Analyze Diet
Scientific reports2018; 8(1); 17501; doi: 10.1038/s41598-018-35561-7

Physiological outcomes of calming behaviors support the resilience hypothesis in horses.

Abstract: To manage a stressful stimulus animals react both behaviorally and physiologically to restore the homeostasis. In stable horses, a stressful stimulus can be represented by social separation, riding discomfort or the presence of novel objects in their environment. Although Heart Rate Variability is a common indicator of stress levels in horses, the behavioral mechanisms concurrently occurring under stressful conditions are still unknown. The sudden inflation of a balloon was administered to 33 horses. Video-recording of self-directed behaviors (snore, vacuum chewing, snort, head/body shaking) and monitoring of heart activity (HR and SDRR) were conducted for five minutes before (Pre-test) and after the stimulus administration (Stress-test). During the Stress-test, only snore and vacuum chewing increased and a significant increase was also recorded in both HR and SDRR. Moreover, the snore variation between the two conditions showed a significant correlation with the variation of both HR and SDRR. With the snore acting as stress-releasing behavior to restore basal condition, the homeostasis recovered via the enactment of such behavior could be physiologically expressed by an increasing vagal activity. Hence, the capacity to maintain homeostasis (resilience) could correspond to a prevalence of parasympathetic control on heart activity, intervening when certain behaviors are performed.
Publication Date: 2018-11-30 PubMed ID: 30504840PubMed Central: PMC6269543DOI: 10.1038/s41598-018-35561-7Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
  • Journal Article

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The research explores how horses respond to stress and identifies specific behaviors, like snoring and vacuum chewing, that may facilitate a horse’s ability to regain calmness and physiological balance after a stressful event.

Understanding the Research Topic

  • The main focus of this study is to investigate how horses physiologically react to stress, and how they regain balance, or homeostasis, afterwards. Homeostasis refers to a stable, balanced, or constant condition in the body, maintained by biological processes.
  • The researchers wanted to better understand the specific behaviors horses use to mitigate stress and restore homeostasis.
  • Common stressors for horses can include social separation, discomfort during riding, or exposure to unfamiliar objects. This study introduced a sudden stimulus – the inflation of a balloon – to induce stress.

Methodology

  • The researchers used 33 horses for the experiment. They monitored and recorded the horses’ self-directed behaviors and heart activity for five minutes before and after introducing the stressor. The behaviors observed included snoring, vacuum chewing, snorting, and shaking of the head or body.
  • Heart activity was measured using Heart Rate (HR) and Standard Deviation of RR intervals (SDRR), with the latter being a common indicator of stress levels in horses.

Findings

  • The study found that during the stress test, only snoring and vacuum chewing increased significantly. Additionally, there was a significant increase in both HR and SDRR, indicating elevated stress.
  • The increased frequency of snoring between the pre-test and stress-test was significantly correlated with the variation in HR and SDRR, suggesting that the snoring behavior might be a stress-releasing mechanism for the horses.

Significance of the Findings

  • The researchers suggest that the horse’s ability to stabilize its physiological state after a stressful event could be linked to an increase in parasympathetic control over heart activity. Parasympathetic control is part of the nervous system that generally serves to slow the heart rate and calm the body.
  • Therefore, understanding specific calming behaviors like snoring may provide insights into a horse’s resilience, or the ability to maintain homeostasis under stress.

In summary, this research provides valuable insights into how horses physiologically respond to and mitigate stress, which has implications for horse care and management practices.

Cite This Article

APA
Scopa C, Palagi E, Sighieri C, Baragli P. (2018). Physiological outcomes of calming behaviors support the resilience hypothesis in horses. Sci Rep, 8(1), 17501. https://doi.org/10.1038/s41598-018-35561-7

Publication

ISSN: 2045-2322
NlmUniqueID: 101563288
Country: England
Language: English
Volume: 8
Issue: 1
Pages: 17501
PII: 17501

Researcher Affiliations

Scopa, Chiara
  • Italian National Reference Centre for Animal Assisted Interventions, Istituto Zooprofilattico Sperimentale delle Venezie, Legnaro (Padua), Italy.
Palagi, Elisabetta
  • Unit of Ethology, Department of Biology, University of Pisa, Pisa, Italy.
Sighieri, Claudio
  • Department of Veterinary Sciences, University of Pisa, Pisa, Italy.
Baragli, Paolo
  • Department of Veterinary Sciences, University of Pisa, Pisa, Italy. paolo.baragli@unipi.it.

