Animal Cognition

, Volume 14, Issue 2, pp 245–257 | Cite as

Olfactory recognition of individual competitors by means of faeces in horse (Equus caballus)

  • Konstanze KruegerEmail author
  • Birgit Flauger
Original Paper


Living in complex social systems requires perceptual and cognitive capacities for the recognition of group membership and individual competitors. Olfaction is one means by which this can be achieved. Many animals can identify individual proteins in urine, skin secretions, or saliva by scent. Additionally, marking behaviour in several mammals and especially in horses indicates the importance of sniffing conspecifics’ faeces for olfactory recognition. To test this hypothesis, we conducted two separate experiments: Experiment 1 addressed the question of whether horses can recognise the group membership of other horses by sniffing their faeces. The horses were presented with four faecal samples: (1) their own, (2) those of other members of their own group, (3) those of unfamiliar mares, and (4) those of unfamiliar geldings. Experiment two was designed to assess whether horses can identify the group member from whom a faecal sample came. Here, we presented two groups of horses with faecal samples from their group mates in random distribution. As controls, soil heaps and sheep faecal samples were used. In experiment one, horses distinguished their own from their conspecifics’ faeces, but did not differentiate between familiarity and sex. In experiment two, the horses from both groups paid most attention to the faeces of the horses from which they received the highest amount of aggressive behaviours. We therefore suggest that horses of both sexes can distinguish individual competitors among their group mates by the smell of their faeces.


Equids Faecal samples Horse Olfaction Sociality 



We wish to thank Katherine Albro Houpt for discussions on horses’ dominance relationships, Christine Nicol for discussing the scientific background, Juergen Heinze and Bernd Kramer for helpful suggestions, Elisabeth D’Antoni and Kate Farmer for language corrections, Knut Krüger for the analysis in “R statistical environment” and all the owners of the horses who allowed us to test their horses and even helped with the tests. The study was supported by an HWP II grant of the University of Regensburg, an Excellence grant of the Bavarian Government and a habilitation grant of the Dr. Peter Deubner Stiftung. We declare that the experiments comply with the current laws of the country in which they were performed.


  1. Acuna BD, Sanes JN, Donoghue JP (2002) Cognitive mechanisms of transitive inference. Exp Brain Res 146:1–10. doi: 10.1007/s00221-002-1092-y CrossRefPubMedGoogle Scholar
  2. Allen C (2006) Transitive inference in animals: Reasoning or conditioned associations? In: Hurley S, Nudds M (eds) Rational animals?. Oxford University Press, Oxford, pp 175–186Google Scholar
  3. Arakawa H, Arakawa K, Blanchard DC, Blanchard RJ (2008) A new test paradigm for social recognition evidenced by urinary scent marking behavior in C57BL/6 J mice. Behav Brain Res 190:97–104. doi: 10.1016/j.bbr.2008.02.009 CrossRefPubMedGoogle Scholar
  4. Aureli F, de Waal FBM (2000) Natural conflict resolution. University of California Press, BerkeleyGoogle Scholar
  5. Basile M, Boivin S, Boutin A, Blois-Heulin C, Hausberger M, Lemasson A (2009) Socially dependent auditory laterality in domestic horses (Equus caballus). Anim Cogn 12:611–619. doi: 10.1007/s10071-009-0220-5 CrossRefPubMedGoogle Scholar
