How do we bond to one another? While in some species, like humans, physical contact plays a role in the process of attachment, it has been suggested that tactile contact's value may greatly differ according to the species considered. Nevertheless, grooming is often considered as a pleasurable experience for domestic animals, even though scientific data is lacking. On another hand, food seems to be involved in the creation of most relationships in a variety of species.
In this study, we used the horse training context to test the effects of food versus grooming during repeated human-horse interactions. The results reveal that food certainly holds a key role in the attachment process, while tactile contact was here clearly insufficient for bonding to occur.
Citation: Sankey C, Henry S, Górecka-Bruzda A, Richard-Yris M-A, Hausberger M (2010) The Way to a Man's Heart Is through His Stomach: What about Horses? PLoS ONE5(11): e15446. https://doi.org/10.1371/journal.pone.0015446
Editor: Georges Chapouthier, Université Pierre et Marie Curie, France
Received: August 13, 2010; Accepted: September 21, 2010; Published: November 15, 2010
Copyright: © 2010 Sankey et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: Funding was provided by Comité d'Orientation Scientifique et Technique (COST, Les Haras Nationaux, http://www.haras-nationaux.fr/portail/) and Région Bretagne (http://www.bretagne.fr/internet/jcms/j_6/accueil). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
How do we bond to each other? What is it that leads to the process of attachment? In psychology, bonding is defined as the process of development of a close, interpersonal relationship . Bonding typically refers to the process of attachment that develops between romantic partners, close friends or parents and children, but has also been used for human-animal relationships . There is evidence that oxytocin and vasopressin hormones are involved in the bonding process and in other forms of prosocial and reproductive behaviour . Of all bonds, the maternal (mother-infant) bond is one of the strongest, in which suckling (i.e. breastfeeding in humans) has been reported to have a fostering role , . Animal research has shown that the endocrine response to suckling (oxytocin release) plays an essential role in maternal bonding by promoting maternal care-giving behavior . Thus one of the strongest bonds in the animal kingdom is, at least partly, a feeding bond. Interestingly, the detachment in the feeding bond goes together with a detachment in the affectionate bond . More generally, food sharing has been described as a reciprocal act of physical affiliation  and an essential component for the development of pair bond . Food calls are another example of how food holds a prime position in the formation and maintenance of close relationships . Don't we also say that little gifts keep friendship warm? Is there a better little gift than a box of sweets or chocolates to make a lover's heart melt or fill a grandmother with joy?
However, inter-individual bonding is often described in terms of social interactions and physical contacts. For this may well reflect real bonding in some species (e.g. in humans: , in cats: ), the value of tactile contact may differ according to the species considered. The same questioning arises when considering human-animal relationships. Even though it is clear that the taming process can be achieved by positive association conditioning: humans being the providers of food and water for domestic animals, they become secondarily associated with those positive stimuli , many still use diverse forms of tactile contact (e.g. stroking, grooming) to initiate bonding. While for the domestic dog, the human presence itself may be rewarding , more precocial species seem to have a less positive perception of human contact . Nevertheless, grooming is often believed to be and used as a primary reinforcement, partly because it has been shown to induce a decrease in the groomee's heart rate , . Here, we investigated whether grooming could be used to promote bonding and facilitate learning, by comparing it to a food-reward that has proven efficient for both , .
Materials and Methods
Experiments complied with the current French and Polish laws related to animal experimentation and were in accordance to the European directive 86/609/CEE. This experiment only included behavioural observations, routine training and non-invasive contacts with the horses (giving carrots or scratching the withers) which did not require the approval of an ethics committee. Animal husbandry and care were under management of the staff of the research station in Popielno.
Study subjects were 20 Konik horses, a primitive breed originating directly from the wild Tarpan horse . Subjects were reared under either conventional domestic conditions (N = 12) or with their respective families in semi-natural conditions in a 1600 ha forest reserve (N = 8). Forest-reared youngstock was caught and put together with their stabled peers at about 10 months. All weanlings were then kept together in multi-age groups, where they were able to express their natural behavioural repertoire in which grooming the withers is considered to play a socio-positive role . Horses were aged one to two years old at the time of the experiment and housed in loose stables. No additional contact with humans took place, except for daily tethering for feeding. Horses were randomly allocated to one of two training groups:
- food-reward group (FR: N = 10): the experimenter hand-gave a small piece of carrot to the horse when it responded correctly to her command.
