Intra and interspecific audience effect on domestic dogs' behavioural displays and facial expressions.
Animal communication
Audience effects
Displacement behaviours
Domestic dog
Facial expressions
Interspecific communication
Intraspecific communication
Stress signals
Visual signals
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
25 04 2024
25 04 2024
Historique:
received:
22
12
2023
accepted:
02
04
2024
medline:
26
4
2024
pubmed:
26
4
2024
entrez:
25
4
2024
Statut:
epublish
Résumé
The aim of the current study was to investigate the influence of both intra- and interspecific audiences on dogs' facial expressions and behaviours. Forty-six dogs were exposed to three test conditions in which a food reward, initially available, was denied when in the presence of either a human (Human condition) or a dog audience (Dog condition), or in the absence of a visible audience (Non-social condition). Salivary cortisol was collected to evaluate the stress/arousal activation in the different conditions. Compared to the Non-social condition, the presence of a conspecific evoked more facial expressions, according to the DogFACS (Facial Action Coding System, an anatomically based tool to analyze facial expressions in domestic dogs), (EAD105-Ears downward), displacement behaviours (AD137-Nose licking, AD37-Lip wiping), tail wagging, whining, and panting (AD126). When facing a conspecific, dogs assumed a more avoidant attitude, keeping a distance and not looking at the stimuli, compared to when in the presence of the human partner. Dogs also exhibited more facial expressions (EAD102-Ears Adductor, EAD104-Ears Rotator), displacement behaviours (AD137-Nose licking, AD37-Lip wiping), panting (AD126) and whining when facing the conspecific than the human partner. Post-test cortisol was not influenced by any condition, and no association between pre-test cortisol and behavioural variables was found, thus strong differences in the levels of stress/arousal were unlikely to be responsible for differences in behavior between conditions. Considering the current results in the context of the available literature, we suggest that the higher displacement behaviors exhibited with the conspecifics were likely due to an increased level of uncertainty regarding the situations.
Identifiants
pubmed: 38664496
doi: 10.1038/s41598-024-58757-6
pii: 10.1038/s41598-024-58757-6
doi:
Substances chimiques
Hydrocortisone
WI4X0X7BPJ
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
9546Subventions
Organisme : Austrian Science Fund
ID : P34675G
Informations de copyright
© 2024. The Author(s).
Références
Simpson, B. S. Canine communication. Vet. Clin. N. Am. Small Anim. Practice 27(3), 445–464. https://doi.org/10.1016/S0195-5616(97)50048-9 (1997).
doi: 10.1016/S0195-5616(97)50048-9
Doupe, A. J. & Kuhl, P. K. Birdsong and human speech: Common themes and mechanisms. Ann. Rev. Neurosci. 22, 567–631. https://doi.org/10.1146/annurev.neuro.22.1.567 (1999).
doi: 10.1146/annurev.neuro.22.1.567
pubmed: 10202549
Peters, S. & Nowicki, S. Overproduction and attrition: The fates of songs memorized during song learning in songbirds. Anim. Behav. 124, 255–261. https://doi.org/10.1016/j.anbehav.2016.09.019 (2017).
doi: 10.1016/j.anbehav.2016.09.019
Townsend, S. W. & Manser, M. B. Functionally referential communication in mammals: The past, present and the future. Ethology 119(1), 1–11. https://doi.org/10.1111/eth.12015 (2013).
doi: 10.1111/eth.12015
Tinbergen, N. ‘Derived’ activities; their causation, biological significance, origin, and emancipation during evolution. Quart. Rev. Biol. 27(1), 1–32. https://doi.org/10.1086/398642 (1952).
doi: 10.1086/398642
pubmed: 14930222
Maglieri, V., Zanoli, A., Mastrandrea, F. & Palagi, E. The relaxed open mouth is a true signal in dogs: Demonstrating Tinbergen’s ritualization process. Anim. Behav. 188, 65–74. https://doi.org/10.1016/j.anbehav.2022.03.015 (2022).
