Effects of breed, management and personality on cortisol reactivity in sport horses

English version

Autoři: Fay J. Sauer ^aff001; Marco Hermann ^aff002; Alessandra Ramseyer ^aff001; Dominik Burger ^aff001; Stefanie Riemer ^aff003; Vinzenz Gerber ^aff001
Působiště autorů: Department of Clinical Veterinary Medicine, Swiss Institute for Equine Medicine (ISME), Vetsuisse Faculty, University of Bern, and Agroscope, Bern, Bern, Switzerland ^aff001; Pferdemedizin Hermann GmbH, Niederlenz, Aargau, Switzerland ^aff002; Division of Animal Welfare, Vetsuisse Faculty, University of Bern, Bern, Switzerland ^aff003
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0221794

Souhrn

Sport horses need to fulfill high physical and psychological requirements during training and competition. These as well as certain conditions of modern husbandry may affect their wellbeing. Here we aimed to (1) evaluate effects of demographic and management factors as well as personality traits on stress reactivity of sport horses, (2) investigate if elite sport horses have elevated stress levels compared to amateur sport horses, and (3) assess whether different equestrian disciplines differentially influence equine adrenal cortex responsiveness. For this purpose, we visited 149 healthy elite (n = 94) and amateur (n = 54) sport horses in Switzerland and performed an adrenocorticotropic hormone (ACTH) stimulation test. Additionally, a person who was familiar with the horse completed a questionnaire about demographic and management factors and their horses’ personality traits. Linear models were calculated to assess associations between the questionnaire data and salivary cortisol 60 (T60) and 90 (T90) minutes after ACTH stimulation. While the model at T90 was not significant, post-stimulatory cortisol after 60 minutes appears most informative in line with a previous study and was significantly affected by the breed and by three management factors: “number of riders”, “hours spent outside” and “group housing” (adjusted r² = 15%, p<0.001). Thoroughbred and Warmblood horses displayed an increased adrenal response compared to Franches-Montagnes horses. Horses with several riders had a less pronounced reaction than horses with one rider, and horses that spent more time outside had a decreased response compared to horses that were stabled most of the time. Horses living in groups showed higher post-stimulatory cortisol values than horses that were housed singly. However, no significant associations of cortisol responsiveness with personality traits were found, and neither the use as elite or as amateur sport horses nor the discipline had an effect on the cortisol response. This suggests that optimizing husbandry conditions may be more important for improving equine welfare than changing their use.

Klíčová slova:

Animal husbandry – Cortisol – Horses – Personality – Personality tests – Personality traits – Sports – Traditional ACTH stimulation test

Zdroje

1. Houpt KA. Domestic animal behavior for veterinarians and animal scientists. 6th ed. Hoboken, NJ: John Wiley & Sons; 2018.

2. Mayes E, Duncan P. Temporal Patterns of Feeding Behaviour in Free-Ranging Horses. Behaviour. 1986;96(1–2):105–29.

3. Hinchcliff KW, Kaneps AJ, Geor RJ. Equine sports medicine and surgery: basic and clinical sciences of the equine athlete. 2nd ed. Philadelphia: Saunders Elsevier; 2013.

4. Hinchcliff K, Geor R. The horse as an athlete: a physiological overview. In: Hinchcliff KW, Geor RJ, Kaneps AJ, editors. Equine exercise physiology: the science of exercise in the athletic horse. 1st ed. Philadelphia: Saunders Elsevier; 2008.

5. Art T, Lekeux P. Exercise-induced physiological adjustments to stressful conditions in sports horses. Livestock Production Science. 2005;92(2):101–11.

6. Werhahn H, Hessel EF, Van den Weghe HFA. Competition Horses Housed in Single Stalls (II): Effects of Free Exercise on the Behavior in the Stable, the Behavior during Training, and the Degree of Stress. J Equine Vet Sci. 2012;32(1):22–31.

7. Ruet A, Lemarchand J, Parias C, Mach N, Moisan MP, Foury A, et al. Housing Horses in Individual Boxes Is a Challenge with Regard to Welfare. Animals (Basel). 2019;9(9).

