The ability to discriminate between different individuals based on identity cues, which is important to support the social behaviour of many animal species, has mostly been investigated in conspecific contexts. A rare example of individual heterospecific discrimination is found in domestic dogs, who are capable of recognising their owners’ voices. Here, we test whether grey wolves, the nearest wild relative of dogs, also have the ability to distinguish familiar human voices, which would indicate that dogs’ ability is not a consequence of domestication. Using the habituation–dishabituation paradigm, we presented captive wolves with playback recordings of their keepers’ and strangers’ voices producing either familiar or unfamiliar phrases. The duration of their response was significantly longer when presented with keepers’ voices than with strangers’ voices, demonstrating that wolves discriminated between familiar and unfamiliar speakers. This suggests that dogs’ ability to discriminate between human voices was probably present in their common ancestor and may support the idea that this is a general ability of vertebrates to recognise heterospecific individuals. Our study also provides further evidence for familiar voice discrimination in a wild animal in captivity, indicating that this ability may be widespread across vertebrate species.
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The datasets generated during and/or analysed during the current study are available at the following address: https://github.com/sciabola/Grey-wolves-voice-discrimination.
Adachi I, Hiroko K, Fujita K (2007) Dogs recall their owner’s face upon hearing the owner’s voice. Anim Cogn 10:17–21. https://doi.org/10.1007/s10071-006-0025-8
Albuquerque N, Guo K, Wilkinson A, Savalli C, Otta E, Mills D (2016) Dogs recognize dog and human emotions. Biol Lett. https://doi.org/10.1098/rsbl.2015.0883
Balieiro F, Monticelli PF (2019) Evidence of individual discrimination in the maned wolf long-distance extended bark. Behav Processes 158:219–227. https://doi.org/10.1016/j.beproc.2018.12.004
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 Processes 110:37–46. https://doi.org/10.1016/j.beproc.2014.02.011
Candiotti A, Zuberbühler K, Lemasson A (2013) Voice discrimination in four primates. Behav Proc 99:67–72. https://doi.org/10.1016/j.beproc.2013.06.010
Carlson Nora V, McKenna KE, Couzin I (2020) Individual vocal recognition across taxa: a review of the literature and a look into the future. Phil Trans R Soc. https://doi.org/10.1098/rstb.2019.0479
Cheney DL, Seyfarth RM (1982) Recognition of individuals within and between groups of free-ranging vervet monkeys. Am Zool 22:519–529. https://doi.org/10.1093/icb/22.3.519
Cohen J (1960) A coefficient of agreement for nominal scales. Educ Psychol Measur 20(1):37–46. https://doi.org/10.1177/001316446002000104
Coutellier L (2006) Are dogs able to recognize their handler’s voice? A preliminary study. Anthrozoös 19:278–284. https://doi.org/10.2752/089279306785415529
Friard O, Gamba M (2016) BORIS: a free, versatile open-source event-logging software for video/audio coding and live observations. Methods Ecol Evolut 7:1325–1330. https://doi.org/10.1111/2041-210X.12584
Gábor A, Kaszás N, Faragó T, Pérez Fraga P, Lova M, Andics A (2022) The acoustic bases of human voice identity processing in dogs. Anim Cong. https://doi.org/10.1007/s10071-022-01601-z
Godard R (1991) Long-term memory of individual neighbours in a migratory songbird. Nature 350:228–229. https://doi.org/10.1038/350228a0
Goodmann PA, Klinghammer E, Willard J (2002) Wolf ethogram (revised 2002). Eckhard H, Hess Institute of Ethology, Battle Ground, IN
Goumas M, Boogert NJ, Kelley LA, Holding T (2022) Predator or provider? How wild animals respond to mixed messages from humans. Roy Soc Open Sci 9(3):211742. https://doi.org/10.1098/rsos.211742
Harrington FH, Mech LD (1978) Wolf vocalization. In: Hall RL, Sharp HS (eds) Wolf and man: evolution in parallel. Academic, New York, NY, pp 109–132
Holekamp KE, Boydston EE, Szykam M, Graham I, Nutt KJ, Birch S, Piskiel A, Singh M (1999) Vocal recognition in the spotted hyaena and its possible implications regarding the evolution of intelligence. Anim Behav 58:383–395. https://doi.org/10.1006/anbe.1999.1157
