Accepted Manuscript

Potential effects of stress on the performance of sport horses

E. Bartolomé, M.S. Cockram

PII: S0737-0806(15)30072-1
DOI: 10.1016/j.jevs.2016.01.016
Reference: YJEVS 2032

To appear in: Journal of Equine Veterinary Science

Received Date: 2 November 2015

Revised Date: 26 January 2016
Accepted Date: 31 January 2016

Please cite this article as: Bartolomé E, Cockram MS, Potential effects of stress on the performance of
sport horses, Journal of Equine Veterinary Science (2016), doi: 10.1016/j.jevs.2016.01.016.

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 ACCEPTED MANUSCRIPT

1 Potential effects of stress on the performance of sport horses

2 Bartolomé, E.1*, Cockram, M.S.2

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3 Lusófona University, Faculty of Veterinary Medicine, Campo Grande 376, 1749-024 Lisbon,

4 Portugal.

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5 Sir James Dunn Animal Welfare Centre, Department of Health Management, Atlantic

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6 Veterinary College, University of Prince Edward Island, 550 University Avenue, Charlottetown,

7 PEI, Canada C1A 4P3.

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8 *Corresponding author: p5016@ulusofona.pt.

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10 ABSTRACT

11 Due to its physical and physiological characteristics, the horse has a natural predisposition for

12 use in sport. However, the use of horses as “competition tools” frequently results in several

13 problems related to stress that directly or indirectly bias their sporting performance.

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14 Hence, the aim of this manuscript is to examine literature on the influence of stress on sport

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15 horse performance and highlight potential avenues for improvements in their breeding and

16 welfare.

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17 The stress response is initiated when a stimulus (the stressor) is perceived as a potential threat,

18 resulting in a combination of biological responses designed to alleviate the effects of the

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perceived stressor. Stress can have positive as well as negative effects on the body helping the
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20 animal to cope with routine short-term stressors that in some circumstances can enhance

performance, but in others it can impair performance. A good sport performer has a combination
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22 of superior conformation, an appropriate temperament, a healthy physical condition and primed

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23 physiological mechanisms and function for optimal fitness that keeps the horse performing well.
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24 In addition, it is more valuable if it has the appropriate genetic background and good

25 reproductive ability. How stress can potentially affect these characteristics is discussed in this
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26 review. The development of a broader selection strategy for breeding of sport horses that takes

27 into account aspects as conformation, temperament, genetics, health and the physiology of the
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28 horse, together with an adequate control of the environment, is likely to improve the welfare of
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29 horses during competitions.

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31 KEYWORDS

32 Conformation; Physiology; Behaviour; Genetics; Horse; Temperament

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34

35 1. INTRODUCTION

36 The horse is an extraordinary athlete, with incredible speed and endurance abilities developed as

37 the result of their evolution as grazing animals. Horse domestication has subsequently modified

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38 or enhanced these desirable characteristics by selective breeding and horses have been adapted to

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39 a large variety of uses according to their main aptitudes. Hence, large, heavy breeds of horses

40 were bred for draft work and used in either agricultural or military work; whereas lighter horses

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41 were bred for speed and endurance and were used mainly for transportation, herding and sport

42 [1]. In general, the athletic capacity of a horse is attributable to physiologic adaptations from

43
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their time living in the wild, such as their capacity to provide an explosive effort to escape from
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44 predators, becoming a species with superior athletic ability [1,2]. This “natural reaction” is

commonly known as the “flight-fight response”. It is just one mechanism evolved to cope with
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46 daily novel stimuli, hence improving the adaptation of the animal to its environment [3]. On the
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47 other hand, constant exposure to stressors can result in a non-adaptive response and hence
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48 potentially cause deleterious effects on the animal’s physiology [3–7]. As sport animals, horses

49 frequently suffer from several problems, derived from their use as “competition tools”, pushing
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50 them to limits that would not normally be achieved in the wild [2].