- grooming-reward group (GR: N = 10): the experimenter vigorously scratched the horse's withers three times when it responded correctly to her command.
Subjects underwent a training program to learn to remain immobile in response to a vocal command: “reste!”, for an increasing duration (5 to 60 seconds). Training was performed 5 min per day for 6 days and took place in the horses' home stable, where they were tethered facing the walls and given hay ad libitum. For training, the experimenter led the focal horse to the center of the stable. In order to distract the awaiting horses' attention from the vocal command, a white noise was broadcast via two radios placed each side of the stable, facing the tethered horses. After completion of daily training, they were set free in an adjacent outdoor paddock. The data collected during training included the maximum time step validated (i.e. 3 consecutive successes) each day, as well as the maximum time for which the horse remained immobile.
In addition, we performed a “motionless human test”, commonly used in the literature to assess human-animal relationships , before and after training. During 5 min, horses were free to interact with the person (female) standing in the center of the stable. Data collected included latency to approach her and total time spent at a distance of 0.5 m or less.
Non parametric statistics were used: Mann-Whitney U-tests (MW) to compare groups; Friedman (F) and Wilcoxon (W) tests to evaluate each group's progression. These analyses were conducted using Statistica© 7.1 software (accepted p level at 0.05).
Clear differences occurred both in learning performance and in the relationship to humans according to the type of “reinforcement” used. While on the last day of training almost all horses trained with the food reward had successfully reached the last step and managed to maintain immobility for 1 min, only 4 of the GR group did (NFR = 9/10, NGR = 4/10, Friedman test: P = 0.03; mean step reached on day6: FR±SE = 40±5.7 s, GR±SE = 18±6.1, MW: U = 20, P = 0.02).
FR horses progressed rapidly, especially during the first three days of training: the maximum duration of immobility greatly increased from day1 to day2 (day1±SE = 9±1, day2±SE = 23±3.7, W: t = 0, P = 0.02) and from day2 to day3 (day2±SE = 23±3.7, day3±SE = 42±4.5, W: t = 0, P = 0.03) and reached a mean duration of 55.7±4.3 s on the last day (day3±SE = 42±4.5, day6±SE = 57±3.6 s, n = 10, W: t = 0, P = 0.04). On the contrary, GR horses' progression was limited to the first two days of training (day1±SE = 5±1.3, day2±SE = 15.5±4, W: t = 0, P = 0.02) after what they stagnated (day2±SE = 15.5±4, day6±SE = 31.5±8.9, W: P = 0.08; fig. 1). FR horses almost always managed to maintain immobility longer than GR horses in response to the order (fig. 1).
Friedman tests: P<0.001, Mann-Whitney U-test, *P<0.05.
More interesting is that while FR training had a positive impact on the relationship (shorter latency to approach the human: before±SE = 235.6±32.7, after±SE = 78.8±37.7 s, n = 10, W: t = 3, P = 0.02, more time spent near her, before±SE = 16.8±9.4, after±SE = 117.7±30.5 s, W: n = 10, t = 1, P = 0.01, after than before training), the grooming procedure had none (latency to approach: before±SE = 202.8±40.9, after±SE = 211.4±37.5 s, P>0.1, time spent near : before±SE = 28±11.6, after±SE = 44±21.3 s, P>0.1), showing that in fact it is not a proper reinforcement. Secondly, while no difference in the horses' relation to humans was observed between groups before training, FR horses approached sooner than GR horses after training (MW, U = 15, P = 0.007), and also spent more time near (MW, U = 23.5, P = 0.04) (fig. 2).
Using food rewards had beneficial effects on horses' attachment to humans and facilitated learning, whereas the tactile contact was clearly not perceived sufficiently positively, neither for bonding to occur, nor for enhancing learning.
Food-rewarded animals learned the immobility task faster than grooming-rewarded animals. In fact, the performance of the latter on the sixth day of training was very close to that found in control horses trained to the same task in a previous study (28.7±3.7 s, ). Grooming the withers therefore does not appear to be an efficient reinforcement for horses. The positive value of human tactile contact sometimes described may in fact be acquired through association with other primary positive reinforcements such as food , , and should therefore be qualified of secondary reinforcement. Since Skinner's pioneering work , , food reinforcement has become one of the main incentives in conditioning procedures . For example, scientists have obtained considerable success in training primates to cooperate during blood sample collection  or during various other handling or veterinary procedures –. Food rewards have been successfully used in a variety of conditioning paradigms and with a variety of species (e.g. in rats , dogs  or rhinoceros ).