MeSH Terms

  • Animals
  • Behavior, Animal / physiology
  • Homeostasis
  • Horses / physiology
  • Vital Signs

Conflict of Interest Statement

The authors declare no competing interests.

References

This article includes 67 references
  1. Moberg GP. A model for assessing the impact of behavioral stress on domestic animals.. J Anim Sci 1987 Nov;65(5):1228-35.
    doi: 10.2527/jas1987.6551228xpubmed: 3693149google scholar: lookup
  2. Selye H. The Physiology and Pathology of Exposures to Stress. Acta Medica Publ. Montreal (1950).
  3. Koolhaas JM, Bartolomucci A, Buwalda B, de Boer SF, Flügge G, Korte SM, Meerlo P, Murison R, Olivier B, Palanza P, Richter-Levin G, Sgoifo A, Steimer T, Stiedl O, van Dijk G, Wöhr M, Fuchs E. Stress revisited: a critical evaluation of the stress concept.. Neurosci Biobehav Rev 2011 Apr;35(5):1291-301.
  4. Chrousos GP. Stress and disorders of the stress system.. Nat Rev Endocrinol 2009 Jul;5(7):374-81.
    doi: 10.1038/nrendo.2009.106pubmed: 19488073google scholar: lookup
  5. Lazarus RS. Cognition and motivation in emotion.. Am Psychol 1991 Apr;46(4):352-67.
    doi: 10.1037/0003-066X.46.4.352pubmed: 2048794google scholar: lookup
  6. Dingemanse NJ, Kazem AJ, Réale D, Wright J. Behavioural reaction norms: animal personality meets individual plasticity.. Trends Ecol Evol 2010 Feb;25(2):81-9.
    doi: 10.1016/j.tree.2009.07.013pubmed: 19748700google scholar: lookup
  7. Visser EK, van Reenen CG, van der Werf JT, Schilder MB, Knaap JH, Barneveld A, Blokhuis HJ. Heart rate and heart rate variability during a novel object test and a handling test in young horses.. Physiol Behav 2002 Jun 1;76(2):289-96.
    doi: 10.1016/S0031-9384(02)00698-4pubmed: 12044602google scholar: lookup
  8. Hagan JJ, Bohus B. The effects of endorphins on cardiac responses during an emotional stress.. Physiol Behav 1983 Nov;31(5):607-14.
    doi: 10.1016/0031-9384(83)90272-Xpubmed: 6141580google scholar: lookup
  9. Korte SM, Koolhaas JM, Schuurman T, Traber J, Bohus B. Anxiolytics and stress-induced behavioural and cardiac responses: a study of diazepam and ipsapirone (TVX Q 7821).. Eur J Pharmacol 1990 Apr 25;179(3):393-401.
    doi: 10.1016/0014-2999(90)90180-Epubmed: 1973110google scholar: lookup
  10. Sgoifo A, Koolhaas JM, Musso E, De Boer SF. Different sympathovagal modulation of heart rate during social and nonsocial stress episodes in wild-type rats.. Physiol Behav 1999 Nov;67(5):733-8.
    doi: 10.1016/S0031-9384(99)00134-1pubmed: 10604845google scholar: lookup
  11. von Borell E, Langbein J, Després G, Hansen S, Leterrier C, Marchant J, Marchant-Forde R, Minero M, Mohr E, Prunier A, Valance D, Veissier I. Heart rate variability as a measure of autonomic regulation of cardiac activity for assessing stress and welfare in farm animals -- a review.. Physiol Behav 2007 Oct 22;92(3):293-316.
    doi: 10.1016/j.physbeh.2007.01.007pubmed: 17320122google scholar: lookup
  12. Segerstrom SC, Nes LS. Heart rate variability reflects self-regulatory strength, effort, and fatigue.. Psychol Sci 2007 Mar;18(3):275-81.
  13. Gross JJ. The emerging field of emotion regulation: an integrative review. Rev. Gen Psychol 1998;2(3):271–299.
    doi: 10.1037/1089-2680.2.3.271google scholar: lookup
  14. Appelhans BM, Luecken LJ. Heart rate variability as an index of regulated emotional responding. Rev Gen Psychol 2006;10(3):229–240.
  15. Mendl M, Burman OH, Paul ES. An integrative and functional framework for the study of animal emotion and mood.. Proc Biol Sci 2010 Oct 7;277(1696):2895-904.