doi: 10.1016/j.anbehav.2022.03.015
Sherman, P. W. Nepotism and the evolution of alarm calls. Science 197(4310), 1246–1253. https://doi.org/10.1126/science.197.4310.1246 (1977).
doi: 10.1126/science.197.4310.1246
pubmed: 17781971
Evans, C. S. & Marler, P. Food calling and audience effects in male chickens (Gallus gallus): Their relationship to food availability, courtship, and social facilitation. Anim. Behav. 47(5), 1159–1170 (1994).
doi: 10.1006/anbe.1994.1154
Wich, S. A. & de Vries, H. Male monkeys remember which group members have given alarm calls. Proc. Royal Soc. B Biol. Sci. 273, 735–740 (2006).
doi: 10.1098/rspb.2005.3320
Demuru, E., Ferrari, P. F. & Palagi, E. Emotionality and intentionality in bonobo playful communication. Anim. Cognit. 18(1), 333–344. https://doi.org/10.1007/s10071-014-0804-6 (2015).
doi: 10.1007/s10071-014-0804-6
Kaminski, J., Hynds, J., Morris, P. & Waller, B. M. Human attention affects facial expressions in domestic dogs. Sci. Rep. 7(1), 12914. https://doi.org/10.1038/s41598-017-12781-x (2017).
doi: 10.1038/s41598-017-12781-x
pubmed: 29051517
pmcid: 5648750
Pedretti, G. et al. Audience effect on domestic dogs’ behavioural displays and facial expressions. Sci. Rep. 12(1), 9747. https://doi.org/10.1038/s41598-022-13566-7 (2022).
doi: 10.1038/s41598-022-13566-7
pubmed: 35697913
pmcid: 9192729
Kuhne, F., Hößler, J. C. & Struwe, R. Emotions in dogs being petted by a familiar or unfamiliar person: Validating behavioural indicators of emotional states using heart rate variability. Appl. Animal Behav. Sci. 161, 113–120. https://doi.org/10.1016/j.applanim.2014.09.020 (2014).
doi: 10.1016/j.applanim.2014.09.020
Firnkes, A., Bartels, A., Bidoli, E. & Erhard, M. Appeasement signals used by dogs during dog–human communication. J. Vet. Behav. 19, 35–44. https://doi.org/10.1016/j.jveb.2016.12.012 (2017).
doi: 10.1016/j.jveb.2016.12.012
Siniscalchi, M., d’Ingeo, S., Minunno, M. & Quaranta, A. Communication in dogs. Animals 8(8), 131. https://doi.org/10.3390/ani8080131 (2018).
doi: 10.3390/ani8080131
pubmed: 30065156
pmcid: 6116041
Hauser, M. D. Perseveration, inhibition and the prefrontal cortex: A new look. Curr. Opinion Neurobiol. 9(2), 214–222. https://doi.org/10.1016/S0959-4388(99)80030-0 (1999).
doi: 10.1016/S0959-4388(99)80030-0
Gillam, E. An introduction to animal communication. Nat. Educ. Knowl. 3(10), 70 (2011).
Siniscalchi, M., Lusito, R., Vallortigara, G. & Quaranta, A. Seeing left- or right-asymmetric tail wagging produces different emotional responses in dogs. Curr. Biol. 23(22), 2279–2282. https://doi.org/10.1016/j.cub.2013.09.027 (2013).
doi: 10.1016/j.cub.2013.09.027
pubmed: 24184108
Mariti, C. et al. Analysis of the intraspecific visual communication in the domestic dog (Canis familiaris): A pilot study on the case of calming signals. J. Vet. Behav. 18, 49–55. https://doi.org/10.1016/j.jveb.2016.12.009 (2017).
doi: 10.1016/j.jveb.2016.12.009
Pedretti, G., Canori, C., Biffi, E., Marshall-Pescini, S. & Valsecchi, P. Appeasement function of displacement behaviours? Dogs’ behavioural displays exhibited towards threatening and neutral humans. Animal Cognit. https://doi.org/10.1007/s10071-023-01742-9 (2023).