Nevertheless, because we, humans, are sensitive to tactile stimulations , , we often assume that stroking or other forms of gentling animals have positive effects. This may indeed be the case for some species, but this study clearly demonstrates that interspecies differences are to be expected: the results suggest that human tactile contact, even when imitating intraspecific natural interactions, is not necessarily perceived positively and is surely not sufficient to create attachment . In horses, physical contact is very restricted through occasional licking of the young by its dam and later mutual grooming, it only represents 2–3% of their time-budget  and is often restricted to specific body regions . Studies have reported that grooming at the withers, whether performed by a conspecific or a human handler induced a decrease in horses' heart rate , . However grooming was performed for a much longer duration (∼3 min) and a decrease in heart rate does not mean that it is perceived sufficiently positively to be considered as reinforcement and thus promote learning or bonding.
Moreover, the few and short food mediated interactions had a major positive effect on horse-human attachment: horses trained with a food reward approached sooner and were closer to humans. Proximities between horses are generally used to evaluate individual preferences and affinities . Thus, food appears to be one of the keys in the bonding process , . There is an idiomatic expression that says: “the way to a man's heart is through his stomach”. It seems that this may not only apply to humans, but could indeed be the case for many species, amongst which horses.
The authors wish to thank Professor Jaworski and the staff at the Research Station for Ecological Agriculture and Preservation of Animal Breeding, Popielno, Poland, where the study was performed.
Conceived and designed the experiments: CS MH MARH SH. Performed the experiments: CS. Analyzed the data: CS. Contributed reagents/materials/analysis tools: CS AGB. Wrote the paper: CS.
- 1. Bowlby J (2005) The making and breaking of affectional bonds. Chapter 4: Effects on behavior of disruption of an affectionnal bond. Routledge classics. J. Bowlby2005The making and breaking of affectional bonds. Chapter 4: Effects on behavior of disruption of an affectionnal bond.Routledge classics
- 2. Beck A, Katcher A (2003) Future Directions in Human-Animal Bond Research. Am Behav Sci 47: 79–93.A. BeckA. Katcher2003Future Directions in Human-Animal Bond Research.Am Behav Sci477993
- 3. Donaldson Z, Young L (2008) Oxytocin, vasopressin, and the neurogenetics of sociality. Sci 322: 900–904.Z. DonaldsonL. Young2008Oxytocin, vasopressin, and the neurogenetics of sociality.Sci322900904
- 4. Hausberger M, Henry S, Larose C, Richard-Yris M-A (2007) First Suckling: A Crucial Event for Mother–Young Attachment? An Experimental Study in Horses (Equus caballus). J Comp Psy 121(1): 109–112.M. HausbergerS. HenryC. LaroseM-A Richard-Yris2007First Suckling: A Crucial Event for Mother–Young Attachment? An Experimental Study in Horses (Equus caballus).J Comp Psy1211109112
- 5. Jansen J, deWeerth C, Riksen-Walraven M (2008) Breastfeeding and the mother-infant relationship – A review. Dev Rev 28: 503–521.J. JansenC. deWeerthM. Riksen-Walraven2008Breastfeeding and the mother-infant relationship – A review.Dev Rev28503521
- 6. Uvnäs-Moberg K (1998) Oxytocin may mediate the benefits of positive social interaction and emotions. Psychoneuroendocrino 23: 819–835.K. Uvnäs-Moberg1998Oxytocin may mediate the benefits of positive social interaction and emotions.Psychoneuroendocrino23819835
- 7. Henry S, Briefer S, Richard-Yris M-A, Hausberger M (2007) Are 6-month-old foals sensitive to dam's influence? Dev Psychobiol 49: 514–521.S. HenryS. BrieferM-A Richard-YrisM. Hausberger2007Are 6-month-old foals sensitive to dam's influence?Dev Psychobiol49514521