8. Goodwin D, Davidson HP, Harris P. Foraging enrichment for stabled horses: effects on behaviour and selection. Equine Vet J. 2002;34(7):686–91. doi: 10.2746/042516402776250450 12455839

9. McGowan C, Whitworth D. Overtraining syndrome in horses. Comp Exerc Phys. 2008;5(2):57–65.

10. Selye H. The evolution of the stress concept. Am Sci. 1973;61(6):692–9. 4746051

11. Borstel UKv, Visser E, Hall C. Indicators of stress in equitation. Appl Anim Behav Sci. 2017;190:43–56.

12. Moberg GP. Biological response to stress: implications for animal welfare. In: Moberg GP, Mench JA, editors. The biology of animal stress: basic principles and implications for animal welfare. Wallingford CABI Publishing; 2000. p. 1–21.

13. Bachmann I, Bernasconi P, Herrmann R, Weishaupt M, Stauffacher M. Behavioural and physiological responses to an acute stressor in crib-biting and control horses. Appl Anim Behav Sci. 2003;82(4):297–311.

14. Malmkvist J, Poulsen JM, Luthersson N, Palme R, Christensen JW, Sondergaard E. Behaviour and stress responses in horses with gastric ulceration. Appl Anim Behav Sci. 2012;142(3–4):160–7.

15. Schmidt A, Aurich J, Mostl E, Muller 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;58(4):628–36. doi: 10.1016/j.yhbeh.2010.06.011 20600048

16. Wickens CL, Heleski CR. Crib-biting behavior in horses: a review. Appl Anim Behav Sci. 2010;128(1–4):1–9.

17. Pawluski J, Jego P, Henry S, Bruchet A, Palme R, Coste C, et al. Low plasma cortisol and fecal cortisol metabolite measures as indicators of compromised welfare in domestic horses (Equus caballus). PLoS One. 2017;12(9):e0182257. doi: 10.1371/journal.pone.0182257 28886020

18. Yarnell K, Hall C, Royle C, Walker SL. Domesticated horses differ in their behavioural and physiological responses to isolated and group housing. Physiol Behav. 2015;143:51–7. doi: 10.1016/j.physbeh.2015.02.040 25725117

19. Medill SA, Janz DA, cLoughlin PD. Hair testosterone and cortisol concentrations and their relationships to physiological and social status in feral horses (Equus ferus caballus). Nuertingen University: Proceedings of the 3rd International Equine Science Meeting 2015. p. 21.

20. Ladewig J, Smidt D. Behavior, episodic secretion of cortisol, and adrenocortical reactivity in bulls subjected to tethering. Horm Behav. 1989;23(3):344–60. doi: 10.1016/0018-506x(89)90048-2 2793077

21. Van Reenen C, Mars M, Leushuis I, Rijsewijk F, Van Oirschot J, Blokhuis H. Social isolation may influence responsiveness to infection with bovine herpesvirus 1 in veal calves. Vet Microbiol. 2000;75(2):135–43. doi: 10.1016/s0378-1135(00)00211-x 10889404

22. Hedberg Y, Dalin AM, Forsberg M, Lundeheim N, Hoffmann B, Ludwig C, et al. Effect of ACTH (tetracosactide) on steroid hormone levels in the mare. Part A: effect in intact normal mares and mares with possible estrous related behavioral abnormalities. Anim Reprod Sci. 2007;100(1–2):73–91. doi: 10.1016/j.anireprosci.2006.06.008 16870362

23. Scheidegger MD, Gerber V, Bruckmaier RM, van der Kolk JH, Burger D, Ramseyer A. Increased adrenocortical response to adrenocorticotropic hormone (ACTH) in sport horses with equine glandular gastric disease (EGGD). Vet J. 2017;228:7–12. doi: 10.1016/j.tvjl.2017.09.002 29153110

24. Von Borell E, Ladewig J. Altered adrenocortical response to acute stressors or ACTH (1–24) in intensively housed pigs. Domest Anim Endocrinol. 1989;6(4):299–309. doi: 10.1016/0739-7240(89)90024-6 2575968

