Abstract
Rescue behavior is considered a type of pro-social response, defined as a voluntary action directed to benefit another individual who is in a stressful or dangerous situation. In two experiments, we investigated whether dogs would rescue their owners when the person was trapped inside a wooden box and emitted clear signs of stress. The performance of these dogs was compared against that of a control group in which the owners remained calm while trapped. In addition, to assess if training modulated this behavior, we tested a group of dogs from the military trained in search and rescue tasks (Experiment 1). Results showed that dogs opened the box more frequently when the owner pretended to be stressed than when calm. Training shortened latencies to open the door but not the frequency of the behavior. In Experiment 2, we investigated if emotional contagion could be a possible mechanism underlying dogs' rescue responses by measuring dogs’ behavior, heart rate, and saliva cortisol level in the stressed and calm conditions, and also controlled for obedience by having the calm owners call their pets while trapped. We replicated the findings of Experiment 1 as more dogs opened the door in the stressed owner condition than in the calm condition. In addition, we observed an increase in heart rate across trials in the stressed condition and a decrease across trials in the calm condition, but no differences in cortisol levels or stress-related behaviors between conditions. In brief, we found evidence that approximately half of the dogs without previous training showed spontaneous rescue behaviors directed to their owners. Neither was this behavior motivated by obedience nor by the motivation to re-establish social contact with the owner. We conclude that emotional contagion is a plausible mechanism underlying dogs’ rescue behavior in the present protocol.
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References
Albuquerque N, Guo K, Wilkinson A, Otta E, Mills D (2016) Dogs recognize dog and human emotions. Biol Lett. https://doi.org/10.1098/rsbl.2015.0883
Barber A, Muller E, Randi D, Muller C, Huber L (2017) Heart rate changes in pet and lab dogs as response to human Facial expressions. ARC J Anim Vet Sci. https://doi.org/10.20431/2455-2518.0302005
Barrera G, Mustaca A, Bentosela M (2011) Communication between domestic dogs and humans: effects of shelter housing upon the gaze to the human. Anim Cog 14:727–734
Bartal IBA, Decety J, Mason P (2011) Empathy and pro-social behavior in rats. Science 334:1427–1430. https://doi.org/10.1126/science.1210789
Beerda B, Schilder MB, van Hooff JA, de Vries HW (1997) Manifestations of chronic and acute stress in dogs. Appl Anim Behav Sci 52(3–4):307–319
Beerda B, Schilder MB, van Hooff JA, de Vries HW, Mol JA (1998) Behavioural, saliva cortisol and heart rate responses to different types of stimuli in dogs. Appl Anim Behav Sci 58(3–4):365–381
Bergeron R, Scott SL, Émond JP, Mercier F, Cook NJ, Schaefer AI (2002) Physiology and behavior of dogs during air transport. Can J Vet Res 66(3):211–216
Bräuer J, Schönefeld K, Call J (2013) When do dogs help humans? Appl Anim Behav Sci 148(138):149. https://doi.org/10.1016/j.applanim.2013.07.009
Brosnan SF (2013) Justice- and fairness-related behaviors in nonhuman primates. P Natl Aacad Sci 110:10416–10423. https://doi.org/10.1073/pnas.1301194110
Bshary R, Raihani NJ (2017) Helping in humans and other animals: a fruitful interdisciplinary dialogue. P R Soc B 284:20170929. https://doi.org/10.1098/rspb.2017.0929
Carballo F, Freidin E, Putrino N, Shimabukuro C, Casanave E, Bentosela M (2015) Dog’s discrimination of human selfish and generous attitudes: the role of individual recognition, experience, and experimenters’ sex. PLoS ONE 10:e0116314. https://doi.org/10.1371/journal.pone.0116314
Carballo F, Freidin E, Casanave EB, Bentosela M (2017) Dogs’ recognition of human selfish and generous attitudes requires little but critical experience with people. PLoS ONE 12:e0185696. https://doi.org/10.1371/journal.pone.0185696
