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Smell facilitates auditory contagious yawning in stranger rats

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Abstract

Most vertebrates yawn in situations ranging from relaxation to tension, but only humans and other primate species that show mental state attribution skills have been convincingly shown to display yawn contagion. Whether complex forms of empathy are necessary for yawn contagion to occur is still unclear. As empathy is a phylogenetically continuous trait, simple forms of empathy, such as emotional contagion, might be sufficient for non-primate species to show contagious yawning. In this study, we exposed pairs of male rats, which were selected for high yawning, with each other through a perforated wall and found that olfactory cues stimulated yawning, whereas visual cues inhibited it. Unexpectedly, cage-mate rats failed to show yawn contagion, although they did show correlated emotional reactivity. In contrast, stranger rats showed auditory contagious yawning and greater rates of smell-facilitated auditory contagious yawning, although they did not show correlated emotional reactivity. Strikingly, they did not show contagious yawning to rats from a low-yawning strain. These findings indicate that contagious yawning may be a widespread trait amongst vertebrates and that mechanisms other than empathy may be involved. We suggest that a communicatory function of yawning may be the mechanism responsible for yawn contagion in rats, as contagiousness was strain-specific and increased with olfactory cues, which are involved in mutual recognition.

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References

  • Adams DB, Schoel WM (1982) A statistical analysis of the social behavior of the male stumptail macaque (Macaca arctoides). Am J Primatol 2:249–273

    Article  Google Scholar 

  • Anderson JR, Myowa-Yamakoshi M, Matsuzawa T (2004) Contagious yawning in chimpanzees. Proc R Soc Lond B 271:S468–S470

    Article  Google Scholar 

  • Anias J, Holmgren B, Urbá-Holmgren R, Eguibar JR (1984) Circadian variation of yawning behavior. Acta Neurobiol Exp 44:179–186

    CAS  Google Scholar 

  • Arnott SR, Singhal A, Goodale MA (2009) An investigation of auditory contagious yawning. Cogn Affect Behav Neurosci 9:335–342

    Article  PubMed  Google Scholar 

  • Baenninger R (1987) Some comparative aspects of yawning in Betta splendens, Homo sapiens, Panthera leo, and Papio sphinx. J Comp Psychol 101:349–354

    Article  Google Scholar 

  • Bartholomew AJ, Cirulli ET (2014) Individual variation in contagious yawning susceptibility is highly stable and largely unexplained by empathy or other known factors. PLoS ONE 9:e91773

    Article  PubMed Central  PubMed  Google Scholar 

  • Ben-Ami Bartal I, Decety J, Mason P (2011) Empathy and pro-social behavior in rats. Science 334:1427–1430

    Article  PubMed  Google Scholar 

  • Boissy A (1995) Fear and fearfulness in animals. Q Rev Biol 70:165–191

    Article  CAS  PubMed  Google Scholar 

  • Bradbury JW, Vehrencamp SL (1998) Principles of animal communication. Sinauer Associates, Sunderland

    Google Scholar 

  • Bradbury JW, Vehrencamp SL (2011) Principles of animal communication, 2nd edn. Sinauer Associates, Sunderland

    Google Scholar 

  • Brennan PA, Kendrick KM (2006) Mammalian social odours: attraction and individual recognition. Phil Trans R Soc B 361:2061–2078

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Brennan PA, Zufall F (2006) Pheromonal communication in vertebrates. Nature 444:308–315

    Article  CAS  PubMed  Google Scholar 

  • Brudzynski SM, Fletcher NH (2010) Rat ultrasonic vocalization: short-range communication. In: Brudzynski SM (ed) Handbook of mammalian vocalization. Academic Press, Oxford, pp 69–76

    Chapter  Google Scholar 

  • Byrne RW (1994) The evolution of intelligence. In: Slater PJB, Halliday TR (eds) Behaviour and evolution. Cambridge University Press, Cambridge, pp 223–265

    Google Scholar 

  • Campbell MW, de Waal FMB (2010) Methodological problems in the study of contagious yawning. In: Walusinski O (ed) The mistery of yawning in physiology and disease: frontiers of neurology and neuroscience. Karger, Basel, pp 120–127

    Chapter  Google Scholar 

  • Campbell MW, de Waal FMB (2011) Ingroup-outgroup bias in contagious yawning by chimpanzees supports link to empathy. PlosONE 6:e18283