doi: 10.1007/s10071-023-01742-9
Crivelli, C. & Fridlund, A. J. Facial displays are tools for social influence. Trends Cognit. Sci. 22(5), 388–399. https://doi.org/10.1016/j.tics.2018.02.006 (2018).
doi: 10.1016/j.tics.2018.02.006
Waller, B. M., Whitehouse, J. & Micheletta, J. Rethinking primate facial expression: A predictive framework. Neurosci. Biobehav. Rev. 82, 13–21. https://doi.org/10.1016/j.neubiorev.2016.09.005 (2017).
doi: 10.1016/j.neubiorev.2016.09.005
pubmed: 27637495
Parr, L. A. & Waller, B. M. Understanding chimpanzee facial expression: Insights into the evolution of communication. Social Cognit. Affect. Neurosci. 1(3), 221–228. https://doi.org/10.1093/scan/nsl031 (2006).
doi: 10.1093/scan/nsl031
Pedretti, G., Canori, C., Marshall-Pescini, S., Pavan, G. & Valsecchi, P. Behavioural analysis of dogs’ response to threatening and neutral conspecific video stimuli. Appl. Sci. 13(16), 9254. https://doi.org/10.3390/app13169254 (2023).
doi: 10.3390/app13169254
Topál, J., Miklósi, Á., Csányi, V. & Dóka, A. Attachment behavior in dogs (Canis familiaris): A new application of Ainsworth’s (1969) Strange Situation Test. J. Comp. Psychol. 112(3), 219–229. https://doi.org/10.1037/0735-7036.112.3.219 (1998).
doi: 10.1037/0735-7036.112.3.219
pubmed: 9770312
Prato-Previde, E., Spiezio, C., Sabatini, F. & Custance, D. M. Is the dog-human relationship an attachment bond? An observational study using Ainsworth’s strange situation. Behaviour 140(2), 225–254. https://doi.org/10.1163/156853903321671514 (2003).
doi: 10.1163/156853903321671514
Gácsi, M., Maros, K., Sernkvist, S., Faragó, T. & Miklósi, Á. Human analogue safe haven effect of the owner: Behavioural and heart rate response to stressful social stimuli in dogs. PLoS ONE 8(3), e58475. https://doi.org/10.1371/journal.pone.0058475 (2013).
doi: 10.1371/journal.pone.0058475
pubmed: 23469283
pmcid: 3587610
Cimarelli, G., Marshall-Pescini, S., Range, F. & Virányi, Z. Pet dogs’ relationships vary rather individually than according to partner’s species. Sci. Rep. 9(1), 3437. https://doi.org/10.1038/s41598-019-40164-x (2019).
doi: 10.1038/s41598-019-40164-x
pubmed: 30837560
pmcid: 6401312
Range, F., Marshall-Pescini, S., Kratz, C. & Virányi, Z. Wolves lead and dogs follow, but they both cooperate with humans. Sci. Rep. 9(1), 3796. https://doi.org/10.1038/s41598-019-40468-y (2019).
doi: 10.1038/s41598-019-40468-y
pubmed: 30846770
pmcid: 6405935
Range, F., Ritter, C. & Virányi, Z. Testing the myth: Tolerant dogs and aggressive wolves. Proc. R. Soc. B Biol. Sci. 282(1807), 20150220. https://doi.org/10.1098/rspb.2015.0220 (2015).
doi: 10.1098/rspb.2015.0220
Dale, C. & Range, S. Avoiding conflicts: Wolves and dogs. Behav. Ecol. Sociobiol. 71(7), 107 (2017).
doi: 10.1007/s00265-017-2339-8
pubmed: 28725102
pmcid: 5493712
Soproni, K., Miklósi, A., Topál, J. & Csányi, V. Comprehension of human communicative signs in pet dogs (Canis familiaris). J. Comp. Psychol. 115(2), 122–126. https://doi.org/10.1037/0735-7036.115.2.122 (2001).
doi: 10.1037/0735-7036.115.2.122
pubmed: 11459158
Virányi, Z., Topál, J., Gácsi, M., Miklósi, Á. & Csányi, V. Dogs respond appropriately to cues of humans’ attentional focus. Behav. Process. 66(2), 161–172. https://doi.org/10.1016/j.beproc.2004.01.012 (2004).