51 Hence, stress could appear either as an enhancer or as a limiting factor for the sport ability of the
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52 horse, thus determining the performance obtained [6–9]. Given the international scope of the
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53 equine industry, with the continuous trade of horses and a recent increase in the exchange of

54 genetic material in sport horse breeding [10], obtaining poor performance (or even failure to

55 compete at all) due to stress could seriously affect the economic value of the animal and hence

56 the value of its semen/ova. Thus, knowing the factors that produce stress and hence bias the

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57 performance ability of the horse is of great interest for not only riders or horse breeders, but for

58 the whole equine industry.

59 Hence, the main aim of this manuscript was to examine literature on the influence of stress on

60 horse sport performance to highlight potential avenues for improvements in sport horse breeding

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61 and welfare.

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62

63 2. STRESS IN SPORT PERFORMANCE

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64 2.1. What is stress?

65 Stress is an ambiguous term used to define a wide range of responses by the animal to its

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environment. There are many definitions of stress. However, most definitions consider that “…
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67 stress is the recognition by the body of a stressor and therefore the state of threatened

homeostasis; stressors are threats against homeostasis; and adaptive responses are the body’s
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69 attempt to counteract the stressor and re-establish homeostasis” [11]. A key part of the response
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70 to a stressor is the recognition by the Central Nervous System (CNS) of a stimulus perceived as a
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71 potential threat to body homeostasis. In fact, the “perception of threat” from the animal is crucial,

72 no matter whether or not it comprises a real danger [12]. Once the CNS perceives this potential
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73 threat, it develops a biological response that consists of a combination of biological “defense

74 responses”, that will work together (either all or only some of them) to attempt to alleviate the
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75 effects of the perceived stressor: the behavioural response, the Autonomic Nervous System
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76 (ANS) response and the neuroendocrine response [3].

77 The behavioural response is the most biologically economical and is usually the first response

78 shown by the animal. There are a number of different behavioural patterns indicative of stress in

79 any animal species [13]. However, as the behavioural response is usually stressor- and animal-

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80 specific, ‘general’ behavioural stress responses that animals show in every situation regardless of

81 the type of stressor are ill-defined [14].

82 The ANS is associated with the well-known ‘flight or fight’ response [15]. When stimulated, it

83 affects a diverse number of biological systems, including the cardiovascular system, the

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84 gastrointestinal system, the exocrine glands and the adrenal medulla [16]. Both branches of the

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85 ANS, the Sympathetic Nervous System (SNS) and the Parasympathetic Nervous System (PNS)

86 are stimulated during exercise. The PNS increases in the beginning of the exercise, activating the

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87 SNS, which stimulates a systemic release of catecholamines (epinephrine and norepinephrine)

88 that potentiates the response to exercise, increasing muscle blood flow and mobilizing glycogen

89 and free fatty acids to fuel exertion [17, 18].

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90 Last, the neuroendocrine response, mediated by the hypothalamus-pituitary-adrenal (HPA) axis

can produce a release of cortisol that can have broad, long-lasting effects on the body, regulating
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92 a range of biological functions, such as immune competence, reproduction, metabolism and

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93 behaviour [3].
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94 At least two general types of coping strategies can be found when confronting stress: active

95 copers or “proactive horses” and passive copers or “reactive horses” [20]. The proactive response
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96 is mainly characterized by active behavioural reactivity such as the ‘fight-flight response’ (fight

97 and aggressive-dominant behaviour or flight and fearful behaviour), predominance of the SNS
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98 and low HPA axis reactivity. On the other hand, the reactive response involves behavioural
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99 inhibition, with lower locomotion, immobility, freezing behaviour or withdrawal; predominance

100 of PNS and high HPA response [21].

