1–e4

    Article  Google Scholar 

  • Yong MH, Ruffman T (2014) Emotional contagion: dogs and humans show a similar physiological response to human infant crying. Behav Process 108:155–165

    Article  Google Scholar 

  • Zahn-Waxler C, Hollenbeck B, Radke-Yarrow M (1984) The origins of empathy and altruism. In: Fox MW, Mickley LD (eds) Advances in animal welfare science. Kluwer Academic, Norwell, pp 21–41

    Google Scholar 

  • Zhou W, Chen D (2009) Fear-related chemosignals modulate recognition of fear in ambiguous facial expressions. Psychol Sci 20:177–183

    Article  PubMed  Google Scholar 

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Acknowledgements

The authors would like to thank all the handlers who participated in the test with great enthusiasm. This research was supported by ordinary funding from the University of Naples “Federico II”. G.R. Semin gratefully acknowledges the financial support provided by the Portuguese Science Foundation (IF/00085/2013/CP1186/CT0001).

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Correspondence to Biagio D’Aniello.

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This study was approved by the Ethical Animal Care and Use Committee of the University of Naples “Federico II” (Protocol Number 2017/0025509). All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

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Informed consent was obtained from the owners of all dogs included in the study.

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D’Aniello, B., Semin, G.R., Alterisio, A. et al. Interspecies transmission of emotional information via chemosignals: from humans to dogs (Canis lupus familiaris). Anim Cogn 21, 67–78 (2018). https://doi.org/10.1007/s10071-017-1139-x

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