Carter GG, Wilkinson GS (2013) Food sharing in vampire bats: reciprocal help predicts donations more than relatedness or harassment. P R Soc B280:20122573–20122573. https://doi.org/10.1098/rspb.2012.2573
Custance D, Mayer J (2012) Emphatic-like responding by domestic dogs (Canis familiaris) to distress in humans: an exploratory study. Anim Cog 15:851–859. https://doi.org/10.1007/s10071-012-0510-1
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 Processes 110:68–73. https://doi.org/10.1016/j.beproc.2014.09.022
Damián JP, Bengoa L, Pessina P, Martínez S, Fumagalli F (2018) Serial collection method of dog saliva: Effects of different chemical stimulants on behaviour, volume and saliva composition. Open Vet J 8(3):229–235. https://doi.org/10.4314/ovj.v8i3.1
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. https://doi.org/10.1007/s10071-017-1098-2
D'Aniello B, Semin GR, Alterisio A, Aria M, Scandurra A (2018) Interspecies transmission of emotional information via chemosignals: from humans to dogs (Canis lupus familiaris). Anim Cogn 21(1):67–78
Diverio S, Menchetti L, Riggio G, Azzari C, Iaboni M, Zasso R, Di Mari W, Santoro M (2017) Dogs’ coping styles and dog-handler relationships influence avalanche search team performance. Appl Anim Behav Sci 191:67–77. https://doi.org/10.1016/j.applanim.2017.02.005
Fallani G, Prato Previde E, Valsecchi P (2007) Behavioral and physiological responses of guide dogs to a situation of emotional distress. Physiol Behav 90:648–655. https://doi.org/10.1016/j.physbeh.2006.12.001. https://doi.org/10.1007/s10071-017-1139-x
Freidin E, Putrino N, D’Orazio M, Bentosela M (2013) Dogs’ eavesdropping from people’s reactions in third party interactions. PLoS ONE 8:e79198. https://doi.org/10.1371/journal.pone.0079198
Freidin E, Carballo F, Bentosela M (2017) Direct reciprocity in animals: the roles of bonding and affective processes. Int J Psychol 52:163–170. https://doi.org/10.1002/ijop.12215
Galibert F, Quignon P, Hitte C, André C (2011) Toward understanding dog evolutionary and domestication history. CR Biol 334(3):190–196. https://doi.org/10.1016/j.crvi.2010.12.011
Gfrerer N, Taborsky M (2017) Working dogs cooperate among one another by generalized reciprocity. Nature Sci Rep 7:43–67. https://doi.org/10.1038/srep43867
Hare B, Tomasello M (2005) Human-like social skills in dogs? Trends Cogn Sci 9:439–444. https://doi.org/10.1016/j.tics.2005.07.003
Hatfield E, Cacioppo JT, Rapson RL (1994) Emotional contagion: Studies in emotion and social interaction. Editions de la Maison des sciences de l’homme.
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(4):703–715. https://doi.org/10.1007/s10071-017-1092-8
Jezierski T, Adamkiewicz E, Walczak M, Sobczyńska M, Górecka-Bruzda A, Ensminger J, Papet E (2014) Efficacy of drug detection by fully-trained police dogs varies by breed, training level, type of drug and search environment. Forensic Sci Int 237:112–118. https://doi.org/10.1016/j.forsciint.2014.01.013
Kaminski J, Neumann M, Bräuer J, Call J, Tomasello M (2011) Dogs, Canis Faniliaris, Communicate with humans to request but not to inform. Anim Behav 82:651–658
Kaminski J, Nitzschner M (2013) Do dogs get the point? A review of dog–human communication ability Learn Motiv 44 294 302 10.1016/j.lmot.2013.05.001.
King T, Hemsworth PH, Coleman GJ (2003) Fear of novel and startling stimuli in domestic dogs. Appl Anim Behavr Sci 82(1):45–64. https://doi.org/10.1016/S0168-1591(03)00040-6
Kundey S, De Los RA, Arbuthnot J, Allen R, Cochum A, Molina S, Royer E (2010a) Domesticated dogs’ (Canis familiris) response to dishonest human points. Int J Comp Psychol 23:201–215
Kundey S, De Los Reyes A, Royer E, Molina S, Monnier B, German R, Coshun A (2010b) Reputation-like inference in domestic dogs (Canis familiris). Anim Cogn 14:291–302. https://doi.org/10.1007/s10071-010-0362-5
Macpherson K, Roberts WA (2006) Do dogs (Canis familiris) seek help in an emergency? J Comp Psychol 120:113–119. https://doi.org/10.1037/0735-7036.120.2.113
Marshall-Pescini S, Passalacqua C, Barnard S, Valsecchi P, Prato-Previde E (2009) Agility and search and rescue training differently affects pet dogs’ behaviour in socio-cognitive tasks. Behav Proc 81(3):416–422. https://doi.org/10.1016/j.beproc.2009.03.015