101 A diagram describing the stress process is shown in Figure 1.

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103 2.2. Stress versus Distress

104 Stress does not always result in a negative influence on body homeostasis, as it is one of the

105 physiological mechanisms that animals have evolved to cope with normal short-term stressors

106 that are routinely encountered [3]. Thus, in these cases, the biological costs of the stress response

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107 are lower than the animal’s biological reserves to cope with them. The problem comes when this

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108 balance is broken, as then the resources demanded from the stress response must be shifted away

109 from other biological functions of the animal, such as reproduction or growth. This situation has

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110 been described as “distress” rather than stress [3]. On the other hand, Sanford et al. [22] made a

111 further distinction between distress and short-term, adaptive physiological stress stating that

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during distress the animal is likely to be aware that is making an increased effort to respond to a
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113 stimulus, whereas during “physiological stress” the animal is unaware of having to make a

homeostatic response to it. This difference has significance to studies of animal welfare. Distress
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115 implies that an animal is experiencing a negative emotional state [4], thus affecting its welfare.
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116 However, when considering sport horses, a stress response during a competition could have
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117 either positive or negative consequences on performance. During normal exercise activity, the

118 sympathoadrenal axis and HPA functions are activated, increasing heart rate and plasma cortisol
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119 concentration in the horse [19,20]. Cortisol has many positive and desirable physiological

120 functions that, in the short term, might be beneficial for the adaptation of the horse to exercise
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121 demands. These include reducing inflammation, stimulating movement and raising blood glucose
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122 concentration. Healthy sport horses recover quickly once the threatening stimuli from the

123 competition day are finished, hence decreasing their plasma cortisol concentration a short time

124 after exercise [6]. However, maintaining a high concentration of cortisol during prolonged

125 periods can cause deleterious effects, such as inducing immune-suppression or muscle wasting

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126 [24]. These effects indicate that the animal is not coping with the stress experienced during

127 exercise. One specific effect observed in sport horses of not coping is the suppression of the

128 cortisol circadian rhythm [11,21]. In normal competition circumstances, a circadian cortisol

129 rhythm emerges when horses are accustomed to a management routine, showing the highest

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130 concentrations between 08:00 and 10:00 h, and the lowest during the afternoon and evening [21].

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131 Hence, when the animal is exposed to a continuous stressful condition (e.g. high physically-

132 demanding sport competitions), it reacts by modifying normal release of cortisol, hence affecting

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133 homeostasis [25]. For this review, the negative emotional state associated with stress will be

134 referred to as “distress”, whereas the physiological positive/neutral response of the body to a

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potential threatening stimuli and to sport activity will be referred to as “physiological stress”.
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3. MAIN COMPONENTS OF A SUCCESSFUL SPORT HORSE THAT CAN BE

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138 AFFECTED BY STRESS

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139 The discipline in which the horse performs will affect the type of physical work and exercise
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140 necessary to compete in that specific sport and potentially the severity of stress that the horse

141 will have to cope with [23,26]. The thermal conditions (e.g. high temperature and high humidity)
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142 can increase the stress experienced by horses undertaking physical work and adverse weather

143 e.g. rainfall can result in deterioration of track conditions that can affect exercise performance
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144 [32–36]. Hence, some disciplines such as endurance, will require the horse to complete long
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145 distances with a low-intensity work, in external weather conditions on mainly dirt tracks [27];

146 whereas others such as dressage or show jumping require mainly agility and obedience from the

147 horse to accomplish these events of mild intensity and short duration which are normally

148 developed on covered tracks with controlled weather conditions. Galloping and trotting races are

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149 more energy-demanding disciplines, with very high-intensity and short-duration events on open

150 field tracks; whereas cross-country (or eventing) consists of high intensity and longer duration

151 events which combines three different kinds of exercise on both closed paths and open field with

152 natural obstacles [28].

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153 Therefore, information on the physical abilities and conformation as well as character traits of

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154 the horse has to be considered in the selection of the best discipline for the horse to perform in

155 [44]. Table 1 shows a summary of the literature on the influence of stress on horses according to

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156 discipline.