    doi: 10.1098/rspb.2010.0303pmc: PMC2982018pubmed: 20685706google scholar: lookup
  16. Alvares GA, Quintana DS, Kemp AH, Van Zwieten A, Balleine BW, Hickie IB, Guastella AJ. Reduced heart rate variability in social anxiety disorder: associations with gender and symptom severity.. PLoS One 2013;8(7):e70468.
  17. Hart J. Association between heart rate variability and manual pulse rate.. J Can Chiropr Assoc 2013 Sep;57(3):243-50.
    pmc: PMC3743650pubmed: 23997250
  18. Lai FC, Chang WL, Jeng C. The relationship between physical activity and heart rate variability in orthotopic heart transplant recipients.. J Clin Nurs 2012 Nov;21(21-22):3235-43.
  19. Liu J, Wei W, Kuang H, Zhao F, Tsien JZ. Changes in heart rate variability are associated with expression of short-term and long-term contextual and cued fear memories.. PLoS One 2013;8(5):e63590.
  20. Stucke D, Ruse MG, Lebelt D. Measuring heart rate variability in horses to investigate the autonomic nervous system activity – Pros and cons of different methods. Appl Anim Behav Sci 2015;166:1–10.
  21. Baragli P, Vitale V, Sighieri C, Lanata A, Palagi E, Reddon AR. Consistency and flexibility in solving spatial tasks: different horses show different cognitive styles.. Sci Rep 2017 Nov 29;7(1):16557.
    doi: 10.1038/s41598-017-16729-zpmc: PMC5707407pubmed: 29185468google scholar: lookup
  22. Schmidt A, Aurich J, Möstl E, Müller J, Aurich C. Changes in cortisol release and heart rate and heart rate variability during the initial training of 3-year-old sport horses.. Horm Behav 2010 Sep;58(4):628-36.
    doi: 10.1016/j.yhbeh.2010.06.011pubmed: 20600048google scholar: lookup
  23. Rietmann TR. Assessment of mental stress in warmblood horses: Heart rate variability in comparison to heart rate and selected behavioural parameters. Appl Anim Behav Sci 2004;88(1-2):121–136.
  24. Fischer CP, Franco LA, Romero LM. Are novel objects perceived as stressful? The effect of novelty on heart rate.. Physiol Behav 2016 Jul 1;161:7-14.
    doi: 10.1016/j.physbeh.2016.04.014pubmed: 27072510google scholar: lookup
  25. Budzyńska M. Stress reactivity and coping in horse adaptation to environment. J. Equine Vet Sci 2014;34(8):935–941.
  26. Boissy A, Manteuffel G, Jensen MB, Moe RO, Spruijt B, Keeling LJ, Winckler C, Forkman B, Dimitrov I, Langbein J, Bakken M, Veissier I, Aubert A. Assessment of positive emotions in animals to improve their welfare.. Physiol Behav 2007 Oct 22;92(3):375-97.
    doi: 10.1016/j.physbeh.2007.02.003pubmed: 17428510google scholar: lookup
  27. Fox E. Emotion Science Cognitive and Neuroscientific Approaches to Understanding Human Emotions. Palgrave Macmillan, 2008.
  28. Borstel KU, Visser EK, Hall C. Indicators of stress in equitation. Appl Anim Behav Sci 2017;190:43–56.
  29. Mason JW. Emotion as reflected in patterns of endocrine integrations. in Emotions - Their parameters and measurement (ed. Levi, L.) 143–181 (Raven, 1975).
  30. De Santis M, Contalbrigo L, Borgi M, Cirulli F, Luzi F, Redaelli V, Stefani A, Toson M, Odore R, Vercelli C, Valle E, Farina L. Equine Assisted Interventions (EAIs): Methodological Considerations for Stress Assessment in Horses.. Vet Sci 2017 Sep 8;4(3).
    doi: 10.3390/vetsci4030044pmc: PMC5644660pubmed: 29056702google scholar: lookup
  31. Waring GH. Horse Behaviour, 2nd ed.. Noyes Publications William Andrew Publishing, 2003.
  32. Lesimple C, Sankey C, Richard MA, Hausberger M. Do horses expect humans to solve their problems?. Front Psychol 2012;3:306.
    doi: 10.3389/fpsyg.2012.00306pmc: PMC3426792pubmed: 22936923google scholar: lookup