doi: 10.1016/j.beproc.2004.01.012
Miklósi, Á., Topál, J. & Csányi, V. Comparative social cognition: What can dogs teach us?. Animal Behav. 67(6), 995–1004. https://doi.org/10.1016/j.anbehav.2003.10.008 (2004).
doi: 10.1016/j.anbehav.2003.10.008
Andics, A. et al. Neural mechanisms for lexical processing in dogs. Science. 353(6303), 1030–1032. https://doi.org/10.1126/science.aaf3777 (2016).
doi: 10.1126/science.aaf3777
pubmed: 27576923
Albuquerque, N., Guo, K., Wilkinson, A., Resende, B. & Mills, D. S. Mouth-licking by dogs as a response to emotional stimuli. Behav. Process. 146, 42–45. https://doi.org/10.1016/j.beproc.2017.11.006 (2018).
doi: 10.1016/j.beproc.2017.11.006
Albuquerque, N. et al. Dogs recognize dog and human emotions. Biol. Lett. 12(1), 20150883. https://doi.org/10.1098/rsbl.2015.0883 (2016).
doi: 10.1098/rsbl.2015.0883
pubmed: 26763220
pmcid: 4785927
D’Aniello, B., Semin, G. R., Alterisio, A., Aria, M. & Scandurra, A. Interspecies transmission of emotional information via chemosignals: From humans to dogs (Canis lupus familiaris). Animal Cognit. 21(1), 67–78. https://doi.org/10.1007/s10071-017-1139-x (2018).
doi: 10.1007/s10071-017-1139-x
Miklósi, A., Polgárdi, R., Topál, J. & Csányi, V. Intentional behaviour in dog-human communication: An experimental analysis of “showing” behaviour in the dog. Animal Cognit. 3(3), 159–166. https://doi.org/10.1007/s100710000072 (2000).
doi: 10.1007/s100710000072
Heberlein, M. T. E., Turner, D. C., Range, F. & Virányi, Z. A comparison between wolves, Canis lupus, and dogs, Canis familiaris, in showing behaviour towards humans. Animal Behav. 122, 59–66. https://doi.org/10.1016/j.anbehav.2016.09.023 (2016).
doi: 10.1016/j.anbehav.2016.09.023
Prato-Previde, E. et al. When the owner does not know: Comparing puppies and adult dogs’ showing behavior. Animal Cognit. https://doi.org/10.1007/s10071-023-01744-7 (2023).
doi: 10.1007/s10071-023-01744-7
Slabbert, J. M. & Rasa, O. A. E. Observational learning of an acquired maternal behaviour pattern by working dog pups: An alternative training method?. Appl. Animal Behav. Sci. 53(4), 309–316. https://doi.org/10.1016/S0168-1591(96)01163-X (1997).
doi: 10.1016/S0168-1591(96)01163-X
Bremhorst, A., Sutter, N. A., Würbel, H., Mills, D. S. & Riemer, S. Differences in facial expressions during positive anticipation and frustration in dogs awaiting a reward. Sci. Rep. 9(1), 19312. https://doi.org/10.1038/s41598-019-55714-6 (2019).
doi: 10.1038/s41598-019-55714-6
pubmed: 31848389
pmcid: 6917793
Coppinger, B. et al. Studying audience effects in animals: What we can learn from human language research. Animal Behav. 124, 161–165. https://doi.org/10.1016/j.anbehav.2016.12.020 (2017).
doi: 10.1016/j.anbehav.2016.12.020
Marshall-Pescini, S. Importance of a species’ socioecology: Wolves outperform dogs in a conspecific cooperation task. Proc. Natl. Acad. Sci. USA. 114(2017), 11793–11798. https://doi.org/10.1073/pnas.1709027114 (2017).