157 Another factor that could determine sport performance is the genetic composition of the horse, as

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it will determine both the physical and the psychological potential of the horse to perform in a
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159 certain discipline and hence, its predisposition to become stressed. Although all horse breeds can

perform any equestrian discipline, some of them are more adapted than others to certain kinds of
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161 sports due to a better physical, physiological and morphological predisposition for them, hence
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162 achieving better performance easily as a result of maximizing their inherited physical and
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163 physiological potential [29]. Thus, these animals will cope better with the stress derived from

164 sport performance as they will be physically better adapted to the physiological demands
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165 required in their discipline [30]. Hence, Warmblood breeds are more adapted for show jumping

166 and dressage competitions [10, 31], Thoroughbreds and Trotters perform better in flat and
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167 trotting races (respectively) [38,39], whereas smaller breeds such as Arabians and Arabian
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168 crosses (Anglo-Arab, Hispano-Arab, etc.) are the most competitive for endurance races and

169 three-day competitions (eventing) [40,41]. The breed also influences the psychological

170 predisposition of the horse [42,43]. Many of these differences arise from the domestication of the

171 horse (Equus caballus) when, not only physical or physiological attributes from the horses were

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172 selected by humans, but also desirable behaviours were selected for the specific purposes they

173 wanted the animals to undertake [44].

174 On the other hand, as sport ability and performance is a heritable character, humans have

175 developed strategies to improve this ability within breeds. Hence, every sport horse breed society

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176 has developed a breeding program with the selection strategies to be followed by the horses they

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177 are improving [10]. The main biological traits that breeding organizations consider as important

178 to be achieved by a sport horse are: good performance ability on the discipline they were bred

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179 for, an adequate conformation and good gait and some important, but more general aspects such

180 as fertility, good health and suitable behaviour (including soundness, durability and robustness)

181 [10].
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182 Finally, another important factor that should be accounted for in every sport performance horse

is the effect of the rider [46], as it is a major component of the reaction of the horse to their
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184 environment. Success in equestrian sports depends not only on the ability of the horse but on the
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185 rider-horse interaction and their cooperation [47]. Thus, the best horse can obtain the worst
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186 results with the wrong rider whereas a good rider can get the best potential from a mediocre

187 horse [37,48]. In fact, this rider-horse relationship can have a major influence on the level of
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188 stress perceived by the horse during the exercise. A bad balance of the rider over the horse could

189 break its normal movement hence stressing the horse [49,50]. A wrong rider perception of a
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190 horse’s temperament, not perceiving adequately the reactivity of the horse and hence its
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191 predisposition for distress [51-53] or using the wrong training techniques [54] would make

192 horses with a good physical/psychological predisposition perform badly due to the distress

193 generated by the influence of the rider.

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194 Therefore, there are many aspects of a sport horse that could be affected by stress; different

195 approaches should be taken into consideration according to the different components of

196 performance: The effect of stress on these components and how does it affects sport horse

197 performance will be discussed below.

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198

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199 4. HOW DOES STRESS AFFECT SPORT HORSES AND THUS, SPORT

200 PERFORMANCE?

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201 Stress can affect the characteristics of a good performing horse through two different

202 approaches: extrinsic and intrinsic. On the extrinsic approach, a dysfunction of one of the main

203
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components of a good performer could produce discomfort in the horse that predisposes it to
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204 suffer distress hence affecting its sporting ability. On the intrinsic approach, the physiological

stress or distress response developed by a certain stimuli (such as exercise) could produce a
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206 change in any of the main components of a good performer, biasing performance and hence
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207 changing the results of a sporting activity, to produce either better or worse results. Hence, each
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208 of the five main components that constitute a good sport performer horse will be discussed below

209 taking into account these two approaches.

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211 4.1. Conformation, gait and movement

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212 During equestrian sports, horses are forced to develop and/or maintain certain positions that
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213 differ considerably from their natural position but are necessary to develop an adequate

214 performance within that discipline [55]. During dressage, in particular, the rider has to control

215 the horse so that it maintains certain unnatural positions, that can predispose the horse to suffer

216 distress [56,57]. This has been enhanced with the use of certain types of apparatus specifically

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217 developed to control the movements of the horse, hence allowing the rider to guide the animal

218 into the exercises he wants to do. Despite being widely accepted and utilized, some of them such

219 as double bridles and jaw-clamping crank nosebands, can produce distress in the horse [58].