- 8. Emery N, Seed A, von Bayern A, Clayton N (2007) Cognitive adaptations of social bonding in birds. Phil Trans R Soc B29 vol.362 no.1480: 489–505.N. EmeryA. SeedA. von BayernN. Clayton2007Cognitive adaptations of social bonding in birds.Phil Trans R Soc B29vol.362 no.1480489505
- 9. deKort S, Emery N, Clayton N (2006) Food sharing in jackdaws, Corvus monedula: what, why and with whom? Anim Behav 72(2): 297–304.S. deKortN. EmeryN. Clayton2006Food sharing in jackdaws, Corvus monedula: what, why and with whom?Anim Behav722297304
- 10. Wauters A-M, Richard-Yris M-A (2003) Maternal food calling in domestic hens: influence of feeding context. Comptes rendus Biologies 326(7): 677–686.A-M WautersM-A Richard-Yris2003Maternal food calling in domestic hens: influence of feeding context.Comptes rendus Biologies3267677686
- 11. Ditzen B, Neumann I, Bodenmann G, von Dawans B, Turner R, et al. (2007) Effects of different kinds of couple interaction on cortisol and heart rate responses to stress in women. Psychoneuroendocrino 32: 565–574.B. DitzenI. NeumannG. BodenmannB. von DawansR. Turner2007Effects of different kinds of couple interaction on cortisol and heart rate responses to stress in women.Psychoneuroendocrino32565574
- 12. Lowe S, Bradshaw J (2001) Ontogeny of individuality in the domestic cat in the home environment. Anim Behav 61: 231–237.S. LoweJ. Bradshaw2001Ontogeny of individuality in the domestic cat in the home environment.Anim Behav61231237
- 13. Price E (1999) Behavioral development in animals undergoing domestication. Appl Anim Behav Sci 65: 245–271.E. Price1999Behavioral development in animals undergoing domestication.Appl Anim Behav Sci65245271
- 14. Henry S, Richard-Yris M-A, Hausberger M (2006) Influence of Various Early Human–Foal Interferences on Subsequent Human–Foal Relationship. Dev Psychobiol 48: 712–718.S. HenryM-A Richard-YrisM. Hausberger2006Influence of Various Early Human–Foal Interferences on Subsequent Human–Foal Relationship.Dev Psychobiol48712718
- 15. Feh C, deMazières J (1993) Grooming at a preferred site reduces heart rate in horses. Anim Behav 46: 1191–1194.C. FehJ. deMazières1993Grooming at a preferred site reduces heart rate in horses.Anim Behav4611911194
- 16. Normando S, Haverbeke A, Meers L, Ödberg F, Ibanez Talegon M, et al. (2003) Effect of manual imitation of grooming on riding horses' heart rate in different environmental situations. Vet Res Com 27: suppl615–617.S. NormandoA. HaverbekeL. MeersF. ÖdbergM. Ibanez Talegon2003Effect of manual imitation of grooming on riding horses' heart rate in different environmental situations.Vet Res Com27suppl615617
- 17. Sankey C, Richard-Yris M-A, Leroy H, Henry S, Hausberger M (2010a) Positive interactions lead to lasting positive memories in horses, Equus caballus. Anim Behav 79: 869–875.C. SankeyM-A Richard-YrisH. LeroyS. HenryM. Hausberger2010aPositive interactions lead to lasting positive memories in horses, Equus caballus.Anim Behav79869875
- 18. Sankey C, Richard-Yris M-A, Henry S, Fureix C, Nassur F, et al. (2010b) Reinforcement as a mediator of the perception of humans by horses (Equus caballus). Anim Cogn 13: 753–764.C. SankeyM-A Richard-YrisS. HenryC. FureixF. Nassur2010bReinforcement as a mediator of the perception of humans by horses (Equus caballus).Anim Cogn13753764
- 19. Jezierski T, Jaworski Z, Górecka A (1999) Effects of handling on behaviour and heart rate in Könik horses: Comparison of stable and forest reared youngstock. Appl Anim Behav Sci 62: 1–11.T. JezierskiZ. JaworskiA. Górecka1999Effects of handling on behaviour and heart rate in Könik horses: Comparison of stable and forest reared youngstock.Appl Anim Behav Sci62111
- 20. Feh C, Mills D, McDonnell S (2005) Relationship and communication in socially natural horse herds. The Domestic Horse. Cambridge: Cambridge University Press. C. FehD. MillsS. McDonnell2005Relationship and communication in socially natural horse herds.The Domestic HorseCambridgeCambridge University PressIn:.