doi: 10.1073/pnas.1709027114
pubmed: 29078337
pmcid: 5676910
Range, F., Marshall-Pescini, S. (2022). Social Dynamics Between Conspecifics. In: Wolves and Dogs. Fascinating Life Sciences. Springer, Cham. https://doi.org/10.1007/978-3-030-98411-3_5
Bremhorst, A., Mills, D. S., Würbel, H. & Riemer, S. Evaluating the accuracy of facial expressions as emotion indicators across contexts in dogs. Animal Cognit. https://doi.org/10.1007/s10071-021-01532-1 (2021).
doi: 10.1007/s10071-021-01532-1
Caeiro, C., Guo, K. & Mills, D. Dogs and humans respond to emotionally competent stimuli by producing different facial actions. Sci. Rep. 7(1), 15525. https://doi.org/10.1038/s41598-017-15091-4 (2017).
doi: 10.1038/s41598-017-15091-4
pubmed: 29138393
pmcid: 5686192
Beerda, B., Schilder, M. B. H., van Hooff, J. A. R. A. M. & de Vries, H. W. Manifestations of chronic and acute stress in dogs. Appl. Animal Behav. Sci. 52(3–4), 307–319. https://doi.org/10.1016/S0168-1591(96)01131-8 (1997).
doi: 10.1016/S0168-1591(96)01131-8
Rooney, N., Gaines, S. & Hiby, E. A practitioner’s guide to working dog welfare. J. Vet. Behav. 4(3), 127–134. https://doi.org/10.1016/j.jveb.2008.10.037 (2009).
doi: 10.1016/j.jveb.2008.10.037
Bonanni, R. et al. Age-graded dominance hierarchies and social tolerance in packs of free-ranging dogs. Behav. Ecol. 28(4), 1004–1020. https://doi.org/10.1093/beheco/arx059 (2018).
doi: 10.1093/beheco/arx059
Bálint, A. et al. “Do not choose as I do!”—Dogs avoid the food that is indicated by another dog’s gaze in a two-object choice task. Appl. Animal Behav. Sci. 170, 44–53. https://doi.org/10.1016/j.applanim.2015.06.005 (2015).
doi: 10.1016/j.applanim.2015.06.005
Dale, R., Marshall-Pescini, S. & Range, F. Do females use their sexual status to gain resource access? Investigating food-for-sex in wolves and dogs. Curr. Zool. 63(3), 323–330. https://doi.org/10.1093/cz/zow111 (2017).
doi: 10.1093/cz/zow111
pubmed: 29491991
pmcid: 5804177
Chmelíková, E. et al. Salivary cortisol as a marker of acute stress in dogs: A review. Domest. Anim. Endocrinol. 72, 106428. https://doi.org/10.1016/j.domaniend.2019.106428 (2020).
doi: 10.1016/j.domaniend.2019.106428
pubmed: 32213439
Rooney, N. J., Gaines, S. A. & Bradshaw, J. W. S. Behavioural and glucocorticoid responses of dogs (Canis familiaris) to kennelling: Investigating mitigation of stress by prior habituation. Physiol. Behav. 92(5), 847–854. https://doi.org/10.1016/j.physbeh.2007.06.011 (2007).
doi: 10.1016/j.physbeh.2007.06.011
pubmed: 17617429
Palme, R. & Mostl, E. Measurement of cortisol metabolites in faeces of sheep as a parameter of cortisol concentration in blood. Z. Saugetierkd. Int. J. Mammal. Biol. 62(2), 192–197 (1997).
Ekman, P., Friesen, W.V. and Hager, J.C. (1978) Facial Action Coding System (FACS). A Technique for the Measurement of Facial Action. Consulting, Palo Alto, 22.
Waller, B. et al. Paedomorphic facial expressions give dogs a selective advantage. PloS One 8, e82686 (2013).
doi: 10.1371/journal.pone.0082686
pubmed: 24386109
pmcid: 3873274
Forstmeier, W. & Schielzeth, H. Cryptic multiple hypotheses testing in linear models: Overestimated effect sizes and the winners curse. Behav. Ecol. Sociobiol. 65, 47–55 (2011).
doi: 10.1007/s00265-010-1038-5
pubmed: 21297852
Dobson, A. J. An Introduction to Generalized Linear Models (Chapman Hall/CRC, 2002).