220 They may also not allow the horse to develop some natural behaviours, for example, “chewing

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221 gently” with the jaw [59,60].

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222 On the other hand, the use of some training methods on the sport horse could influence their

223 locomotion and conformation balance, producing an evident distress response. Some of the

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224 techniques promoted and enhanced by the equestrian federations such as the International

225 Equestrian Federation (FEI), with statements like “the head should remain in a steady position,

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as a rule slightly in front of the vertical, with a supple poll as the highest point of the neck, and
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227 no resistance should be offered to the athlete…’’ [61] lead to the use of training methods, such as

forcing the “on the bit” head and neck position [62]. McLean and McGreevy [54] described
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229 some other training techniques that may produce distress in horses during sport performance
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230 hence compromising their welfare, like hyper-flexion of the neck or rollkur position, rapping,
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231 gingering, soring, sedation and nerve blocks, electric shock-collars, horse-walkers, water

232 deprivation, apparatus intended to increase control or alter the horse’s head and neck position,
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233 certain nosebands, whips and spurs, and finally hobbles. Even though these training methods

234 could produce better sport results, at least at the beginning, they could also in the longer term
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235 comprise the horse’s sporting abilities in their discipline [59,60]. Recent studies have found a
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236 positive relationship between sport horse welfare and training techniques based on the natural

237 behaviour of the horse [52,63], hence highlighting the need to develop techniques that arise from

238 the application of learning theory to horse training [64].On the other hand, one common issue is

239 distress produced by an uncomfortable sensation. In order to avoid it, the animal would

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240 consciously develop some compensatory movements and/or positions that would alter its

241 symmetry and general conformation, hence affecting its sport performance [65].

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243 4.2. Temperament and behaviour

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244 To attain optimal individual performance within any equestrian discipline, horses must be in

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245 peak physical fitness and be in the correct psychological state [26]. This last state comprises

246 factors that exist at three inter-related but separate levels: temperament, mood and emotional

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247 reaction [66], which can influence the interaction of the horse with its environment, hence

248 changing its predisposition to develop a stress response that could bias sport performance [67].

249
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Horse temperament is reported as a consistent predisposition of the horse, influenced by either
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250 genetics and early experience of the animal [68,69], whereas mood and emotional reaction

describe a more temporary state of mind that would bias the behavioural response of the animal
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252 in a certain environment at a certain moment. Hence, mood would basically influence the
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253 emotional reaction of the horse towards a novel and potentially stressful stimuli [70].
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254 McBride and Mills [26] reviewed the psychological factors that could influence sport

255 performance in horses by developing a stress response that could bias their performance, either
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256 improving or worsening horse results. The main findings focused on first, the need to ensure

257 optimal environmental conditions and second, to apply behavioural modification techniques in
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258 order to sufficiently motivate the animal to perform and to attenuate overly reactive behaviour
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259 either in anticipation of the competitive event, related to novel stimuli or in response to stimuli

260 that are a result of previous negative experiences. Furthermore, Young et al. [71] developed a

261 “handy” and easy to use physiologically validated scale of behavioural indicators of stress,

262 making it easier to recognize signs of stress in these animals. Hence, promoting and reinforcing

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263 the appropriate behavioural characteristics according to the discipline to be developed, would

264 improve the animal psychological adaptation to it, hence diminishing the level of distress

265 developed during training and performance. Horses can be trained to habituate to specific fear-

266 inducing situations, but this reduced fear response is not necessarily generalized to the wide

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267 range of potentially fearful stimuli encountered by sport horses ([99]) and there is a large genetic

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268 component to the fear reactions of sport horses ([86]).

