Abstract
Many animal species that rely mainly on calls to communicate produce individual acoustic structures, but we wondered whether individuals of species better known as visual communicants, with small vocal repertoires, would also exhibit individual distinctiveness in calls. Moreover, theoretical advances concerning the evolution of social intelligence are usually based on primate species data, but relatively little is known about the social cognitive capacities of non-primate mammals. However, some non-primate species demonstrate auditory recognition of social categories and possess mental representation of their social network. Horses (Equus caballus) form stable social networks and although they display a large range of visual signals, they also use long-distance whinny calls to maintain contact. Here, we investigated the potential existence of individual acoustic signatures in whinny calls and the ability of horses to discriminate by ear individuals varying in their degree of familiarity. Our analysis of the acoustic structure of whinnies of 30 adult domestic horses (ten stallions, ten geldings, ten mares) revealed that some of the frequency and temporal parameters carried reliable information about the caller’s sex, body size and identity. However, no correlations with age were found. Playback experiments evaluated the behavioural significance of this variability. Twelve horses heard either control white noise or whinnies emitted by group members, familiar neighbours or unfamiliar horses. While control sounds did not induce any particular response, horses discriminated the social category of the callers and reacted with a sound-specific behaviour (vigilance and attraction varied with familiarity). Our results support the existence of social knowledge in horses and suggest a process of vocal coding/decoding of information.
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Barfield CH, Tang-Martinez Z, Trainer JM (1994) Domestic calves (Bos taurus) recognize their own mothers by auditory cues. Ethology 97:257–264
Basile M, Boivin S, Boutin A, Blois-Heulin C, Hausberger M, Lemasson A (2009a) Socially dependent auditory laterality in domestic horses (Equus caballus). Anim Cogn (in press)
Basile M, Lemasson A, Blois-Heulin C (2009b) Social and emotional values of sounds influence human (Homo sapiens) and non-human primate (Cercopithecus campbelli) auditory laterality. Plos One (in press)
Blumstein DT, Daniel JC (2004) Yellow-bellied marmots discriminate between the alarm calls of individuals and are more responsive to calls from juveniles. Anim Behav 68:1257–1265
Blumstein DT, Munos O (2005) Individual, age and sex-specific information is contained in yellow-bellied marmot alarm calls. Anim Behav 69:353–361
Boinski S, Mitchell CL (1997) Chuck vocalizations of wild female squirrel monkeys (Saimiri sciureus) contain information on caller identity and foraging activity. Int J Primatol 18:975–993
Brown ED, Farabaugh SM (1997) What birds with complex social relationships can tell us about vocal learning: vocal sharing in avian groups. In: Snowdon CT, Hausberger M (eds) Social influences on vocal development. Cambridge University Press, Cambridge, pp 98–127
Caldwell JCM, Caldwell DK, Tyack PL (1990) Review of signature-whistle hypothesis for the atlantic bottlenose dolphin. In: Leatherwood S, Reeves RR (eds) The bottlenose dolphin. Academic Press, New York, pp 199–234
Charrier I, Harcourt RG (2006) Individual vocal identity in mother and pup Australian sea lions (Neophoca cinera). J Mammol 87:929–938
Charrier I, Mathevon N, Aubin T, Jouventin P (2001) Acoustic communication in a black-headed gull colony: how chicks identify their parents? Ethology 107:961–974
