Skip to main content
Log in

Early-life object exposure with a habituated mother reduces fear reactions in foals

  • Original Paper
  • Published:
Animal Cognition Aims and scope Submit manuscript

Abstract

Fear reactions in horses are a major cause of horse–human accidents, and identification of effective pathways for reduction in fearfulness can help decreasing the frequency of accidents. For a young mammal, the mother is one of the most salient aspects of its environment, and she can have a strong influence on her offspring’s behaviour. This study investigated whether fearfulness in foals can be reduced through weekly exposure to usually frightening objects with a habituated mother during the first 8 weeks of life. Prior to foaling, mares (N = 22) were habituated to five initially fear-eliciting situations, including exposure to novel stationary and moving objects. At birth, the foals were randomly assigned to either a Demonstration group (N = 11) or a Control group (N = 11). Demonstration mares demonstrated habituation towards the objects to their foals once per week in weeks 1–8 post-partum. Control mares were inside the empty test arena with their foals for the same amount of time. The foals were tested at 8 weeks and 5 months of age in four standardised fear tests. Demonstration foals showed significantly reduced fear responses (behaviour and heart rate) and increased exploratory behaviour at both 8 weeks and 5 months of age. The effect was likely achieved through a combination of maternal transmission and individual learning. It is concluded that fearfulness in foals may be reduced through exposure to frightening objects together with their habituated mother during the first 8 weeks of life.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Ahrendt LP, Christensen JW, Ladewig J (2012) The ability of horses to learn an instrumental task through social observation. Appl Anim Behav SciPLoS One 139:105–113

    Article  Google Scholar 

  • Ball JE, Ball CG, Mulloy RH, Datta I, Kirkpatrick AW (2009) Ten years of major equestrian injury: are we addressing functional outcomes? J Trauma Manag Outcomes 3:2

    Article  PubMed  PubMed Central  Google Scholar 

  • Bender CE, Herzing DL, Bjorklund DF (2009) Evidence of teaching in Atlantic spotted dolphins (Stenella frontalis) by mother dolphins foraging in the presence of their calves. Anim Cogn 12:43–53

    Article  PubMed  Google Scholar 

  • Bruchey AK, Jones CE, Monfils M-H (2010) Fear conditioning by-proxy: social transmission of fear during memory retrieval. Behav Brain Res 214:80–84

    Article  PubMed  PubMed Central  Google Scholar 

  • Calatayud F, Coubard S, Belzung C (2004) Emotional reactivity in mice may not be inherited but influenced by parents. Physiol Behav 80:465–474

    Article  PubMed  CAS  Google Scholar 

  • Ceroni D (2007) Support and safety features in preventing foot and ankle injuries in equestrian sports. Int Sportmed J 8:166–178

    Google Scholar 

  • Champagne FA (2011) Maternal imprints and the origins of variation. Horm Behav 60:4–11

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Christensen JW, Malmkvist J, Nielsen BL, Keeling LJ (2008) Effects of a calm companion on fear reactions in naïve test horses. Equine Vet J 40:46–50

    Article  PubMed  CAS  Google Scholar 

  • Christensen JW, Zharkikh T, Chovaux E (2011) Object recognition and generalization during habituation in horses. Appl Anim Behav Sci 129:83–91

    Article  Google Scholar 

  • Crane AL, Ferrari MCO (2015) Minnows trust conspecifics more than themselves when faced with conflicting information about predation risk. Anim Behav 100:184–190

    Article  Google Scholar 

  • Egliston K-A, Rapee RM (2007) Inhibition of fear acquisition in toddlers following positive modelling by their mothers. Behav Res Ther 45:1871–1882

    Article  PubMed  Google Scholar 

  • Francis D, Diorio J, Liu D, Meaney MJ (1999) Nongenomic transmission across generation of maternal behavior and stress responses in the rat. Science 286:1155–1158

    Article  PubMed  CAS  Google Scholar 

  • Golkar A, Castro V, Olsson A (2015) Social learning of fear and safety is determined by the demonstrator’s racial group. Biol Lett 11:20140817

    Article  PubMed  PubMed Central  Google Scholar 

  • Griffin AS (2004) Social learning about predators: a review and prospectus. Learn Behav 32:131–140

    Article  PubMed  CAS  Google Scholar 

  • Gudsnuk KMA, Champagne FA (2011) Epigenetic effects of early developmental experiences. Clin Perinatol 38:703–717

    Article  PubMed  Google Scholar 

  • Guzmán YF, Tronson NC, Guedea A, Huh KH, Gao C, Radulovic J (2009) Social modeling of conditioned fear in mice by non-fearful conspecifics. Behav Brain Res 201:173–178

    Article  PubMed  PubMed Central  Google Scholar 

  • Hawson L, McLean A, McGreevy P (2010) The roles of equine ethology and applied learning theory in horse-related human injuries. J Vet Behav 5:324–338