    Article  CAS  Google Scholar 

  • Campbell MW, de Waal FBM (2014) Chimpanzees empathize with group mates and humans, but not with baboons or unfamiliar chimpanzees. Proc R Soc B 281:20140013. doi:10.1098/rspb.2014.0013

    Article  PubMed  Google Scholar 

  • Campbell MW, Carter JD, Proctor D, Eisenberg ML, de Waal FMB (2009) Computer animations stimulate contagious yawning in chimpanzees. Proc R Soc B 276:4255–4259

    Article  PubMed Central  PubMed  Google Scholar 

  • Collins GT, Eguibar JR (2010) Neuropharmachology of yawning. In: Walusinski O (ed) The mystery of yawning in physiology and disease: frontiers of neurology and neuroscience. Karger, Basel, pp 90–106

    Chapter  Google Scholar 

  • Crawley MJ (2007) The R book. Wiley, Chichester

    Book  Google Scholar 

  • Delius JD (1967) Displacement activities and arousal. Nature 214:1259–1260

    Article  CAS  PubMed  Google Scholar 

  • Demuru E, Palagi E (2012) In bonobos yawn contagion is higher among kin and friends. Plose ONE 7:e49613

    Article  CAS  Google Scholar 

  • Deputte BL (1994) Ethological study of yawning in primates. I. Quantitative analysis and study of causation in two species of old world monkeys (Cercocebus albigena and Macaca fascicularis). Ethology 98:221–245

    Article  Google Scholar 

  • Dunstan FDJ (1993) Time series analysis. In: Fry JC (ed) Biological data analysis: a practical approach. Oxford University Press, Oxford, pp 243–310

    Google Scholar 

  • Gallup AC, Gallup GG Jr (2008) Yawning and thermoregulation. Physiol Behav 95:10–16

    Article  CAS  PubMed  Google Scholar 

  • Greco M, Baenninger R, Govern J (1993) On the context of yawning: when, where, and why? Psychol Rec 43:175–183

    Google Scholar 

  • Guggisberg AG, Mathis J, Schnider A, Hess CW (2010) Why do we yawn? Neurosci Biobehav Rev 34:1267–1276

    Article  PubMed  Google Scholar 

  • Harr AL, Gilbert VR, Phillips KA (2009) Do dogs (Canis familiaris) show contagious yawning? Anim Cogn 12:833–837

    Article  PubMed  Google Scholar 

  • Hatfield E, Cacioppo JT, Rapson RL (1993) Emotional contagion. Curr Dir Psychol Sci 2:96–99

    Article  Google Scholar 

  • Holmgren B, Urbá-Holmgren R, Aguiar M, Rodríguez R (1980) Sex hormone influences on yawning behavior. Acta Neurobiol Exp 40:515–519

    CAS  Google Scholar 

  • Holmgren B, Urbá-Holmgren R, Trucios N, Zermeño M, Eguibar JR (1985) Association of spontaneous and dopaminergic-induced yawning and penile erection in the rat. Pharmacol Biochem Behav 22:31–35

    Article  CAS  PubMed  Google Scholar 

  • Holmgren B, Budelli R, Urbá-Holmgren R, Eguibar JR, Holmgren M, Baz-Tellez G, Anias J (1991) Food anticipatory yawning rhythm in the rat. Acta Neurobiol Exp 51:97–105

    CAS  Google Scholar 

  • Hurst JL, Beynon RJ (2004) Scent wars: the chemobiology of competitive signalling in mice. BioEssays 26:1288–1298

    Article  CAS  PubMed  Google Scholar 

  • Huston JP (1971) Yawning and penile erection induced in rats by cortical spreading depression. Nature 232:274–275

    Article  CAS  PubMed  Google Scholar 

  • Johnston RE (2003) Chemical communication in rodents: from pheromones to individual recognition. J Mammal 84:1141–1162

    Article  Google Scholar 

  • Joly-Mascheroni RM, Senju A, Shepherd AJ (2008) Dogs catch human yawns. Biol Lett 4:446–448

    Article  PubMed Central  PubMed  Google Scholar 

  • Langford DJ, Crager SE, Shehzad Z, Smith SB, Sotocinal G, Levenstadt JS, Chanda ML, Levitin DJ, Mogil JS (2006) Social modulation of pain as evidence for empathy in mice. Science 312:1967–1970

    Article  CAS  PubMed  Google Scholar 

  • McKenzie AA (1994) The tonsillar evacuation hypothesis of yawning behaviour. S Afr J Sci 90:64–66