Charrier I, Mathevon N, Jouventin P (2003) Vocal signature recognition of mothers by fur seal pups. Anim Behav 65:543–550
Cheney DL, Seyfarth RM (1999) Recognition of other individuals’ social relationships by female baboons. Anim Behav 58:67–75
Dallmann R, Geissman T (2001) Different levels of variability in the female song of wild silvery gibbons (Hylobates moloch). Behaviour 138:629–648
de Waal FBM, Tyack PL (2003) Animal social complexity. Harvard University Press, Cambridge
Engh AL, Siebert ER, Greenberg DA, Holekamp KE (2005) Patterns of alliance formation and post-conflict aggression indicate spotted hyaenas recognize third party relationships. Anim Behav 69:209–217
Evans S, Neave N, Wakelin D (2006) Relationships between vocal characteristics and body size and shape in human males: an evolutionary explanation for a deep male voice. Biol Psychol 72:160–163
Ey E, Hammerschmidt K, Seyfarth RM, Fischer J (2007) Age- and sex-related variations in clear calls of Papio ursinus. Int J Primatol 28:947–960
Feh C (2005) Relationships and communication in socially natural horse herds. In: Miller D, Mc Donnell S (eds) The domestic horse. The evolution, development and management of its behaviour. Cambridge University Press, Cambridge, pp 82–93
Feighny JA, Williamson KE, Clarke JA (2006) North American elk bugle vocalizations: male and female bugle call structure and context. J Mammal 87:1072–1077
Fernandez-Juricic E, Campagna C, Enriquez V, Leo Ortiz C (1999) Vocal communication and individual variation in breeding South American sea lions. Behaviour 136:495–517
Fichtel C, Hammerschmidt K, Jürgens U (2001) On the vocal expression of emotion. A multi-parametric analysis of different states of aversion in the squirrel monkey. Behaviour 138:97–116
Fischer J, Kitchen DM, Seyfarth RM, Cheney DL (2004) Baboon loud calls advertise male quality: acoustic features and their relation to rank, age, and exhaustion. Behav Ecol Sociobiol 56:140–148
Fitch W (1997) Vocal tract length and formant frequency dispersion correlate with body size in rhesus macaques. J Acoust Soc Am 102:1213–1221
Fitch WT, Reby D (2001) The descended larynx is not uniquely human. R Soc 268:1669–1675
Ford JKB (1991) Vocal traditions among resident killer whales (Orcinus orca) in coastal waters of British Columbia. Can J Zool 69:1454–1483
Gautier J-P (1978) Répertoire sonore de Cercopithecus cephus. Zeitschrift für Tierpsychologie 46:113–169
Gautier J-P (1988) Interspecific affinities among guenons as deduced from vocalizations. In: Gautier-Hion A, Bourlière F, Gautier J-P, Kingdon J (eds) A primate radiation evolutionary biology of the African guenons. Cambridge University Press, Cambridge, pp 194–226
Gautier J-P, Gautier A (1977) Communication in old world monkeys. In: Sebeok T (ed) How animals communicate. Indiana University Press, Bloomington, pp 890–964
Gouzoules H, Gouzoules S (1989) Design features and developmental modification of pigtail macaque, Macaca nemestrina, agonistic screams. Anim Behav 37:383–401
Gouzoules H, Gouzoules S, Ashley J (1995) Representational signaling in non-human primate vocal communication. In: Zimmermann E, Newman JD, Jürgens U (eds) Current topics in primate vocal communication. Plenum Press, New York, pp 235–252
Hammerschmidt K, Newmann JD, Champoux M, Suomi SJ (2000) Changes in rhesus macaque «coo» vocalizations during early development. Ethology 106:873–886
Hausberger M, Richard J-P, Black JM, Quris R (1994) Quantitative analysis of individuality in barnacle goose loud calls. Bioacoustics 5:247–260
Hausberger M, Richard-Yris M-A, Henry L, Lepage L, Schmidt I (1995) Song sharing reflects the social organization in a captive group of European starling (Sturnus vulgaris). J Comp Psychol 109:222–241