269

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270 4.3. Genetics

271 From a genetic point of view, selecting for stress would imply altering the sensitivity of the

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animal itself to potentially stressful stimuli [73]. It has been widely implemented mainly for
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273 species bred in intensive systems like sheep [74,75], goats [76], dairy cattle [77,78], pigs [79,80]

and different poultry species [72,81]. This selection is for a better adaptation of the animal to its
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275 “human controlled” environment, hence minimizing the stress responses to effects such as heat
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276 stress, that could bias both animal welfare and animal production [3]. For sport horses,
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277 controlling the environment is not that simple as there are many different environments. Sport

278 events are organized per discipline, hence selecting for better-adapted horses to these
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279 environments is problematic. However, character traits such as fear, temperament or reactivity

280 may determine the sensitivity of the animal to novel environmental stimuli as they are the basic
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281 response of an individual to its environment [68,69]. Thus, selecting for less reactive/fearful
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282 animals would diminish their stress reaction to sport competitions [20,82], hence producing

283 calmer animals, with a proactive stress response rather with a reactive one, able to concentrate

284 more during the sport exercise and thereby enabling them to achieve higher scores. On the other

285 hand, despite the different studies that have been developed to assess the stress of the horse

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286 during sport competitions [6,26,83-87], none of them reported the genetic basis of the stress

287 response described. Recently, studies developed to find genes associated with stress due to sport

288 in horses are focused mainly on strenuous exercise, like exhaustive endurance races, as they may

289 have detrimental effects on the immune system, producing changes in the cellular composition of

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290 peripheral blood and inducing the expression of genes that appear to be related to the

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291 overtraining-syndrome [41,88,89]. Cappelli et al. [90] found six candidate genes involved in the

292 cellular stress response developed by athlete endurance horses during strenuous exercise and

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293 suggested that a constant and focused training regime could increase the baseline expression of

294 these genes preparing horses for acute stress. Capomaccio et al. [91], focused on the

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transcriptional landscape before and after physiological stress in equine athletes, revealing
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296 differential expression of numerous genes related to inflammation and immune system

activation, involving the regulation and activation of new and uncharacterized transcriptionally
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298 active regions. On the other hand, Tortonese et al. [92] reported rapid genetic adaptation of
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299 horses to photoperiodic changes that were not accompanied by an increase in the level of stress,
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300 but by an improvement of their physical capacity for athletic performance, or physiological

301 stress. These studies indicate that efforts could be made on developing a selection strategy within
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302 these animals in order to breed for reduced stress in sport horses. Table 2 includes a summary of

303 genes found in horses related to stress and temperament.

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304 A major factor affecting the stress response developed by a horse during a sport competition is
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305 the rider-horse connection within the exercise [49,87,88]. This effect has been studied

306 extensively and included in many genetic models for the genetic evaluation of sport performance

307 of different equestrian disciplines including dressage [93,94], show jumping [37,95,96], trotting

308 races [39,48,97,98], and eventing [100,101]. These studies highlight a key factor that could bias

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309 stress and hence sport performance, as a well-balanced rider-horse combination can result in

310 improved animal behaviour, thereby reducing the stress associated with the sport competition

311 and the possible accidents that it may cause [102,103].

312

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313 4.4. Health and reproductive ability

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314 Obtaining the maximum potential from a sport horse implies taking its physical abilities to the

315 limit, which sometimes could lead to suffering from subsequent injuries [1]. After injury, intense

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316 physical activity, or psychological strain [104], horses can develop a stress response, that is

317 probably more related to pain than with reactivity [105]. Considering that the degree of pain

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perceived depends not only on its intensity but also on the psychological state of the individual at
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319 the time of that painful stimuli [106], a sport horse that suffers a serious leg injury during the

excitement of a competition could keep competing despite its rider’s efforts to stop. This may be
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321 a stress-induced analgesia (SIA), which was described by Butler and Finn [107] as “an in-built
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322 mammalian pain suppression response that occurs during or following exposure to a stressful or
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323 fearful stimulus”. Another factor to consider is the discipline that the animal competes in, as it

324 will change the performance-limiting factors of a horse’s physiology that would hence determine
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325 the types of injuries associated with that discipline. Thus, race horses running at top speed are

326 probably limited by oxygen transport, so that any pathology that affects lung volume or tracheal
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327 diameter (like a.e. laryngeal hemiplegia [108]) will have important consequences for these horses
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328 that are performing at maximal intensity. However, the same pathology in dressage horses will