Huber L, Racca A, Scafb B, Virányi Z, Range F (2013) Discrimination of familiar human faces in dogs (Canis familiaris). Learn Motiv 44:258–269. https://doi.org/10.1016/j.lmot.2013.04.005
Johnston RE, Bullock TA (2001) Individual recognition by use of odours in golden hamsters: the nature of individual representations. Anim Behav 61:545–555. https://doi.org/10.1006/anbe.2000.1637
Jouventin P, Aubin T (2002) Acoustic systems are adapted to breeding ecologies: individual recognition in nesting penguins. Anim Behav 64:747–757. https://doi.org/10.1006/anbe.2002.4002
Kaur AW, Ackels T, Kuo TH, Cichy A, Dey S, Hays C, Kateri M, Logan DW, Marton TF, Spehr M, Stowers L (2014) Murine pheromone proteins constitute a context-dependent combinatorial code governing multiple social behaviors. Cell 157:676–688. https://doi.org/10.1016/j.cell.2014.02.025
Kriengwatana B, Escudero P, Cate C (2015) Revisiting vocal perceptioninnon-human animals: are viewof vowel discrimination, speaker voice recognition, and speaker normalization. Front Psychol. https://doi.org/10.3389/fpsyg.2014.01543
Kubinyi E, Viranyi Z, Miklosi A (2007) Comparative social cognition: from wolf and dog to humans. Comp Cogn Behav Rev 2:26–46. https://doi.org/10.3819/ccbr.2008.20002
Lank DB, Dale J (2001) Visual signals for individual identification: the silent ‘“song”’ of ruffs. Auk 118:759–765. https://doi.org/10.1093/auk/118.3.759
Leroux M, Hetem RS, Hausberger M, Lemasson A (2018) Cheetahs discriminate familiar and unfamiliar human voices. Sci Rep. https://doi.org/10.1038/s41598-018-33971-1
Magrath RD, Haff TM, Fallow PM, Radford AN (2015) Eavesdropping on heterospecific alarm calls: from mechanisms to consequences. Biol Rev 90:560–586. https://doi.org/10.1111/brv.12122
Manser MB, Seyfarth RM, Cheney DL (2002) Suricate alarm calls signal predator class and urgency. Trends Cogn Sci 6:55–57. https://doi.org/10.1016/S1364-6613(00)01840-4
McComb K, Shannon G, Sayialelb KN, Mossb C (2014) Elephants can determine ethnicity, gender, and age from acoustic cues in human voices. Proc Natl Acad Sci USA 111:5433–5438. https://doi.org/10.1073/pnas.1321543111
Molnár C, Pongrácz P, Dóka A, Miklósi A (2006) Can humans discriminate between dogs on the base of the acoustic parameters of barks? Behav Proc 73:76–83. https://doi.org/10.1016/j.beproc.2006.03.014
Palacios V, Font E, Marquez R, Carazo P (2015) Recognition of familiarity on the basis of howls: a playback experiment in a captive group of wolves. Behaviour 152:593–614. https://doi.org/10.1163/1568539X-00003244
Parr LA, Winslow JT, Hopkins WD, de Waal FBM (2000) Recognizing facial cues: individual discrimination by chimpanzees (Pan troglodytes) and rhesus monkeys (Macaca mulatta). J Comp Psychol 114(1):47–60. https://doi.org/10.1037/0735-7036.114.1.47
Peirce JW, Leigh AE, daCosta APC, Kendrick KM (2001) Human face recognition in sheep: lack of configurational coding and right hemisphere advantage. Behav Proc 55:13–26. https://doi.org/10.1016/S0376-6357(01)00158-9
Proops L, McComb K (2012) Cross-modal individual recognition in domestic horses (Equus caballus) extends to familiar humans. Proc R Soc B 279:3131–3138. https://doi.org/10.1098/rspb.2012.0626Rakotonirina
Proops L, McComb K, Reby D (2009) Cross-modal individual recognition in domestic horses (Equus caballus). Proc Natl Acad Sci USA 106:947–951. https://doi.org/10.1073/pnas.0809127105
Rakotonirina H, Kappeler PM, Fichtel C (2018) The role of facial pattern variation for species recognition in red-fronted lemurs (Eulemur rufifrons). BMC Evol Biol. https://doi.org/10.1186/s12862-018-1126-0
Randler C (2006) Red squirrels (Sciurus vulgaris) respond to alarm calls of eurasian jays (Garrulus glandarius). Ethology 112:411–416. https://doi.org/10.1111/j.1439-0310.2006.01191.x
Ranjard L, Anderson MG, Rayner MJ, Payne RB, McLean I, Briskie JV, Ross HA, Brunton DH, Woolley SMN, Hauber ME (2010) Bioacoustic distances between the begging calls of brood parasites and their host species: a comparison of metrics and techniques. Behav Ecol Sociobiol 64:1915–1926. https://doi.org/10.1007/s00265-010-1065-2
Ratcliffe VF, McComb K, Reby D (2014) Cross-modal discrimination of human gender by domestic dogs. Anim Behav 91:127–135. https://doi.org/10.1016/j.anbehav.2014.03.009