Marshall-Pescini S, Passalacqua C, Ferrario A, Valsecchi P, Prato-Previde E (2011) Social eavesdropping in the domestic dog. Anim Behav 81:1177–1183. https://doi.org/10.1016/j.anbehav.2011.02.029
Marshall-Pescini S, Colombo E, Passalacqua C, Merola I, Prato-Previde E (2013) Gaze alternation in dogs and toddlers in an unsolvable task: evidence of an audience effect. Anim Cogn 16:933–943. https://doi.org/10.1007/s10071-013-0627-x
Marshall-Pescini S, Dale R, Quervel-Chaumette M, Range F (2016) Critical issues in experimental studies of prosociality in non-human species. Anim Cogn 19:679–705. https://doi.org/10.1007/s10071-016-0973-6
McGowan RT, Bolte C, Barnett HR, Perez-Camargo G, Martin F (2018) Can you spare 15 min? The measurable positive impact of a 15-min petting session on shelter dog well-being. Appl Anim Behav Sci 203:42–54. https://doi.org/10.1016/j.applanim.2018.02.011
Merola I, Prato-Previde E, Lazzaroni M, Marshall-Pescini S (2013) Dogs’ comprehension of referential emotional expressions: familiar people and familiar emotions are easier. Anim Cogn 17:373–385. https://doi.org/10.1007/s10071-013-0668-1
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. https://doi.org/10.1016/j.tics.2013.04.005
Moberg GP (2000) Biological response to stress: implications for animal welfare. In: Moberg GP, Mench JA (eds) The biology of animal stress: basic principles and implications for animal welfare. CABI Publishing, Wallingford, Oxon, UK, pp 1–22
Müller CA, Schmitt K, Barber ALA, Huber L (2015) Dogs can discriminate emotional expressions of human faces. Curr Biol 25:601–605. https://doi.org/10.1016/j.cub.2014.12.055
Nagasawa M, Mitsui S, En S, Ohtani N, Ohta M, Sakuma Y, Onaka T, Mogi K, Kikusui T (2015) Oxytocin-gaze positive loop and the coevolution of human-dog bonds. Science 348(6232):333–336. https://doi.org/10.1126/science.1261022
Nitzschner M, Melis AP, Kaminski J, Tomasello M (2012) Dogs (Canis familiris) Evaluate humans on the basis of direct experiences only. PLoS ONE 7:e46880. https://doi.org/10.1371/journal.pone.0046880
Nowak MA (2006) Five rules for the evolution of cooperation. Science 314:1560–1563. https://doi.org/10.1126/science.1133755
Nowbahari E, Hollis K (2010) Distinguishing between recue, cooperation and other forms of altruistic behavior. Communicative and Integrative Biology 3(2):77–79
Nowbahari E, Scohier A, Durand J-L, Hollis KL (2009) Ants, cataglyphis cursor, use precisely directed rescue behavior to free entrapped relatives. PLoS ONE 4:e6573. https://doi.org/10.1371/journal.pone.0006573
Pacák K, Palkovits M, Yadid G, Kvetnansky R, Kopin IJ, Goldstein DS (1998) Heterogeneous neurochemical responses to different stressors: a test of Selye’s doctrine of nonspecificity. Am J Physiol Regul Integr Comp Physiol 275:1247–1255
Palestrini C, Previde EP, Spiezio C, Verga M (2005) Heart rate and behavioural responses of dogs in the Ainsworth’s Strange Situation: A pilot study. Appl Anim Behav Sci 94:75–88. https://doi.org/10.1016/j.applanim.2005.02.005
Panksepp J, Panksepp JB (2013) Toward a cross-species understanding of empathy. Trends Neurosci 36:489–496. https://doi.org/10.1016/j.tins.2013.04.009
Parthasarathy V, Crowell-Davis SL (2006) Relationship between attachment to owners and separation anxiety in pet dogs (Canis lupus familiris). J Vet Behav 1:109–120. https://doi.org/10.1016/j.jveb.2006.09.005
Plotnik JM, Lair R, Suphachoksahakun W, de Waal FBM (2011) Elephants know when they need a helping trunk in a cooperative task. P Natl Aacad Sci 108:5116–5121. https://doi.org/10.1073/pnas.1101765108
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. Behaviour 140:225–254. https://doi.org/10.1163/156853903321671514
Quervel-Chaumette M, Dale R, Marshall-Pescini S, Range F (2015) Familiarity affects other-regarding preferences in pet dogs. Sci Rep Uk 5:18102. https://doi.org/10.1038/srep18102
Quervel-Chaumette M, Mainix G, Range F, Marshall-Pescini S (2016) Dogs Do Not Show Pro-social Preferences towards Humans. Front Psychol 7:1416. https://doi.org/10.3389/fpsyg.2016.01416