25. Freymond SB, Bardou D, Briefer EF, Bruckmaier R, Fouche N, Fleury J, et al. The physiological consequences of crib-biting in horses in response to an ACTH challenge test. Physiol Behav. 2015;151:121–8. doi: 10.1016/j.physbeh.2015.07.015 26187578

26. Sauer FJ, Bruckmaier RM, Ramseyer A, Vidondo B, Scheidegger MD, Gerber V. Diagnostic accuracy of post-ACTH challenge salivary cortisol concentrations for identifying horses with equine glandular gastric disease. J Anim Sci. 2018;96(6):2154–61. doi: 10.1093/jas/sky074 29762691

27. Visser EK, Ellis AD, Van Reenen CG. The effect of two different housing conditions on the welfare of young horses stabled for the first time. Appl Anim Behav Sci. 2008;114(3–4):521–33.

28. McGreevy PD, Cripps PJ, French NP, Green LE, Nicol CJ. Management factors associated with stereotypic and redirected behaviour in the thoroughbred horse. Equine Vet J. 1995;27(2):86–91. doi: 10.1111/j.2042-3306.1995.tb03041.x 7607155

29. Parker M, Goodwin D, Redhead ES. Survey of breeders’ management of horses in Europe, North America and Australia: comparison of factors associated with the development of abnormal behaviour. Appl Anim Behav Sci. 2008;114(1–2):206–15.

30. Bachmann I, Audige L, Stauffacher M. Risk factors associated with behavioural disorders of crib-biting, weaving and box-walking in Swiss horses. Equine Vet J. 2003;35(2):158–63. doi: 10.2746/042516403776114216 12638792

31. Christie JL, Hewson CJ, Riley CB, McNiven MA, Dohoo IR, Bate LA. Management factors affecting stereotypies and body condition score in nonracing horses in Prince Edward Island. Can Vet J. 2006;47(2):136–43. 16579039

32. McGreevy PD, French NP, Nicol CJ. The prevalence of abnormal behaviours in dressage, eventing and endurance horses in relation to stabling. Vet Rec. 1995;137(2):36–7. doi: 10.1136/vr.137.2.36 8525580

33. Becker-Birck M, Schmidt A, Lasarzik J, Aurich J, Mostl E, Aurich C. Cortisol release and heart rate variability in sport horses participating in equestrian competitions. Journal of Veterinary Behavior-Clinical Applications and Research. 2013;8(2):87–94.

34. Janczarek I, Bereznowski A, Strzelec K. The influence of selected factors and sport results of endurance horses on their saliva cortisol concentration. Pol J Vet Sci. 2013;16(3):533–41. doi: 10.2478/pjvs-2013-0074 24195289

35. Bartolome E, Cockram MS. Potential Effects of Stress on the Performance of Sport Horses. J Equine Vet Sci. 2016;40:84–93.

36. Valenchon M, Levy F, Moussu C, Lansade L. Stress affects instrumental learning based on positive or negative reinforcement in interaction with personality in domestic horses. PLoS One. 2017;12(5):e0170783. doi: 10.1371/journal.pone.0170783 28475581

37. Valenchon M, Levy F, Prunier A, Moussu C, Calandreau L, Lansade L. Stress modulates instrumental learning performances in horses (Equus caballus) in interaction with temperament. PLoS One. 2013;8(4):e62324. doi: 10.1371/journal.pone.0062324 23626801

38. Valenchon M, Levy F, Fortin M, Leterrier C, Lansade L. Stress and temperament affect working memory performance for disappearing food in horses, Equus caballus. Anim Behav. 2013;86(6):1233–40.

39. Hoffman RM, Kronfeld DS, Holland JL, Greiwe-Crandell KM. Preweaning diet and stall weaning method influences on stress response in foals. J Anim Sci. 1995;73(10):2922–30. doi: 10.2527/1995.73102922x 8617662

40. Golland LC, Evans DL, Stone GM, Tyler-McGowan CM, Hodgson DR, Rose RJ. Plasma cortisol and ß-endorphin concentrations in trained and over-trained Standardbred racehorses. Pflügers Archiv European Journal of Physiology. 1999;439(1):11–7.