  6. Bates LA, Sayialel KN, Njiraini NW, Poole JH, Moss CJ, Byrne RW (2008) African elephants have expectations about the locations of out-of-sight family members. Biol Lett 4:34–36. doi: 10.1098/rsbl.2007.0529 CrossRefPubMedGoogle Scholar
  7. Berger J (1977) Organizational systems and dominance in feral horses in the Grand Canyon. Behav Ecol Sociobiol 2:131–146. doi: 10.1007/BF00361898 Google Scholar
  8. Berger J (1986) Wild horses of the Great Basin: social competition and population size. University of Chicago Press, ChicagoGoogle Scholar
  9. Brennan PA (2004) The nose knows who’s who: chemosensory individuality and mate recognition in mice. Horm Behav 46:231–240. doi: 10.4141/A00-068 CrossRefPubMedGoogle Scholar
  10. Brennan PA, Kendrick KM (2006) Mammalian social odours: attraction and individual recognition. Phil Trans Biol Sci 361:2061–2078. doi: 10.1098/rstb.2006.1931 CrossRefGoogle Scholar
  11. Cheney DL, Seyfarth RM (1990) How monkeys see the world: inside the mind of another species. University of Chicago Press, ChicagoGoogle Scholar
  12. Clutton-Brock TH (1974) Primate social organisation and ecology. Nature 250:539–542. doi: 10.1038/250539a0 CrossRefGoogle Scholar
  13. Connor RC, Wells RS, Mann J, Read AJ (2000) The bottlenose dolphin: social relationships in a fission-fusion society. In: Mann J, Connor RC, Tyack PL, Whitehead H (eds) Cetacean societies: field studies of dolphins and whales. University of Chicago Press, Chicago, pp 91–126Google Scholar
  14. Dawkins R (1982) The extended phenotype. WH Freeman, San FranciscoGoogle Scholar
  15. de Waal FB, Tyack P (2003) Animal social complexity: intelligence, culture, and individualized societies. Harvard University Press, CambridgeGoogle Scholar
  16. Dreier S, van Zweden JS, D’Ettorre P (2007) Long-term memory of individual identity in ant queens. Biol Lett 3:459–462. doi: 10.1098/rsbl.2007.0224 CrossRefPubMedGoogle Scholar
  17. Duncan P (1992) Zebras, asses, and horses. Kelvyn Press, BroadviewGoogle Scholar
  18. Eisenberg JF, Kleiman DG (1972) Olfactory communication in mammals. Annu Rev Ecol Systemat 3:1–32. doi: 10.1146/ CrossRefGoogle Scholar
  19. Feh C (1999) Alliances and reproductive success in Camargue stallions. Anim Behav 57:705–713. doi: 10.1006/anbe.1998.1009 CrossRefPubMedGoogle Scholar
  20. Feh C (2001) Alliances between stallions are more than just multimale groups: reply to Linklater & Cameron (2000). Anim Behav 6:F27–F30. doi: 10.1006/anbe.1998.1009 Google Scholar
  21. Feh C (2005) Relationships and communication in socially natural horse herds. In: Mills DS, McDonnell SM (eds) The domestic horse: the origins, development, and management of its behaviour. Cambridge University Press, CambridgeGoogle Scholar
  22. Feist JD, McCullough DR (1976) Behavior patterns and communication in feral horses. Z Tierpsychol 41:337–371CrossRefPubMedGoogle Scholar
  23. Fischhoff IR, Sundaresan SR, Cordingley J, Larkin HM, Sellier M-J, Rubenstein DI (2007) Social relationships and reproductive state influence leadership roles in movements of plains zebra, Equus burchellii. Anim Behav 73:825–831. doi: 10.1016/j.anbehav.2006.10.012
  24. Flack JC, de Waal FBM, Krakauer DC (2005) Social structure, robustness, and policing cost in a cognitively sophisticated species. Am Nat 165:E126–E139. doi: 10.1086/429277 CrossRefPubMedGoogle Scholar