Rendall D, Rodman PS, Emond RE (1996) Vocal recognition of individuals and kin in free ranging rhesus monkeys. Anim Behav 51:1007–1015. https://doi.org/10.1006/anbe.1996.0103
Root-Gutteridge H, Ratcliffe VF, Korzeniowska AT, Reby D (2019) Dogs perceive and spontaneously normalize formant-related speaker and vowel differences in human speech sounds. Biol Lett. https://doi.org/10.1098/rsbl.2019.0555
Saito A, Shinozuka K (2013) Vocal recognition of owners by domestic cats (Felis catus). Anim Cogn 16:685–690. https://doi.org/10.1007/s10071-013-0620-4
Salmi R, Jones CE, Carrigan J (2020) Who is there? Captive western gorillas distinguish human voices based on familiarity and nature of previous interactions. Anim Cogn 25:217–228. https://doi.org/10.1007/s10071-021-01543-y
Seiler M, Schwitzer C, Gamba M, Holderied MW (2013) Interspecific semantic alarm call recognition in the solitary Sahamalaza Sportive Lemur, Lepilemur sahamalazensis. PLoS One. https://doi.org/10.1371/journal.pone.0067397
Seyfarth RM, Cheney DL, Marler P (1980) Vervet monkey alarm calls: semantic communication in a free-ranging primate. Anim Behav 28:1070–1094. https://doi.org/10.1016/S0003-3472(80)80097-2
Siniscalchi M, D’Ingeo S, Minunno M, Quaranta A (2018) Communication in dogs. Animals 8:131. https://doi.org/10.3390/ani8080131
Sliwa J, Duhamel JR, Pascalis O, Wirth S (2011) Spontaneous voice–face identity matching by rhesus monkeys for familiar conspecifics and humans. Proc Natl Acad Sci USA 108:1735–1740. https://doi.org/10.1073/pnas.1008169108
Theberge FJB (1967) Howling as a means of communication in timber wolves. Am Zool 7:331–338. https://doi.org/10.1093/icb/7.2.331
Wascher CAF, Szipl G, Boeckle M, Wilkinson A (2012) You sound familiar: carrion crows can differentiate between the calls of known and unknown heterospecifics. Anim Cogn 15:1015–1019. https://doi.org/10.1007/s10071-012-0508-8
Young SJ, Woodland PC, Byrne WJ (1993) HTK: Hidden Markov model toolkit V1. 5. Cambridge Univ. Eng. Dept. Speech Group and Entropic Research Lab. Inc., Washington DC
We would like to thank Enrique Font and Pau Carazo for their support at the Cavanilles Institute of Biodiversity and Evolutionary Biology. We thank “Centro del Lobo Ibérico Félix Rodríguez de la Fuente”, “La Grandera”, “Centro de Naturaleza Cañada Real”, “Centro de Education Ambiental La Dehesa” and “Lobo Park” for making possible the study realization. DR and HRG were supported by BBSRC grant BB/P00170X/1 (How dogs hear us) and DR was also supported by the University of Lyon IDEXLYON project as part of the ‘Programme Investissements d’Avenir’ (ANR-16-IDEX-0005). We would also like to thank the three reviewers whose helpful comments substantially improved the manuscript.
Conflict of interest
Beatrice Gammino was supported by the Erasmus traineeship program of the University of Turin. David Reby and Holly Root-Gutteridge were supported by BBSRC grant BB/P00170X/1 (How dogs hear us) and David Reby was also supported by the University of Lyon IDEXLYON project as part of the ‘Programme Investissements d’Avenir’ (ANR-16-IDEX-0005). The authors have no financial or proprietary interests in any material discussed in this article.
All the institutions hosting the animals granted permission to conduct this study. Playbacks were always emitted from outside the enclosures without invasive or exceptional manipulation of the subjects and wolves were monitored for any signs of stress. If any had been observed, the study would have been suspended. The care of the wolves adhered to the guidelines of the European Endangered Species Program, developed by the European Association and Zoos and Aquaria (EAZA). We collected consent forms for all the individuals who contributed recordings of their voices we then used during the experiments. Due to the absence of potential discomfort for the wolves (e.g., separation of the animals during the playbacks, direct contact with humans), the study did not require approval from the Ethics Committee of the Department of Life Sciences and Systems Biology of the University of Torino at the time the experiments were performed.
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Gammino, B., Palacios, V., Root-Gutteridge, H. et al. Grey wolves (Canis lupus) discriminate between familiar and unfamiliar human voices. Anim Cogn 26, 1589–1600 (2023). https://doi.org/10.1007/s10071-023-01796-9