    Google Scholar 

  • Melis MR, Mauri A, Argiolas A (1994) Apomorphine- and oxytocin-induced penile erections and yawning in intact and castrated male rats: effect of sexual steroids. Neuroendocrinology 59:349–354

    Article  CAS  PubMed  Google Scholar 

  • Mendl M, Burman OHP, Paul ES (2010) An integrative and functional framework for the study of animal emotion and mood. Proc R Soc Lond B 277:2895–2904

    Article  Google Scholar 

  • Miller ML, Gallup AC, Vogel AR, Vicario SM, Clark AB (2012) Evidence for contagious behaviors in budgerigars (Melopsittacus undulatus): an observational study of yawning and stretching. Behav Process 89:264–270

    Article  Google Scholar 

  • Moyaho A, Valencia J (2002) Grooming and yawning trace adjustment to unfamiliar environments in laboratory Sprague-Dawley rats (Rattus norvegicus). J Comp Psychol 116:263–269

    Article  PubMed  Google Scholar 

  • Moyaho A, Eguibar JR, Díaz JL (1995) Induced grooming transitions and open field behaviour differ in high- and low-yawning sublines of Sprague-Dawley rats. Anim Behav 50:61–72

    Article  Google Scholar 

  • Moyaho A, Barajas M, Ugarte A, Eguibar JR (2009) Genetic and littermate influences on yawning in two selectively bred strains of rats. Dev Psychobiol 51:243–248

    Article  PubMed  Google Scholar 

  • O’Hara SJ, Reeve AV (2011) A test of the yawning contagion and emotional connectedness hypothesis in dogs, Canis familiaris. Anim Behav 81:335–340

    Article  Google Scholar 

  • Palagi E, Leone A, Mancini G, Ferrari PF (2009) Contagious yawning in gelada baboons as a possible expression of empathy. Proc Natl Acad Sci USA 17:19262–19267

    Article  Google Scholar 

  • Paukner A, Anderson JR (2006) Video-induced yawning in stumptail macaques (Macaca arctoides). Biol Lett 2:36–38

    Article  PubMed Central  PubMed  Google Scholar 

  • Phoenix CH, Chambers KC (1982) Sexual behavior in adult gonadectomized female pseudohermaphrodite, female and male rhesus macaques treated with estradiol benzoate and testosterone proprionate. J Comp Physiol Psychol 96:823–833

    Article  CAS  PubMed  Google Scholar 

  • Platek SM, Critton SR, Myers TE, Gallup GG Jr (2003) Contagious yawning: the role of self-awareness and mental state attribution. Cogn Brain Res 17:223–227

    Article  Google Scholar 

  • Preston SD, de Waal FBM (2002) Empathy: its ultimate and proximate bases. Behav Brain Sci 25:1–72

    PubMed  Google Scholar 

  • Provine RR (1986) Yawning as a stereotyped action pattern and releasing stimulus. Ethology 72:109–122

    Article  Google Scholar 

  • Provine RR, Hamernik HB, Curchack BC (1987) Yawning: relation to sleeping and stretching in humans. Ethology 76:152–160

    Article  Google Scholar 

  • Prusky GT, Harker KT, Douglas RM, Whishaw IQ (2002) Variation in visual acuity within pigmented, and between pigmented and albino rat strain. Behav Brain Res 136:339–348

    Article  PubMed  Google Scholar 

  • Ramos A, Mormède P (1998) Stress and emotionality: a multidimensional and genetic approach. Neurosci Biobehav Rev 22:33–57

    Article  CAS  PubMed  Google Scholar 

  • R Development Core Team (2012) R: a language and environment for statistical computing. R foundation for statistical computing, Vienna

  • Redican WK (1982) An evolution perspective on human facial displays. In: Ekman P (ed) Emotion in the human face, 2nd edn. Cambridge University Press, Cambridge UK, pp 212–280

    Google Scholar 

  • Romero T, Konno A, Hasegawa T (2013) Familiarity bias and physiological responses in contagious yawning by dogs support link to empathy. PLoS ONE 8:e71365

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sauer EG, Sauer EM (1967) Yawning and other maintenance activities in the South African Ostrich. Auk 84:571–587

    Article  Google Scholar 

  • Silberberg A, Allouch C, Sandfort S, Kearns D, Karpel H, Slotnick B (2014) Desire for social contact, not empathy, may explain “rescue” behavior in rats. Anim Cogn 17:609–618