329 probably not limit the physiological capacity of the horse to perform its exercise, as it is not so

330 energy-demanding [109]. Yet these animals will suffer from different limb and muscle

331 pathologies, such as desmitis, suspensory branch injuries, degenerative joint diseases, synovitis

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332 or degenerative joint diseases, tenosynovitis of the digital flexor tendon sheath, primary or

333 secondary palmar cortical fatigue fractures and thoracolumbar and sacroiliac pain [110]. Three-

334 day event horses may be limited by their capacity to thermoregulate [109,111], endurance horses

335 by their capacity to maintain fluid and electrolyte homeostasis, with the majority of them

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336 suffering from injuries to soft tissues or joints, or from the result of direct trauma [110], whereas

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337 draft horses would be limited by the strength of their muscles [1]. Furthermore, it must be taken

338 into account that a traumatic experience (derived from a previous pathology or as a consequence

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339 of an accident during training or sport performance), may affect subsequent performance of the

340 animal, creating an anxious state of mind in the horse that leads to some stress that would affect

341
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its ability to compete at its highest levels. Hence, a horse may compete very successfully at
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342 intermediate level, but not have the confidence or the scope to compete at advanced level, such

as trying to avoid hitting fences (or other potential stressful stimuli) would not make the animal
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344 brave enough for advanced level competitions [109,111]. On the other hand, Sairanen et al. [113]
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345 found a negative influence of the stress suffered during races on mare’s fertility, although no
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346 genetic associations were found, suggesting an environmental basis for this fertility’s

347 impairment.
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348

349 4.5. Physiology

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350 As we have discussed above, any activity related to sport performance (training, competing,
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351 exercising, etc.) is likely to produce a change in homeostasis that leads to an acute stress

352 response. This response would produce different physiological changes that would require the

353 coordination of several systems, including the respiratory, cardiovascular, muscular,

354 integumentary, renal and hepatic systems and the gastrointestinal tract [114-116]. These changes

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355 include a series of endocrinal modifications, as when the animal experiences environmental or

356 internal stressors it responds by secreting a whole array of hormones to re-establish homeostatic

357 balance that can be divided into two phases: First, a catabolic phase, where a decreasing

358 tolerance to effort is produced and it is characterized by reversible biochemical, hormonal and

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359 immunological changes. Here, the sympathoadrenal and the HPA axis are activated, which is

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360 demonstrated by rapid increases in the circulating concentrations of ACTH, adrenaline,

361 noradrenaline, and cortisol [117]. Second, an anabolic phase follows, characterized by a higher

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362 adaptive capacity and enhanced performance capacity, where both the growth hormone-insulin-

363 like factor-I (GH-IGF-I) axis and the gonadal-axis are activated [8,118]. Finally, when

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homeostatic balance is not restored, the body experiences chronic stress which can induce
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365 chronic activation of the endocrine system [7].

The type of exercise that horses perform will also influence this endocrinal response, with
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367 disciplines like show jumping or eventing producing a higher increase in salivary cortisol
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368 concentrations in horses than dressage [85]. Whereas, resistance disciplines such as endurance
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369 produced an increase in plasma volume with an increased intravascular protein content

370 [119,120]. Thus, different disciplines will trigger different stress reactions according to these
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371 differences in the endocrine response.

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373 5. CONCLUSION AND RECOMMENDATIONS FOR FUTURE RESEARCH

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374 There are several ways in which stress can affect sport horse performance, whatever their

375 discipline. When accounting for the five main components considered necessary for a top sport

376 horse performer, stress could be either a result or the origin of an alteration in them.

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377 In order to consider how stress can affect the performance of sport horses, the potential avenues

378 for improvements include consideration of all the different factors reported in this study. Some

379 of them are already implemented by horse breeders, such as selecting animals with an adequate

380 conformation and making genetic selection by sport performance. These, imply a better

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381 adaptation of the animal to the sports conditions for their discipline. Another positive step has

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382 been the implementation of training and performing techniques that are less stressful for the

383 animals. On the other hand, a recommendation should be made to give horses the opportunity to

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384 adapt to potential stressful agents from the very beginning of the training sessions, so that they

385 progressively get used to those stimuli that they will have to face in the future during

386
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competitions (a.e. the noise of the audience, new floor conditions, etc.) so that there is a process
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387 of gradual familiarization..