  25. Franke Stevens E (1988) Contents between bands of feral horses for access to fresh water: the resident wins. Anim Behav 36:1851–1853. doi: 10.1016/S0003-3472(88)80132-5 CrossRefGoogle Scholar
  26. Goldschmidt-Rothschild VB, Tschanz B (1978) Soziale Organisation und Verhalten einer Jungtierherde beim Camargue-Pferd. Z Tierpsychol 46:372–400CrossRefGoogle Scholar
  27. Gosling LM, Roberts SC (2001) Testing ideas about the function of scent marks in territories from spatial patterns. Anim Behav 62:F7–F10. doi: 10.1006/anbe.2001.1802 CrossRefGoogle Scholar
  28. Hemelrijk CK, Wantia J, Gygax L (2005) The construction of dominance order: comparing performance of five methods using an individual-based model. Behaviour 142:1043–1064. doi: 10.1163/156853905774405290 CrossRefGoogle Scholar
  29. Hothersall B, Harris P, Sörtoft L, Nicol C (2010) Discrimination between conspecific odour samples in the horse (Equus caballus). Appl Anim Behav Sci 126:37–44. doi: 10.1016/j.applanim.2010.05.002 CrossRefGoogle Scholar
  30. Howard RW, Blomquist GJ (2005) Ecological, behavioral, and biochemical aspects of insect hydrocarbons. Annu Rev Entomol 50:371–393. doi: 10.1146/annurev.ento.50.071803.130359 CrossRefPubMedGoogle Scholar
  31. Keiper R (1976) Social organization of feral ponies. Proc Pennsyl Acad Sci 50:69–70Google Scholar
  32. Kiley M (1972) The vocalizations of ungulates, their causation and function. Z Tierpsychol 31:171–222CrossRefPubMedGoogle Scholar
  33. Kimura R (2001) Volatile substances in feces, urine and urine-marked feces of feral horses. Can J Anim Sci 81:411–420. doi: 10.4141/A00-068 Google Scholar
  34. King SRB (2002) Home range and habitat use of free-ranging Przewalski horses at Hustai National Park, Mongolia. Appl Anim Behav Sci 78:103–113. doi: 10.1016/S0168-1591(02)00087-4 CrossRefGoogle Scholar
  35. King SRB, Gurnell J (2007) Scent-marking behaviour by stallions: an assessment of function in a reintroduced population of Przewalski horses (Equus ferus przewalskii). J Zool 272:30–36. doi: 10.1111/j.1469-7998.2006.00243.x CrossRefGoogle Scholar
  36. Klingel H (1972) The behavior of horses (Equidae). Handb Zoolog 8:1–68Google Scholar
  37. Krueger K, Heinze J (2008) Horse sense: social status of horses (Equus caballus) affects their likelihood of copying other horses’ behavior. Anim Cogn 11:431–439. doi: 10.1007/s10071-007-0133-0 CrossRefPubMedGoogle Scholar
  38. Krueger K, Flauger B, Farmer K, Maros K (2010) Horses (Equus caballus) use human local enhancement cues and adjust to human attention. Anim Cogn. doi: 10.1007/s10071-010-0352-7
  39. Lemasson A, Boutin A, Boivin S, Blois-Heulin C, Hausberger M (2009) Horse (Equus caballus) whinnies: a source of social information. Anim Cogn 12:693–704. doi: 10.1007/s10071-009-0229-9 CrossRefPubMedGoogle Scholar
  40. Levy F, Keller M, Poindron P (2004) Olfactory regulation of maternal behavior in mammals. Horm Behav 46:284–302. doi: 10.1016/j.yhbeh.2004.02.005 CrossRefPubMedGoogle Scholar
  41. Ligout S, Porter R-H (2006) Social recognition in mammals: mechanisms and sensorial bases. Prod Anim 19:119–133Google Scholar
  42. Lindsay FE, Burton FL (1983) Observational study of “urine testing” in the horse and donkey stallion. Equine Vet J 15:330–336CrossRefPubMedGoogle Scholar
  43. Linklater WL (2000) Adaptive explanation in socio-ecology: lessons from the Equidae. Biol Rev Camb Philos Soc 75:1–20CrossRefPubMedGoogle Scholar