    Article  PubMed  Google Scholar 

  • Silva K, Bessa J, Sousa L (2012) Auditory contagious yawning in domestic dogs (Canis familiaris): first evidence for social modulation. Anim Cogn 15:721–724

    Article  PubMed  Google Scholar 

  • Sinervo B, Miles DB, Frankino WA, Klukowski M, DeNardo DF (2000) Testosterone, endurance, and Darwinian fitness: natural and sexual selection on the physiological bases of alternative male behaviors in side-blotched lizards. Horm Behav 38:222–233

    Article  CAS  PubMed  Google Scholar 

  • Smith EO (1999) Yawning: an evolutionary perspective. Hum Evol 14:191–198

    Article  Google Scholar 

  • Urbá-Holmgren R, Trucios N, Holmgren B, Eguibar JR, Gavito A, Cruz G, Santos A (1990) Genotypic dependency of spontaneous yawning frequency in the rat. Behav Brain Res 40:29–35

    Article  PubMed  Google Scholar 

  • Usui S, Senju A, Kikuchi Y, Akechi H, Tojo Y, Osanai H, Hasegawa T (2013) Presence of contagious yawning in children with autism spectrum disorder. Autism Res Treat 2013:1–8

    Article  Google Scholar 

  • Voigt CC, von Helversen O (1999) Storage and display of odour by male Saccopteryx bilineata (Chiroptera, Emballonuridae). Behav Ecol Sociobiol 47:29–40

    Article  Google Scholar 

  • Voigt-Heucke SL, Taborsky M, Dechmann DKN (2010) A dual function of echolocation: bats use echolocation calls to identify familiar and unfamiliar individuals. Anim Behav 80:59–67

    Article  Google Scholar 

  • Walusinski O, Deputte BL (2004) The physiology, ethology and nosology of yawning. Rev Neurol (Paris) 160:1011–1021

    Article  CAS  Google Scholar 

  • Wehner R (1997) Sensory systems and behaviour. In: Krebs JR, Davies NB (eds) Behavioural Ecology, 4th edn. Blackwell Science, Oxford, pp 19–41

    Google Scholar 

  • Wu W-J, Sha S-H, McLaren DJ, Kawamoto K, Raphael Y, Schacht J (2001) Aminoglycoside ototoxicity in adult CBA, C57BL and BALB mice and the Sprague-Dawley rat. Hearing Res 158:165–178

    Article  CAS  Google Scholar 

  • Yoon JMD, Tennie C (2010) Contagious yawning: a reflection of empathy, mimicry, or contagion? Anim Behav 79:e1–e3

    Article  Google Scholar 

  • Zentall TR (2011) Social Learning Mechanisms: implications for a cognitive theory of imitation. Interact Stud 12:233–261

    Article  Google Scholar 

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Acknowledgments

We thank E. Beristain Castillo for critical discussions on the manuscript and technical help with drug preparations, and two anonymous referees for constructive comments on an earlier version of the manuscript. We also thank A. Escobar Noriega, R. Camarillo Aragón, O. Isidro Maldonado and M. Ita Amador for observing and recording the rats’ behaviour; and G. Gómez Correa for administering the drug treatment to the rats. A.M. was partially funded by the Vicerrectoría de Investigación y Estudios de Posgrado. The work formed part of the thesis of X.R.-Z. as partial fulfilment of requirements for a BSc Biomedicine degree.

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The authors declare that they have no conflict of interest.

Ethical standard

The experiments complied with all applicable institutional and Mexican laws concerning the use of animals in research.

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Authors and Affiliations

  1. Instituto de Fisiología, Benemérita Universidad Autónoma de Puebla, Avenida 14 Sur 6301, Colonia San Manuel, Puebla, Pue, 72570, Mexico

    Alejandro Moyaho, Xaman Rivas-Zamudio, Araceli Ugarte, José R. Eguibar & Jaime Valencia

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  1. Alejandro Moyaho
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  2. Xaman Rivas-Zamudio
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  3. Araceli Ugarte
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  4. José R. Eguibar
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Correspondence to Alejandro Moyaho.

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Alejandro Moyaho and Xaman Rivas-Zamudio are joint first authors.

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Moyaho, A., Rivas-Zamudio, X., Ugarte, A. et al. Smell facilitates auditory contagious yawning in stranger rats. Anim Cogn 18, 279–290 (2015). https://doi.org/10.1007/s10071-014-0798-0

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