41. Wagner EL, Tyler PJ. A Comparison of Weight Estimation Methods in Adult Horses. J Equine Vet Sci. 2011;31(12):706–10.

42. Henneke D, Potter G, Kreider J, Yeates B. Relationship between condition score, physical measurements and body fat percentage in mares. Equine Vet J. 1983;15(4):371–2. doi: 10.1111/j.2042-3306.1983.tb01826.x 6641685

43. Peeters M, Sulon J, Beckers JF, Ledoux D, Vandenheede M. Comparison between blood serum and salivary cortisol concentrations in horses using an adrenocorticotropic hormone challenge. Equine Vet J. 2011;43(4):487–93. doi: 10.1111/j.2042-3306.2010.00294.x 21496072

44. Scheidegger MD, Gerber V, Ramseyer A, Schupbach-Regula G, Bruckmaier RM, van der Kolk JH. Repeatability of the ACTH stimulation test as reflected by salivary cortisol response in healthy horses. Domest Anim Endocrinol. 2016;57:43–7. doi: 10.1016/j.domaniend.2016.04.002 27565229

45. Momozawa Y, Kusunose R, Kikusui T, Takeuchi Y, Mori Y. Assessment of equine temperament questionnaire by comparing factor structure between two separate surveys. Appl Anim Behav Sci. 2005;92(1–2):77–84.

46. R Core Team. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. 2019.

47. Cayado P, Munoz-Escassi B, Dominguez C, Manley W, Olabarri B, Sanchez de la Muela M, et al. Hormone response to training and competition in athletic horses. Equine Vet J Suppl. 2006;38(36):274–8.

48. Marc M, Parvizi N, Ellendorff F, Kallweit E, Elsaesser F. Plasma cortisol and ACTH concentrations in the warmblood horse in response to a standardized treadmill exercise test as physiological markers for evaluation of training status. J Anim Sci. 2000;78(7):1936–46. doi: 10.2527/2000.7871936x 10907837

49. Mircean M, Giurgiu G, Mircean V, Zinveliu E. Serum cortisol variation of sport horses in relation with the level of training and effort intensity. Bulletin USAMV-CN. 2007;64(1–2):488–92.

50. Ille N, Von Lewinski M, Erber R, Wulf M, Aurich J, Möstl E, et al. Effects of the level of experience of horses and their riders on cortisol release, heart rate and heart-rate variability during a jumping course. Animal Welfare. 2013;22(4):457–65.

51. Munsters CC, Visser KE, van den Broek J, van Oldruitenborgh-Oosterbaan MMS. The influence of challenging objects and horse-rider matching on heart rate, heart rate variability and behavioural score in riding horses. The Veterinary Journal. 2012;192(1):75–80. doi: 10.1016/j.tvjl.2011.04.011 21612959

52. Castejon-Riber C, Riber C, Rubio MD, Aguera E, Munoz A. Objectives, Principles, and Methods of Strength Training for Horses. J Equine Vet Sci. 2017;56:93–103.

53. Bruin G, Kuipers H, Keizer HA, Vander Vusse GJ. Adaptation and overtraining in horses subjected to increasing training loads. J Appl Physiol (1985). 1994;76(5):1908–13.

54. Persson SG, Larsson M, Lindholm A. Effects of training on adreno-cortical function and red-cell volume in trotters. Zentralbl Veterinarmed A. 1980;27(4):261–8. doi: 10.1111/j.1439-0442.1980.tb02004.x 6252726

55. Munk R, Jensen RB, Palme R, Munksgaard L, Christensen JW. An exploratory study of competition scores and salivary cortisol concentrations in Warmblood horses. Domest Anim Endocrinol. 2017;61:108–16. doi: 10.1016/j.domaniend.2017.06.007 28800426

56. Brockhurst J, Cheleuitte-Nieves C, Buckmaster CL, Schatzberg AF, Lyons DM. Stress inoculation modeled in mice. Translational psychiatry. 2015;5:e537. doi: 10.1038/tp.2015.34 25826112

57. Parker KJ, Buckmaster CL, Schatzberg AF, Lyons DM. Prospective investigation of stress inoculation in young monkeys. Arch Gen Psychiatry. 2004;61(9):933–41. doi: 10.1001/archpsyc.61.9.933 15351772

58. Fox C, Merali Z, Harrison C. Therapeutic and protective effect of environmental enrichment against psychogenic and neurogenic stress. Behav Brain Res. 2006;175(1):1–8. doi: 10.1016/j.bbr.2006.08.016 16970997

59. Rivera E, Benjamin S, Nielsen B, Shelle J, Zanella AJ. Behavioral and physiological responses of horses to initial training: the comparison between pastured versus stalled horses. Appl Anim Behav Sci. 2002;78(2–4):235–52.