  44. Linklater WL, Cameron EZ (2000) Tests for cooperative behaviour between stallions. Anim Behav 60:731–743. doi: 10.1006/anbe.2000.1525 CrossRefPubMedGoogle Scholar
  45. Linklater WL, Cameron EZ, Minot EO, Stafford KJ (1999) Stallion harassment and the mating system of horses. Anim Behav 58:295–306. doi: 10.1006/anbe.1999.1155 CrossRefPubMedGoogle Scholar
  46. Linklater WL, Cameron EZ, Stafford KJ, Veltman CJ (2000) Social and spatial structure and range use by Kaimanawa wild horses (Equus caballus: Equidae). NZ J Ecol 24:139–152Google Scholar
  47. Malmgren L, Andresen Ø, Dalin A-M (2001) Effect of GnRH immunisation on hormonal levels, sexual behaviour, semen quality and testicular morphology in mature stallions. Equine vet J 33:75–83CrossRefPubMedGoogle Scholar
  48. Mandal MK, Bulman-Fleming MB, Tiwari G (2000) Side bias: a neuropsychological perspective. Springer, NetherlandsGoogle Scholar
  49. Marinier SL, Alexander AJ, Waring GH (1988) Flehmen behaviour in the domestic horse: discrimination of conspecific odours. Appl Anim Behav Sci 19:227–237. doi: 10.1016/0168-1591(88)90003-2 CrossRefGoogle Scholar
  50. Mateo JM (2006) The nature and representation of individual recognition odours in Belding’s ground squirrels. Anim Behav 71:141–154. doi: 10.1016/j.anbehav.2005.04.006 CrossRefGoogle Scholar
  51. McCullough P, Nelder JA (1989) Generalized linear models. Chapman & Hall, New YorkGoogle Scholar
  52. McDonnell SM (2003) The equid ethogram: a practical field guide to horse behavior. Eclipse Press, LexingtonGoogle Scholar
  53. McDonnell SM, Haviland JCS (1995) Agonistic ethogram of the equid bachelor band. Appl Anim Behav Sci 43:147–188. doi: 10.1016/0168-1591(94)00550-X CrossRefGoogle Scholar
  54. Mehlis M, Bakker T, Frommen J (2008) Smells like sib spirit: kin recognition in three-spined sticklebacks (Gasterosteus aculeatus) is mediated by olfactory cues. Anim Cogn 11:643–650. doi: 10.1007/s10071-008-0154-3 CrossRefPubMedGoogle Scholar
  55. Miller R (1981) Male aggression, dominance and breeding behaviour in Red Desert feral horses. Z Tierpsychol 57:340–351CrossRefGoogle Scholar
  56. Miller R, Denniston RH (1979) Interband dominance in feral horses. Z Tierpsychol 51:41–47Google Scholar
  57. Moehlman PD (2002) Equids: zebras, asses and horses: status survey and conservation action plan. IUCN, GlandGoogle Scholar
  58. Moehlman PD (2005) Endangered wild equids. Sci Am 292:74–81CrossRefPubMedGoogle Scholar
  59. Mormède P, Andanson S, Aupérin B, Beerda B, Guémené D, Malmkvist J, Manteca X, Manteuffel G, Prunet P, van Reenen CG, Richard S, Veissier I (2007) Exploration of the hypothalamic-pituitary-adrenal function as a tool to evaluate animal welfare. Physiol Behav 92:317–339. doi: 10.1016/j.physbeh.2006.12.003 CrossRefPubMedGoogle Scholar
  60. Moses SN, Villate C, Ryan JD (2006) An investigation of learning strategy supporting transitive inference performance in humans compared to other species. Neuropsychologia 44:1370–1387. doi: 10.1016/j.neuropsychologia.2006.01.004 CrossRefPubMedGoogle Scholar
  61. Moss CJ, Poole JH (1983) Relationships and social structure in African elephants. In: Hinde RA (ed) Primate social relationships: an integrated approach. Blackwell, OxfordGoogle Scholar
  62. Murphy J, Arkins S (2007) Equine learning behaviour. Behav Process 76:1–13. doi: 10.1016/j.beproc.2006.06.009 CrossRefGoogle Scholar
  63. Nelder JA, Wedderburn RWM (1972) Generalized linear models. J R Stat Soc A 135:370–384CrossRefGoogle Scholar
