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

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Abstract

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.

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References

  • 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

    Article  PubMed  Google Scholar 

  • Allen C (2006) Transitive inference in animals: Reasoning or conditioned associations? In: Hurley S, Nudds M (eds) Rational animals?. Oxford University Press, Oxford, pp 175–186

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Aureli F, de Waal FBM (2000) Natural conflict resolution. University of California Press, Berkeley

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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 

  • Berger J (1986) Wild horses of the Great Basin: social competition and population size. University of Chicago Press, Chicago

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Cheney DL, Seyfarth RM (1990) How monkeys see the world: inside the mind of another species. University of Chicago Press, Chicago

    Google Scholar 

  • Clutton-Brock TH (1974) Primate social organisation and ecology. Nature 250:539–542. doi:10.1038/250539a0

    Article  Google Scholar 

  • 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 91–126

    Google Scholar 

  • Dawkins R (1982) The extended phenotype. WH Freeman, San Francisco

    Google Scholar 

  • de Waal FB, Tyack P (2003) Animal social complexity: intelligence, culture, and individualized societies. Harvard University Press, Cambridge

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Duncan P (1992) Zebras, asses, and horses. Kelvyn Press, Broadview

    Google Scholar 

  • Eisenberg JF, Kleiman DG (1972) Olfactory communication in mammals. Annu Rev Ecol Systemat 3:1–32. doi:10.1146/annurev.es.03.110172.000245

    Article  Google Scholar 

  • Feh C (1999) Alliances and reproductive success in Camargue stallions. Anim Behav 57:705–713. doi:10.1006/anbe.1998.1009

    Article  PubMed  Google Scholar 

  • 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 

  • 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, Cambridge

    Google Scholar 

  • Feist JD, McCullough DR (1976) Behavior patterns and communication in feral horses. Z Tierpsychol 41:337–371

    Article  CAS  PubMed  Google Scholar 

  • 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

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Goldschmidt-Rothschild VB, Tschanz B (1978) Soziale Organisation und Verhalten einer Jungtierherde beim Camargue-Pferd. Z Tierpsychol 46:372–400

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Keiper R (1976) Social organization of feral ponies. Proc Pennsyl Acad Sci 50:69–70

    Google Scholar 

  • Kiley M (1972) The vocalizations of ungulates, their causation and function. Z Tierpsychol 31:171–222

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Klingel H (1972) The behavior of horses (Equidae). Handb Zoolog 8:1–68

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Ligout S, Porter R-H (2006) Social recognition in mammals: mechanisms and sensorial bases. Prod Anim 19:119–133

    Google Scholar 

  • Lindsay FE, Burton FL (1983) Observational study of “urine testing” in the horse and donkey stallion. Equine Vet J 15:330–336

    Article  CAS  PubMed  Google Scholar 

  • Linklater WL (2000) Adaptive explanation in socio-ecology: lessons from the Equidae. Biol Rev Camb Philos Soc 75:1–20

    Article  CAS  PubMed  Google Scholar 

  • Linklater WL, Cameron EZ (2000) Tests for cooperative behaviour between stallions. Anim Behav 60:731–743. doi:10.1006/anbe.2000.1525

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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 24:139–152

    Google Scholar 

  • 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 33:75–83

    Article  CAS  PubMed  Google Scholar 

  • Mandal MK, Bulman-Fleming MB, Tiwari G (2000) Side bias: a neuropsychological perspective. Springer, Netherlands

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • McCullough P, Nelder JA (1989) Generalized linear models. Chapman & Hall, New York

    Google Scholar 

  • McDonnell SM (2003) The equid ethogram: a practical field guide to horse behavior. Eclipse Press, Lexington

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Miller R (1981) Male aggression, dominance and breeding behaviour in Red Desert feral horses. Z Tierpsychol 57:340–351

    Article  Google Scholar 

  • Miller R, Denniston RH (1979) Interband dominance in feral horses. Z Tierpsychol 51:41–47

    Google Scholar 

  • Moehlman PD (2002) Equids: zebras, asses and horses: status survey and conservation action plan. IUCN, Gland

    Google Scholar 

  • Moehlman PD (2005) Endangered wild equids. Sci Am 292:74–81

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Moss CJ, Poole JH (1983) Relationships and social structure in African elephants. In: Hinde RA (ed) Primate social relationships: an integrated approach. Blackwell, Oxford