60. Kiley-Worthington M. The behavior of horses in relation to management and training—towards ethologically sound environments. J Equine Vet Sci. 1990;10(1):62–75.

61. Aurich J, Wulf M, Ille N, Erber R, von Lewinski M, Palme R, et al. Effects of season, age, sex, and housing on salivary cortisol concentrations in horses. Domest Anim Endocrinol. 2015;52:11–6. doi: 10.1016/j.domaniend.2015.01.003 25700267

62. Heleski CR, Shelle AC, Nielsen BD, Zanella AJ. Influence of housing on weanling horse behavior and subsequent welfare. Appl Anim Behav Sci. 2002;78(2–4):291–302.

63. Harewood EJ, McGowan CM. Behavioral and physiological responses to stabling in naive horses. J Equine Vet Sci. 2005;25(4):164–70.

64. Alexander SL, Irvine CH. The effect of social stress on adrenal axis activity in horses: the importance of monitoring corticosteroid-binding globulin capacity. J Endocrinol. 1998;157(3):425–32. doi: 10.1677/joe.0.1570425 9691975

65. Nagy K, Bodó G, Bárdos G, Bánszky N, Kabai P. Differences in temperament traits between crib-biting and control horses. Appl Anim Behav Sci. 2010;122(1):41–7.

66. Anderson MK, Friend TH, Evans JW, Bushong DM. Behavioral assessment of horses in therapeutic riding programs. Appl Anim Behav Sci. 1999;63(1):11–24.

67. Fazio E, Medica P, Cravana C, Ferlazzo A. Cortisol response to road transport stress in calm and nervous stallions. Journal of Veterinary Behavior-Clinical Applications and Research. 2013;8(4):231–7.

68. Hauner KK, Adam EK, Mineka S, Doane LD, DeSantis AS, Zinbarg R, et al. Neuroticism and introversion are associated with salivary cortisol patterns in adolescents. Psychoneuroendocrinology. 2008;33(10):1344–56. doi: 10.1016/j.psyneuen.2008.07.011 18809259

69. Bae YJ, Gaudl A, Jaeger S, Stadelmann S, Hiemisch A, Kiess W, et al. Immunoassay or LC-MS/MS for the measurement of salivary cortisol in children? Clin Chem Lab Med. 2016;54(5):811–22. doi: 10.1515/cclm-2015-0412 26562033

70. Sauer FJ, Gerber V, Frei S, Bruckmaier RM, Groessl M. Salivary cortisol measurement in horses: Immunoassay or LC-MS/MS?: Forthcoming.

71. Cordero M, Brorsen BW, McFarlane D. Circadian and circannual rhythms of cortisol, ACTH, and alpha-melanocyte-stimulating hormone in healthy horses. Domest Anim Endocrinol. 2012;43(4):317–24. doi: 10.1016/j.domaniend.2012.05.005 22717182

72. Irvine CH, Alexander SL. Factors affecting the circadian rhythm in plasma cortisol concentrations in the horse. Domest Anim Endocrinol. 1994;11(2):227–38. doi: 10.1016/0739-7240(94)90030-2 8045104

73. Schmidt A, Aurich C, Neuhauser S, Aurich J, Möstl E. Comparison of cortisol levels in blood plasma, saliva and faeces of horses submitted to different stressors or treated with ACTH. Sydney: Proceedings, 5. Intern. Symposium Equitation Science; 2009. p. 53.

Effects of breed, management and personality on cortisol reactivity in sport horses

Souhrn

Klíčová slova:

Zdroje

PLOS One

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