  64. Nicol CJ (2002) Equine learning: progress and suggestions for future research. Appl Anim Behav Sci 78:193–208. doi: 10.1016/S0168-1591(02)00093-X CrossRefGoogle Scholar
  65. Patris B, Perrier G, Schaal B, Coureaud G (2008) Early development of filial preferences in the rabbit: implications of nursing- and pheromone-induced odour learning? Anim Behav 76:305–314. doi: 10.1016/j.anbehav.2008.01.017 CrossRefGoogle Scholar
  66. Paz-Y-Mino CG, Bond AB, Kamil AC, Balda RP (2004) Pinyon jays use transitive inference to predict social dominance. Nature 430:778–781. doi: 10.1038/nature02723 CrossRefGoogle Scholar
  67. Penn D, Potts WK (1998) Untrained mice discriminate MHC-determined odors. Physiol Behav 64:235–243. doi: 10.1016/S0031-9384(98)00052-3 CrossRefPubMedGoogle Scholar
  68. Pesenti ME, Spinelli S, Bezirard V, Briand L, Pernollet J-C, Tegoni M, Cambillau C (2008) Structural basis of the honey bee PBP pheromone and pH-induced conformational change. J Mol Biol 380:158–169. doi: 10.1016/j.jmb.2008.04.048 CrossRefPubMedGoogle Scholar
  69. Pfungst O (1907) Der Kluge Hans. Ein Beitrag zur nichtverbalen Kommunikation. Frankfurter Fachbuchhandlung für Psychologie, Frankfurt am MainGoogle Scholar
  70. Proops L, McComb K (2010) Attributing attention: the use of human-given cues by domestic horses (Equus caballus). Anim Cogn 13(2):197–205. doi: 10.1007/s10071-009-0257-5 CrossRefPubMedGoogle Scholar
  71. Proops L, McComb K, Reby D (2009) Cross-modal individual recognition in domestic horses (Equus caballus). PNAS 106:947–951. doi: 10.1073/pnas.0809127105 CrossRefPubMedGoogle Scholar
  72. Proops L, Walton M, McComb K (2010) The use of human-given cues by domestic horses, Equus caballus, during an object choice task. Anim Behav 79(6):1205–1209. doi: 0.1016/j.anbehav.2010.02.015 CrossRefGoogle Scholar
  73. Pusey AE, Packer C (2003) The ecology of relationships. In: Krebs JR, Davis NB (eds) Behavioural ecology. Blackwell, Oxford, pp 254–283Google Scholar
  74. Rios JF, Houpt K (1995) Sexual behavior in geldings. Appl Anim Behav Sci 46:133–135CrossRefGoogle Scholar
  75. Roberts J, Kacelnik A, Hunter ML (1979) A model of sound interference in relation to acoustic communication. Anim Behav 27:1271–1273CrossRefGoogle Scholar
  76. Rubenstein DI (1986) Ecology and sociality in horses and zebras. In: Rubenstein DI, Wrangham RW (eds) Ecological aspects of social evolution. Princeton University Press, Princeton, pp 282–302Google Scholar
  77. Rubenstein DI, Hack MA (1992) Horse signals: the sounds and scents of fury. Evol Ecol 6:254–260. doi: 10.1007/BF02214165 CrossRefGoogle Scholar
  78. Rutberg AT (1990) Inter-group transfer in assateague pony mares. Anim Behav 40:945–952. doi: 10.1016/S0003-3472(05)80996-0 CrossRefGoogle Scholar
  79. Rutberg AT, Greenberg SA (1990) Dominance, aggression frequencies and modes of aggressive competition in feral pony mares. Anim Behav 40:322–331CrossRefGoogle Scholar
  80. Rutberg AT, Keiper RR (1993) Proximate causes of natal dispersal in feral ponies: some sex differences. Anim Behav 46:969–975CrossRefGoogle Scholar
  81. Rydhmer L, Lundström K, Andersson K (2010) Immunocastration reduces aggressive and sexual behaviour in male pigs. Animal 4:965–972. doi: 10.1017/S175173111000011X CrossRefGoogle Scholar
  82. Saslow CA (2002) Understanding the perceptual world of horses. Appl Anim Behav Sci 78:209–224. doi: 10.1016/S0168-1591(02)00092-8 CrossRefGoogle Scholar