Rehn T, Handlin L, Uvnäs-Moberg K, Keeling LJ (2014) Dogs’ endocrine and behavioural responses at reunion are affected by how the human initiates contact. Physiol Behav 124:45–53. https://doi.org/10.1016/j.physbeh.2013.10.009
Sanford EM, Burt ER, Meyers-Manor JE (2018) Timmy’s in the well: Empathy and prosocial helping in dogs. Learning & behavior 46(4):374–386. https://doi.org/10.3758/s13420-018-0332-3
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. https://doi.org/10.1007/s10071-015-0864-2
Scandurra A, Alterisio A, D'Aniello B (2016) Behavioural effects of training on water rescue dogs in the Strange Situation Test. Appl Anim Behavr Sci 174:121–127
Schwab C, Huber L (2006) Obey or not obey? Dogs (Canis familiaris) behave differently in response to attentional states of their owners. J Comp Psychol 120:69–175. https://doi.org/10.1037/0735-7036.120.3.169
Silberberg A, Allouch C, Sandfort S, Kearns D, Karpel H, Slotnick B (2013) Desire for social contact, not empathy, may explain “rescue” behavior in rats. Anim Cogn 17:609–618. https://doi.org/10.1007/s10071-013-0692-1
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. https://doi.org/10.1016/j.applanim.2014.09.001
Szetei V, Miklósi Á, Topál J, Csányi V (2003) When dogs seem to lose their nose: an investigation on the use of visual and olfactory cues in communicative context between dog and owner. Appl Anim Behav Sci 83:141–152. https://doi.org/10.1016/s0168-1591(03)00114-x
Topál J, Miklósi Á, Csányi V, Dóka A (1998) Attachment Behavior in Dogs (Canis familiris): A New Application of Ainsworth's (1969) Strange Situation Test. J Comp Psychol 112(3):219–229
Udell MA, Dorey N, Wynne CDL (2008) Wolves outperform dogs in following human social cues. Anim Behav 76:1767–1773. https://doi.org/10.1016/j.anbehav.2008.07.028
Vasconcelos M, Hollis K, Nowbahari E, Kacelnik A (2012) Pro-sociality without empathy. Biol Lett 8:910–912. https://doi.org/10.1098/rsbl.2012.0554
Vilà C, Savolainen P, Maldonado JE, Amorim IR, Rice JE, Honeycutt RL, Crandall KA, Lundeberg J, Wayne RK (1997) Multiple and ancient origins of the domestic dog. Science 276:1687–1689. https://doi.org/10.1126/science.276.5319.1687
Walker JK, Dale AR, D’Eath RB, Wemelsfelder F (2016) Qualitative Behaviour Assessment of dogs in the shelter and home environment and relationship with quantitative behaviour assessment and physiological responses. Appl Anim Behav Sci 184:97–108. https://doi.org/10.1016/j.applanim.2016.08.012
Wallis LJ, Range F, Müller CA, Serisier S, Huber L, Virányi Z (2015) Training for eye contact modulates gaze following in dogs. Anim Behav 106:27–35. https://doi.org/10.1016/j.anbehav.2015.04.020
Warneken F (2015) Precocious Prosociality: Why Do Young Children Help? Child Dev Perspect 9:1–6. https://doi.org/10.1111/cdep.12101
Yong MH, Ruffman T (2014) Emotional contagion: Dogs and humans show a similar physiological response to human infant crying. Behav Processes 108:155–165. https://doi.org/10.1016/j.beproc.2014.10.006
Acknowledgements
This work was financially supported by Consejo Nacional de Investigaciones Científicas y Técnicas: PIP 11220130100182, Agencia Nacional de Promoción Científica y Tecnológica: PICT 2014 N0883 to MB and Universidad Nacional del Sur: PGI 24/B243 INBIOSUR to EBC. We would like to express our special gratitude to all the owners who kindly participated in these experiments. We also thank Hugo Carballo, who helped in the building of the apparatus, to the Captain Martin Carbone and the Batallón “Perros de Guerra” who received us at the Puerto Belgrano’s military installations, and to Gabriel Granada who helped us finding the facilities to run the tests. Finally we would like to thank the Editor and three anonymous reviewers for their valuable comments which helped to improve the article.
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Carballo, F., Dzik, V., Freidin, E. et al. Do dogs rescue their owners from a stressful situation? A behavioral and physiological assessment. Anim Cogn 23, 389–403 (2020). https://doi.org/10.1007/s10071-019-01343-5
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DOI: https://doi.org/10.1007/s10071-019-01343-5