- 21. Hausberger M, Roche H, Henry S, Visser E (2008) A review of the human–horse relationship. Appl Anim Behav Sci 109: 1–24.M. HausbergerH. RocheS. HenryE. Visser2008A review of the human–horse relationship.Appl Anim Behav Sci109124
- 22. Tallet C, Veissier I, Boivin X (2005) Human contact and feeding as rewards for the lamb's affinity to their stockperson. Appl Anim Behav Sci 94: 59–73.C. TalletI. VeissierX. Boivin2005Human contact and feeding as rewards for the lamb's affinity to their stockperson.Appl Anim Behav Sci945973
- 23. Skinner BF (1938) The behaviour of organisms. New-York: Appleton-Century-Crofts. BF Skinner1938The behaviour of organismsNew-YorkAppleton-Century-Crofts
- 24. Skinner BF (1981) Selection by consequences. Science 213: 501–504.BF Skinner1981Selection by consequences.Science213501504
- 25. Kelleher RT, Gollub LR (1962) A review of positive conditioned reinforcement. J Exp Anal Behav 5: 543–597.RT KelleherLR Gollub1962A review of positive conditioned reinforcement.J Exp Anal Behav5543597
- 26. Reinhardt V (1991) Training adult male rhesus monkeys to actively cooperate during in-homecage venipuncture. Anim Tech 42: 11–17.V. Reinhardt1991Training adult male rhesus monkeys to actively cooperate during in-homecage venipuncture.Anim Tech421117
- 27. Laule GE, Bloomsmith MA, Scapiro SJ (2003) The use of positive reinforcement training techniques to enhance the care, management and welfare of primates in the laboratory. J Appl Anim Wel Sci 6(3): 163–173.GE LauleMA BloomsmithSJ Scapiro2003The use of positive reinforcement training techniques to enhance the care, management and welfare of primates in the laboratory.J Appl Anim Wel Sci63163173
- 28. McKinley J, Buchanan-Smith HM, Basset L (2003) Training common marmosets (Callithrix jacchus) to cooperate during routine laboratory procedures: ease of training and time investment. J Appl Anim Wel Sci 6(3): 209–220.J. McKinleyHM Buchanan-SmithL. Basset2003Training common marmosets (Callithrix jacchus) to cooperate during routine laboratory procedures: ease of training and time investment.J Appl Anim Wel Sci63209220
- 29. Prescott MJ, Buchanan-Smith HM (2003) Training non-human primates using positive reinforcement techniques. J Appl Anim Wel Sci 6(3): 157–16130.MJ PrescottHM Buchanan-Smith2003Training non-human primates using positive reinforcement techniques.J Appl Anim Wel Sci6315716130
- 30. Cloutier S, Newberry RC (2008) Use of a conditioning technique to reduce stress associated with repeated intra-peritoneal injections in laboratory rats. Appl Anim Behav Sci 112: 158–173.S. CloutierRC Newberry2008Use of a conditioning technique to reduce stress associated with repeated intra-peritoneal injections in laboratory rats.Appl Anim Behav Sci112158173
- 31. Yin S, Fernandez EJ, Pagan S, Richardson SL, Synder G (2008) Efficacy of a remote-controlled, positive-reinforcement, dog-training system for modifying problem behaviors exhibited when people arrive at the door. Appl Anim Behav Sci 113: 123–138.S. YinEJ FernandezS. PaganSL RichardsonG. Synder2008Efficacy of a remote-controlled, positive-reinforcement, dog-training system for modifying problem behaviors exhibited when people arrive at the door.Appl Anim Behav Sci113123138
- 32. Holden MD, Gregory J, Watkins V, Radford L (2006) Operant conditioning programme for White rhinoceros and Indian or Greater one-horned Asian rhinoceros. Int Zoo Year Book 40: 144–149.MD HoldenJ. GregoryV. WatkinsL. Radford2006Operant conditioning programme for White rhinoceros and Indian or Greater one-horned Asian rhinoceros.Int Zoo Year Book40144149
- 33. Barnard K, Brazelton T (1990) Touch: The foundation of experience. Madison: International Universities Press Inc.. K. BarnardT. Brazelton1990Touch: The foundation of experienceMadisonInternational Universities Press Inc.
- 34. Boyd L, Carbonaro D, Houpt K (1988) The 24-hour time-budget of Przewalski horses. Appl Anim Behav Sci 21: 5–17.L. BoydD. CarbonaroK. Houpt1988The 24-hour time-budget of Przewalski horses.Appl Anim Behav Sci21517