  83. Scordato ES, Drea CM (2007) Scents and sensibility: information content of olfactory signals in the ringtailed lemur, Lemur catta. Anim Behav 73:301–314. doi: 10.1016/j.anbehav.2006.08.006 CrossRefGoogle Scholar
  84. Sherman PW, Reeve HK, Pfenning DW (2003) Recognition systems. In: Krebs JR, Davis NB (eds) Behavioural ecology. Blackwell, Oxford, pp 69–96Google Scholar
  85. Smith JE, Kolowski JM, Graham KE, Dawes SE, Holekamp KE (2008) Social and ecological determinants of fission-fusion dynamics in the spotted hyaena. Anim Behav 76:619–636. doi: 10.1016/j.anbehav.2008.05.001 CrossRefGoogle Scholar
  86. Stahlbaum CC, Houpt KA (1989) The role of the Flehmen response in the behavioral repertoire of the stallion. Physiol Behav 45:1207–1214. doi: 10.1016/0031-9384(89)90111-X CrossRefPubMedGoogle Scholar
  87. Stoddart DM (1980) The ecology of vertebrate olfaction. Chapman and Hall, New York, LondonGoogle Scholar
  88. Stone SM (2010) Human facial discrimination in horses: can they tell us apart. Anim Cogn 13:51–61. doi: 10.1007/s10071-009-0244-x CrossRefPubMedGoogle Scholar
  89. Thor DH, Holloway WR (1982) Social memory of the male laboratory rat. J Comp Physiol Psychol 96:1000–1006CrossRefGoogle Scholar
  90. Tibbetts EA (2002) Visual signals of individual identity in the wasp Polistes fuscatus. Proc R Soc Lond B Biol Sci 269:1423–1428. doi: 10.1098/rspb.2002.2031 CrossRefGoogle Scholar
  91. Tilson RL, Sweeny KA, Binczik GA, Reindl NJ (1988) Buddies and bullies: social structure of a bachelor group of Przewalski horses. Appl Anim Behav Sci 21:169–185CrossRefGoogle Scholar
  92. Timney B, Keil K (1992) Visual acuity in the horse. Vis Res 32:2289–2293. doi: 10.1016/0042-6989(92)90092-W CrossRefPubMedGoogle Scholar
  93. Treichler FR, Van Tilburg D (1996) Concurrent conditional discrimination tests of transitive inference by macaque monkeys: list linking. J Exp Psychol Anim Behav Process 22:105–117. doi: 10.1037/0097-7403.22.1.105 CrossRefPubMedGoogle Scholar
  94. Trillmich F, Rehling A (2006) Animal communication: parent-offspring. In: Brown Keith (ed) Encyclopedia of language & linguistics. Elsevier, Oxford, pp 284–288Google Scholar
  95. Tyler SJ (1972) The behaviour and social organisation of the new Forest ponies. Anim Behav Monogr 5:85–196Google Scholar
  96. Veissier I, Boissy A, Nowak R, Orgeur P, Poindron P (1998) Ontogeny of social awareness in domestic herbivores. Appl Anim Behav Sci 57:233–245. doi: 10.1016/S0168-1591(98)00099-9 CrossRefGoogle Scholar
  97. Vinke CM, van Deijk R, Houx BB, Schoemaker NJ (2008) The effects of surgical and chemical castration on intermale aggression, sexual behaviour and play behaviour in the male ferret (Mustela putorius furo). Appl Anim Behav Sci 115:104–121. doi: 10.1016/j.applanim.2008.05.003 CrossRefGoogle Scholar
  98. Waldmann B (1991) Kin recognition in amphibians. In: Hepper P (ed) Kin recognition. Cambridge University Press, Cambridge, pp 162–219Google Scholar
  99. Waring GH (1983) Horse behaviour: the behavioural traits and adaptations of domestic and wild horses, including ponies. Noyes, Park RidgeGoogle Scholar
  100. Watts DJ, Strogatz SH (1998) Collective dynamics of ‘small-world’ networks. Nature 393:440–442. doi: 10.1038/30918 Google Scholar
  101. Wilson OE (1975) Sociobiology: the new synthesis. Belknap Press, CambridgeGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  1. 1.Biology IUniversity of RegensburgRegensburgGermany

Personalised recommendations