Hauser MD (1989) Ontogenetic changes in the comprehension and production of vervet monkey (C. aethiops) vocalizations. J Comp Psychol 103:149–158
Hauser MD (1993) The evolution of non-human primate vocalizations: effects of phylogeny, body-weight, and social context. Am Naturalist 142:528–542
Heffner HE (1998) Auditory awareness. Appl Anim Behav Sci 57:259–268
Hinde RA (1976) Interactions, relationships, and social structure. Man 11:1–17
Holekamp KE (2007) Questioning the social intelligence hypothesis. Trends Cogn Sci 11:65–69
Janik VM (2000) Whistle matching in wild bottlenose dolphins (Tursiops truncatus). Science 289:1355–1357
Jones G, Ransome R (1993) Echolocation calls of bats are influenced by maternal effects and change over a lifetime. Proc R Soc Lond B 252:125–128
Jouventin P, Aubin T, Lengagne T (1999) Finding a parent in a king penguin colony: the acoustic system of individual recognition. Anim Behav 57:1175–1183
Kent JP (1987) Experiments on the relationships between the hen and chick (Gallus gallus): the role of the auditory mode on recognition and the effects of maternal separation. Behaviour 102:1–14
Kiley M (1972) The vocalizations of ungulates, their causation and function. Zeitschrift für Tierpsychologie 31:171–222
Kober M, Trillmich F, Naguib M (2007) Vocal mother pup communication in guinea pigs: effects of call familiarity and female reproductive state. Anim Behav 73:917–925
Lemasson A, Hausberger M (2004) Patterns of vocal sharing and social dynamics in a captive group of Campbell’s monkeys. J Comp Psychol 118:347–359
Lemasson A, Zuberbühler K, Hausberger M (2005) Socially meaningful vocal plasticity in Campbell’s monkeys. J Comp Psychol 119:220–229
Lemasson A, Palombit RA, Jubin R (2008) Friendships between males and lactating females in a free-ranging group of olive baboons (Papio hamadryas Anubis): evidence from playback experiments. Behav Ecol Sociobiol 62:1027–1035
Lengagne T, Jouventin P, Aubin T (1999) Finding one’s mate in a king penguin colony: efficiency of acoustic communication. Behaviour 136:833–846
Martin-Rosset W (1990) L’alimentation des chevaux. INRA Ed, Paris
Mateo JM, Holmes WG (1999) Plasticity of alarm call response development in belding’s ground squirrels (Spermophilus beldingi, Sciuridae). Ethology 105:193–206
Maurello MA, Clarke JA, Ackley RS (2000) Signature characteristics in contact calls of the white-nosed coati. J Mammal 81:415–421
McComb K, Moss C, Sayialel S, Baker L (2000) Unusually extensive networks of vocal recognition in African elephants. Anim Behav 59:1103–1109
McComb K, Reby D, Baker L, Moss C, Sayialel S (2003) Long-distance communication of acoustic cues to social identity in African elephants. Anim Behav 65:317–329
McCowan B, Hooper SL (2002) Individual acoustic variation in Belding’s ground squirrel alarm chirps in the High Sierra Nevada. J Acoust Soc Am 111:1157–1160
McDonnell SM, Murray SC (1995) Bachelor and harem stallion behavior and endocrinology. Biol Reprod Mono 1:577–590
Mitani JC, Gros-Louis J (1995) Species and sex differences in the screams of chimpanzees and bonobos. Int J Primatol 16:393–411
Ödberg FO (1974) Some aspects of the acoustic expression in horses. In: Zeeb K (ed) Ethologie und Ökologie bei der Haustierhaltung. KTBL, Darmstadt, pp 89–105
Ouattara K, Zuberbühler K, N’goran KE, Gombert J-E, Lemasson A (2009) The alarm call system of female Campbell’s monkeys. Anim Behav (in press)
Poiani A, Fletcher T (1994) Plasma levels of androgens and gonadal development of breeders and helpers in the bell miner (Manorina melanophrys). Behav Ecol Sociobiol 34:31–41
Reby D, McComb K (2003) Anatomical constraints generate honesty: acoustic cues to age and weight in the roars of red deer stags. Anim Behav 65:519–530
Rendall D, Rodman PS, Edmond RE (1996) Vocal recognition of individuals and kin in free-ranging rhesus monkeys. Anim Behav 51:1007–1015