  33. Stomp M, Leroux M, Cellier M, Henry S, Lemasson A, Hausberger M. An unexpected acoustic indicator of positive emotions in horses.. PLoS One 2018;13(7):e0197898.
  34. Bergeron R, Badnell-Waters S, Lambton S, Mason G. Captive ungulates: foraging, diet and gastrointestinal function in Stereotypic Animal Behaviour: Fundamentals and Applications to Welfare 2nd ed.. (eds Mason, G. & Rushen, J.) 19–57 (Oxford Press, 2006).
  35. TINBERGEN N. Derived activities; their causation, biological significance, origin, and emancipation during evolution.. Q Rev Biol 1952 Mar;27(1):1-32.
    doi: 10.1086/398642pubmed: 14930222google scholar: lookup
  36. Troisi A. Displacement activities as a behavioral measure of stress in nonhuman primates and human subjects.. Stress 2002 Feb;5(1):47-54.
    doi: 10.1080/102538902900012378pubmed: 12171766google scholar: lookup
  37. Rochais C, Henry S, Hausberger M. “Hay-bags” and “Slow feeders”: Testing their impact on horse behaviour and welfare. Appl Anim Behav Sci 2018;198:52–59.
  38. Briefer EF, Maigrot AL, Mandel R, Freymond SB, Bachmann I, Hillmann E. Segregation of information about emotional arousal and valence in horse whinnies.. Sci Rep 2015 Apr 21;4:9989.
    doi: 10.1038/srep09989pmc: PMC4404681pubmed: 25897781google scholar: lookup
  39. Kaiser L, Heleski CR, Siegford J, Smith KA. Stress-related behaviors among horses used in a therapeutic riding program.. J Am Vet Med Assoc 2006 Jan 1;228(1):39-45.
    doi: 10.2460/javma.228.1.39pubmed: 16426164google scholar: lookup
  40. Baragli P, Vitale V, Banti L, Sighieri C. Effect of aging on behavioural and physiological responses to a stressful stimulus in horses (Equus caballus). Behaviour 2014;151(11):1513–1533.
    doi: 10.1163/1568539X-00003197google scholar: lookup
  41. Hausberger M, Muller C, Lunel C. Does work affect personality? A study in horses.. PLoS One 2011 Feb 9;6(2):e14659.
  42. Désiré L, Boissy A, Veissier I. Emotions in farm animals: a new approach to animal welfare in applied ethology.. Behav Processes 2002 Nov;60(2):165-180.
    doi: 10.1016/S0376-6357(02)00081-5pubmed: 12426068google scholar: lookup
  43. Stanley DJ, Meyer JP. Two-dimensional affective space: a new approach to orienting the axes.. Emotion 2009 Apr;9(2):214-37.
    doi: 10.1037/a0014612pubmed: 19348534google scholar: lookup
  44. Barrett LF, Mesquita B, Ochsner KN, Gross JJ. The experience of emotion.. Annu Rev Psychol 2007;58:373-403.
  45. Nesse RM, Ellsworth PC. Evolution, emotions, and emotional disorders.. Am Psychol 2009 Feb-Mar;64(2):129-39.
    doi: 10.1037/a0013503pubmed: 19203145google scholar: lookup
  46. . Heart rate variability: standards of measurement, physiological interpretation and clinical use. Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology.. Circulation 1996 Mar 1;93(5):1043-65.
    doi: 10.1161/01.CIR.93.5.1043pubmed: 8598068google scholar: lookup
  47. Yeon SC. Acoustic communication in the domestic horse (Equus caballus). J. Vet Behav 2012;7(3):179–185.
  48. Maestripieri D, Schino G, Aureli F, Troisi A. A modest proposal: displacement activities as an indicator of emotions in primates. Anim Behav 1992;44(5):967–979.
  49. ZEIGLER HP. DISPLACEMENT ACTIVITY AND MOTIVATIONAL THEORY: A CASE STUDY IN THE HISTORY OF ETHOLOGY.. Psychol Bull 1964 May;61:362-76.
    doi: 10.1037/h0044307pubmed: 14147564google scholar: lookup
  50. McFarland DJ. On the causal and functional significance of displacement activities.. Z Tierpsychol 1966 Jun;23(2):217-35.