    Google Scholar 

  • Murphy J, Arkins S (2007) Equine learning behaviour. Behav Process 76:1–13. doi:10.1016/j.beproc.2006.06.009

    Article  Google Scholar 

  • Nelder JA, Wedderburn RWM (1972) Generalized linear models. J R Stat Soc A 135:370–384

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Penn D, Potts WK (1998) Untrained mice discriminate MHC-determined odors. Physiol Behav 64:235–243. doi:10.1016/S0031-9384(98)00052-3

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Pfungst O (1907) Der Kluge Hans. Ein Beitrag zur nichtverbalen Kommunikation. Frankfurter Fachbuchhandlung für Psychologie, Frankfurt am Main

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Pusey AE, Packer C (2003) The ecology of relationships. In: Krebs JR, Davis NB (eds) Behavioural ecology. Blackwell, Oxford, pp 254–283

    Google Scholar 

  • Rios JF, Houpt K (1995) Sexual behavior in geldings. Appl Anim Behav Sci 46:133–135

    Article  Google Scholar 

  • Roberts J, Kacelnik A, Hunter ML (1979) A model of sound interference in relation to acoustic communication. Anim Behav 27:1271–1273

    Article  Google Scholar 

  • 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 282–302

    Google Scholar 

  • Rubenstein DI, Hack MA (1992) Horse signals: the sounds and scents of fury. Evol Ecol 6:254–260. doi:10.1007/BF02214165

    Article  Google Scholar 

  • Rutberg AT (1990) Inter-group transfer in assateague pony mares. Anim Behav 40:945–952. doi:10.1016/S0003-3472(05)80996-0

    Article  Google Scholar 

  • Rutberg AT, Greenberg SA (1990) Dominance, aggression frequencies and modes of aggressive competition in feral pony mares. Anim Behav 40:322–331

    Article  Google Scholar 

  • Rutberg AT, Keiper RR (1993) Proximate causes of natal dispersal in feral ponies: some sex differences. Anim Behav 46:969–975

    Article  Google Scholar 

  • Rydhmer L, Lundström K, Andersson K (2010) Immunocastration reduces aggressive and sexual behaviour in male pigs. Animal 4:965–972. doi:10.1017/S175173111000011X

    Article  CAS  Google Scholar 

  • Saslow CA (2002) Understanding the perceptual world of horses. Appl Anim Behav Sci 78:209–224. doi:10.1016/S0168-1591(02)00092-8

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Sherman PW, Reeve HK, Pfenning DW (2003) Recognition systems. In: Krebs JR, Davis NB (eds) Behavioural ecology. Blackwell, Oxford, pp 69–96

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Stoddart DM (1980) The ecology of vertebrate olfaction. Chapman and Hall, New York, London

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Thor DH, Holloway WR (1982) Social memory of the male laboratory rat. J Comp Physiol Psychol 96:1000–1006

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 21:169–185

    Article  Google Scholar 

  • Timney B, Keil K (1992) Visual acuity in the horse. Vis Res 32:2289–2293. doi:10.1016/0042-6989(92)90092-W

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Trillmich F, Rehling A (2006) Animal communication: parent-offspring. In: Brown Keith (ed) Encyclopedia of language & linguistics. Elsevier, Oxford, pp 284–288

    Google Scholar 

  • Tyler SJ (1972) The behaviour and social organisation of the new Forest ponies. Anim Behav Monogr 5:85–196

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Waldmann B (1991) Kin recognition in amphibians. In: Hepper P (ed) Kin recognition. Cambridge University Press, Cambridge, pp 162–219

    Google Scholar 

  • Waring GH (1983) Horse behaviour: the behavioural traits and adaptations of domestic and wild horses, including ponies. Noyes, Park Ridge

    Google Scholar 

  • Watts DJ, Strogatz SH (1998) Collective dynamics of ‘small-world’ networks. Nature 393:440–442. doi:10.1038/30918

    Google Scholar 

  • Wilson OE (1975) Sociobiology: the new synthesis. Belknap Press, Cambridge

    Google Scholar 

Download references

Acknowledgments

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.

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    Konstanze Krueger & Birgit Flauger

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Krueger, K., Flauger, B. Olfactory recognition of individual competitors by means of faeces in horse (Equus caballus). Anim Cogn 14, 245–257 (2011). https://doi.org/10.1007/s10071-010-0358-1

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