Rendall D, Owren MJ, Rodman PS (1998) The role of vocal tract filtering in identity cueing in rhesus monkey (Macaca mulatta) vocalizations. J Acoust Soc Am 103:602–614
Richard J-P (1991) Sound analysis and synthesis using an amiga micro-computer. Bioacoustics 3:45–60
Robisson P, Aubin T, Brémond JC (1993) Individuality in the voice of emperor penguin Aptenodytes forsteri: adaptation to a noisy environment. Ethology 94:279–290
Rubenstein D, Hack M (1992) Horse signals: the sounds and scents of fury. Evol Ecol 6:254–260
Saltzman W, Schultz-Darken NJ, Wegner FH, Wittwer DJ, Abbott DH (1998) Suppression of cortisol levels in subordinate female marmosets: reproductive and social contributions. Horm Behav 33:58–74
Sanvito S, Galimberti F, Miller EH (2006) Vocal signalling of male southern elephant seals is honest but imprecise. Anim Behav 73:287–299
Searby A, Jouventin P (2003) Mother-young acoustic recognition in sheep: a frequency coding. Proc R Soc Lond B 270:1765–1771
Sèbe F, Nowak R, Poindron P, Aubin T (2007) Establishment of vocal communication and discrimination between ewes and their lamb in the first two days after parturition. Dev Psychobiol 49:375–386
Seyfarth RM, Cheney DL (1986) Vocal development in Vervet Monkeys. Anim Behav 34:1640–1658
Seyfarth RM, Cheney DL, Bergman TJ (2005) Primate social cognition and the origins of language. Trends Cogn Sci 9:264–266
Soltis J, Leong K, Savage A (2005) African elephant vocal communication. I. antiphonal calling behaviour among affiliated females. Anim Behav 70:579–587
Sousa-Lima RS, Paglia AP, Da Fonseca GAB (2002) Signature information and individual recognition in the isolation calls of Amazonian manatees, Trichechus inunguis (Mammalia: Sirenia). Anim Behav 63:301–310
Vannoni E, McElligot AG (2007) Individual acoustic variation in fallow deer (Dama dama) common and harsh groans: a source-filter theory perspective. Ethology 113:223–234
Walser EES (1986) Recognition of the sow’s voice by neonatal biglets. Behaviour 99:177–188
Wanker R, Fischer J (2001) Intra- and interindividual variation in the contact calls of spectacled parrotlets (Forpus conspicillatus). Behaviour 138:709–726
Waring GH (2003) Horse behavior. William Andrew Publishers, New York
Whiten A, van Schaik CP (2007) The evolution of animal ‘cultures’ and social intelligence. Phil Trans R Soc B 362:603–620
Wiley RH, Hatchwell BJ, Davies NB (1991) Recognition of individual males’ songs by female Dunnocks: a mechanism increasing the number of copulatory partners and reproductive success. Ethology 88:145–153
Wittig RM, Crockford C, Seyfarth RM, Cheney DL (2007) Vocal support in Chacma baboons (Papio hamadryas ursinus). Behav Ecol Sociobiol 61:899–909
Yin S, McCowan B (2004) Barking in domestic dogs: context specificity and individual identification. Anim Behav 68:343–355
Zuberbühler K, Byrne RW (2006) Social cognition. Curr Biol 16:R786–R790
Acknowledgments
We are very grateful to Carole Fureix, Haifa Ben Hajali and Jean-Pierre Richard for their technical assistance. We thank the owners of the horses (Mme M. Hausberger, Lycée Agricole de Ploermel, Lycée Agricole de Laval, Centre d’activités équestres de Brocéliande, Mme M. Michelet, Mme M. Ardoin-Lachaume, Melle A. Rantet, Mme D. Beslay). We also thank Ann Cloarec and Stan Kuczaj for English corrections. The experiments comply with the French current laws.
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Lemasson, A., Boutin, A., Boivin, S. et al. Horse (Equus caballus) whinnies: a source of social information. Anim Cogn 12, 693–704 (2009). https://doi.org/10.1007/s10071-009-0229-9
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DOI: https://doi.org/10.1007/s10071-009-0229-9