  51. Spruijt BM, van Hooff JA, Gispen WH. Ethology and neurobiology of grooming behavior.. Physiol Rev 1992 Jul;72(3):825-52.
    doi: 10.1152/physrev.1992.72.3.825pubmed: 1320764google scholar: lookup
  52. Duboscq J, Romano V, Sueur C, MacIntosh AJ. Scratch that itch: revisiting links between self-directed behaviour and parasitological, social and environmental factors in a free-ranging primate.. R Soc Open Sci 2016 Nov;3(11):160571.
    doi: 10.1098/rsos.160571pmc: PMC5180144pubmed: 28018646google scholar: lookup
  53. Schino G, Scucchi S, Maestripieri D, Turillazzi PG. Allogrooming as a tension‐reduction mechanism: a behavioral approach. Am J. Primatol 1988;16(1):43–50.
    doi: 10.1002/ajp.1350160106google scholar: lookup
  54. Aureli F, Van Schaik CP, Van Hooff JARAM. Functional aspects of reconciliation among captive long‐tailed macaques (Macaca fascicularis). Am J. Primatol 1989;19(1):39–51.
    doi: 10.1002/ajp.1350190105google scholar: lookup
  55. Boccia ML, Reite M, Laudenslager M. On the physiology of grooming in a pigtail macaque.. Physiol Behav 1989 Mar;45(3):667-70.
    doi: 10.1016/0031-9384(89)90089-9pubmed: 2756061google scholar: lookup
  56. Liang AC, Grace JK, Tompkins EM, Anderson DJ. Yawning, acute stressors, and arousal reduction in Nazca booby adults and nestlings.. Physiol Behav 2015 Mar 1;140:38-43.
    doi: 10.1016/j.physbeh.2014.11.029pubmed: 25498600google scholar: lookup
  57. Zannella A, Norscia I, Stanyon R, Palagi E. Testing yawning hypotheses in wild populations of two strepsirrhine species: Propithecus verreauxi and Lemur catta.. Am J Primatol 2015 Nov;77(11):1207-15.
    doi: 10.1002/ajp.22459pubmed: 26317594google scholar: lookup
  58. Lansade Léa, Bouissou Marie-France, Erhard Hans W. Fearfulness in horses: A temperament trait stable across time and situations. Applied Animal Behaviour Science 2008;115(3-4):182–200.
  59. Wolff A, Hausberger M, Le Scolan N. Experimental tests to assess emotionality in horses.. Behav Processes 1997 Sep;40(3):209-21.
    doi: 10.1016/S0376-6357(97)00784-5pubmed: 24895882google scholar: lookup
  60. Cannon WB. Homeostasis. The wisdom of the body (Norton, 1932).
  61. Martin K, Wiebe KL. Coping mechanisms of alpine and arctic breeding birds: extreme weather and limitations to reproductive resilience.. Integr Comp Biol 2004 Apr;44(2):177-85.
    doi: 10.1093/icb/44.2.177pubmed: 21680497google scholar: lookup
  62. Wingfield JC. The comparative biology of environmental stress: behavioural endocrinology and variation in ability to cope with novel, changing environments. Anim Behav 2013;85(5):1127–1133.
  63. Hamlin RL, Klepinger WL, Gilpin KW, Smith CR. Autonomic control of heart rate in the horse.. Am J Physiol 1972 Apr;222(4):976-8.
  64. Physick-Sheard PW, Marlin DJ, Thornhill R, Schroter RC. Frequency domain analysis of heart rate variability in horses at rest and during exercise.. Equine Vet J 2000 May;32(3):253-62.
    doi: 10.2746/042516400776563572pubmed: 10836482google scholar: lookup
  65. Nardelli M, Greco A, Bolea J, Valenza G, Scilingo EP, Bailon R. Investigation of Lagged Poincaré Plot reliability in ultra-short synthetic and experimental Heart Rate Variability series.. Annu Int Conf IEEE Eng Med Biol Soc 2017 Jul;2017:2329-2332.
    pubmed: 29060364doi: 10.1109/embc.2017.8037322google scholar: lookup
  66. McGreevy P. Equine behavior: A guide for veterinarians and equine scientists. Saunders, 2004.
  67. McDonnell SM, Haviland JCS. Agonistic ethogram of equid bachelor band. Appl. Anim. Behav. Sci. 1995;43(3):147–188.