    Article  Google Scholar 

  • Hemmi JM, Merkle T (2009) High stimulus specificity characterizes anti-predator habituation under natural conditions. Proc R Soc B-Biol Sci 276:4381–4388

    Article  Google Scholar 

  • Henry S, Hemery D, Richard MA, Hausberger M (2005) Human-mare relationships and behaviour of foals towards human. Appl Anim Behav Sci 93:341–362

    Article  Google Scholar 

  • Henry S, Briefer S, Richard-Yris M-A, Hausberger M (2007) Are 6-months-old foals sensitive to dam’s influence? Dev Psychobiol 49:514–521

    Article  PubMed  CAS  Google Scholar 

  • Jones CE, Riha PD, Gore AC, Monfils M-H (2014) Social transmission of Pavlovian fear: fear conditioning by-proxy in related female rats. Anim Cogn 17:827–834

    Article  PubMed  PubMed Central  Google Scholar 

  • Kavaliers M, Colwell DD, Choleris E (2005) Kinship, familiarity and social status modulate social learning about ‘micropredators’ (biting flies) in deer mice. Behav Ecol Sociobiol 58:60–71

    Article  Google Scholar 

  • Keeling LJ, Blomberg A, Ladewig J (1999) Horse-riding accidents: when the human-animal relationship goes wrong! In: Proc 33rd Int Congr of the ISAE, Lillehammer, Norway:86

  • Ladewig J, Søndergaard E, Christensen JW (2005) Ontogeny: preparing the young horse for its adult life. In: Mills D and McDonnell S (eds) The domestic horse. Cambridge, UK, pp 139-149

  • Laland KN (2004) Social learning strategies. Learn Behav 32:4–14

    Article  PubMed  Google Scholar 

  • Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619640

    Article  Google Scholar 

  • Lindberg AC, Kelland A, Nicol CJ (1999) Effects of observational learning on acquisition of an operant response in horses. Appl Anim Behav Sci 61:187–199

    Article  Google Scholar 

  • Lonsdorf EV (2006) What is the role of mothers in the acquisition of termite-fishing behaviors in wild chimpanzees (Pan troglodytes schweinfurthii)? Anim Cogn 9:36–46

    Article  PubMed  Google Scholar 

  • Maloney RF, McLean IG (1995) Historical and experimental learned predator recognition in free-living New-Zealand Robins. Anim Behav 50:1193–1201

    Article  Google Scholar 

  • Mateo JM (2014) Development, maternal effects, and behavioral plasticity. Integr Comp Biol 54:841–849

    Article  PubMed  Google Scholar 

  • Mathis A, Chivers DP, Smith RJF (1996) Cultural transmission of predator recognition in fishes: intraspecific and interspecific learning. Anim Behav 51:185–201

    Article  Google Scholar 

  • McElreath R, Strimling P (2008) When natural selection favors imitation of parents. Curr Anthropol 49:307–316

    Article  Google Scholar 

  • Meaney MJ (2001) Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu Rev Neurosci 24:1161–1192

    Article  PubMed  CAS  Google Scholar 

  • Mineka S, Cook M (1986) Immunization against the observational conditioning of snake fear in rhesus monkeys. J Abnorm Psychol 95:307–318

    Article  PubMed  CAS  Google Scholar 

  • Mineka S, Davidson M, Cook M, Keir R (1984) Observational conditioning of snake fear in rhesus monkeys. J Abnorm Psychol 93:355–372

    Article  PubMed  CAS  Google Scholar 

  • Pittet F, Houdelier C, Le Bot O, Leterrier C, Lumineau S (2014) Fearfulness affects quail maternal care and subsequent offspring development. PLoS ONE 9:e102800

    Article  PubMed  PubMed Central  Google Scholar 

  • Rørvang MV, Ahrendt LP, Christensen JW (2015) A trained demonstrator has a calming effect on naïve horses when crossing a novel surface. In press: doi:10.1016/j.applanim.2015.08.008

  • Shettleworth SJ (2010) Cognition, evolution, and behavior, 2nd edn. Oxford University Press, Oxford, pp 466–506

    Google Scholar 

Download references

Acknowledgments

The author would like to thank the studs and horse owners for participating in this study; Nanna Lysemose Frederiksen and Kristina Leth, for practical help with the experiments; Jens Malmkvist, Aarhus University, for comments on the manuscript. This study was funded by The Independent Research Council | Technology and Production, grant no. 0602-01907B.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Janne Winther Christensen.

Ethics declarations

Conflicts of interest

The author reports no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Christensen, J.W. Early-life object exposure with a habituated mother reduces fear reactions in foals. Anim Cogn 19, 171–179 (2016). https://doi.org/10.1007/s10071-015-0924-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10071-015-0924-7

Keywords

Navigation