Citations

This article has been cited 10 times.
  1. Seganfreddo S, Fornasiero D, De Santis M, Mutinelli F, Normando S, Contalbrigo L. A Pilot Study on Behavioural and Physiological Indicators of Emotions in Donkeys.. Animals (Basel) 2023 Apr 25;13(9).
    doi: 10.3390/ani13091466pubmed: 37174503google scholar: lookup
  2. Janicka W, Wilk I, Próchniak T, Janczarek I. Can Sound Alone Act as a Virtual Barrier for Horses? A Preliminary Study.. Animals (Basel) 2022 Nov 15;12(22).
    doi: 10.3390/ani12223151pubmed: 36428379google scholar: lookup
  3. Marliani G, Vannucchi I, Kiumurgis I, Accorsi PA. Limitations of Spatial Judgment Bias Test Application in Horses (Equus ferus caballus).. Animals (Basel) 2022 Nov 3;12(21).
    doi: 10.3390/ani12213014pubmed: 36359138google scholar: lookup
  4. Merkies K, Sudarenko Y, Hodder AJ. Can Ponies (Equus Caballus) Distinguish Human Facial Expressions?. Animals (Basel) 2022 Sep 7;12(18).
    doi: 10.3390/ani12182331pubmed: 36139191google scholar: lookup
  5. Baragli P, Scopa C, Felici M, Reddon AR. Horses show individual level lateralisation when inspecting an unfamiliar and unexpected stimulus.. PLoS One 2021;16(8):e0255688.
    doi: 10.1371/journal.pone.0255688pubmed: 34351986google scholar: lookup
  6. Wascher CAF. Heart rate as a measure of emotional arousal in evolutionary biology.. Philos Trans R Soc Lond B Biol Sci 2021 Aug 16;376(1831):20200479.
    doi: 10.1098/rstb.2020.0479pubmed: 34176323google scholar: lookup
  7. Corgan ME, Grandin T, Matlock S. Evaluating the Reaction to a Complex Rotated Object in the American Quarter Horse (Equus caballus).. Animals (Basel) 2021 May 13;11(5).
    doi: 10.3390/ani11051383pubmed: 34068020google scholar: lookup
  8. Norscia I, Collarini E, Cordoni G. Anxiety Behavior in Pigs (Sus scrofa) Decreases Through Affiliation and May Anticipate Threat.. Front Vet Sci 2021;8:630164.
    doi: 10.3389/fvets.2021.630164pubmed: 33665219google scholar: lookup
  9. Scopa C, Greco A, Contalbrigo L, Fratini E, Lanatà A, Scilingo EP, Baragli P. Inside the Interaction: Contact With Familiar Humans Modulates Heart Rate Variability in Horses.. Front Vet Sci 2020;7:582759.
    doi: 10.3389/fvets.2020.582759pubmed: 33330706google scholar: lookup
  10. Gehlen H, Loschelder J, Merle R, Walther M. Evaluation of Stress Response under a Standard Euthanasia Protocol in Horses Using Analysis of Heart Rate Variability.. Animals (Basel) 2020 Mar 13;10(3).
    doi: 10.3390/ani10030485pubmed: 32183168google scholar: lookup