As regards to temperament and genetics, there are two main areas to consider: first, by
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388

389 standardizing some “behaviour scales” veterinarians, breeders, riders and owners would be
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390 helped to recognize distress in their horses; and second, by selecting animals according to
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391 reactivity/fear to new stimuli within their discipline, their predisposition to develop distress in

392 certain specific circumstances in each type of competition would be reduced.

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393 As regards health and sport horse’s physiology, especial attention should be paid to the discipline

394 that the animal will participate in, as it will determine both the type of injuries suffered and the
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395 endocrine response developed during a physiological stress reaction. Hence, selection of the
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396 discipline according to our horse’s best physical and physiological predisposition or vice versa is

397 key.

398 Last, all these recommendations would also be influenced by other multiple environmental and

399 genetic factors, such as the discipline, the rider competing and the training of the animal, the

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400 horse’s breed and the selection strategy chosen for this breed within its Breeding Program,

401 changing the susceptibility of that animal to suffer from distress within equestrian competitions.

402 Thus, a broader selection strategy for breeding of sport horses that includes consideration of

403 stress responses and takes into account aspects such as conformation, temperament, genetics,

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404 health and physiology of the horse, together with an adequate control of the environment, is

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405 recommended to improve a horse’s welfare during equestrian competitions.

406

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407 6. ACKNOWLEDGEMENTS

408 This study was funded by a post-doctoral grant awarded to Dr. Bartolomé by the Junta de

409
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Andalucía (Spain), Resolution 28th of May of 2013 (Order 11th December 2007).
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410
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710 116. McKeever, K.H.; Hinchcliff KW. Neuroendocrine control of blood volume, blood

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718 Physiol 2000;88:1006–13.

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719 120. McKeever, K.H., Schurg, W.A., Jarrett, S.H., Convertino VA. Exercise training-induced
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720 hypervolemia in the horse. Med Sci Sport Exerc 1987;19:21–7.

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722 TABLES

723 Table 1. Summary of literature on the influence of stress on horses competing in different

724 disciplines.

Performance Type of influence on stress Reference

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component

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Head unnatural positions related to dressage Van Breda, 2006 [56]

that causes stress. Smiet et al., 2014 [57]

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Morphology McGreevy et al., 2012 [58]
Bridles developed to control the animal
Anon, 1990 [59]

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during exercise.
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Podhajsky, 1967 [60]

General influence of stress on sport

Dressage

General Strzelec et al., 2011 [85]

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performance

Influence of sport performance on fear

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Behaviour Von Borstel et al., 2010 [86]

reactions
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Limb and muscle pathologies that are a

Health limiting factor for sport performance, Dyson, 2002 [110]

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producing stress.
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Valera et al., 2012 [83]

General influence of stress on sport
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General Peeters et al., 2013 [84]

performance
Show Jumping

Strzelec et al., 2011 [85]

Influence of sport performance on fear

Behaviour Von Borstel et al., 2010 [86]
reactions

Physiology Salivary cortisol increases due to sport Strzelec et al., 2011 [85]

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performance.

General influence of stress on sport

General Strzelec et al., 2011 [85]
performance

Bayly e Foreman, 2004

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Thermoregulation problems that are a limiting
Eventing

Health [109]
factor for sport performance, producing stress.

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Hodgson et al., 1994 [34]

Salivary cortisol increases due to sport

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Physiology Strzelec et al., 2011 [85]
performance.

Geral General influence of stress on performance Alexander e Irvine, 1998 [6]

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Respiratory problems that are a limiting factor
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Health Hillidge, 1985 [108]
Races

for sport performance, producing stress.

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Reproductive
Stress during sport affects mare’s fertility Sairanen et al., 2011 [113]
ability
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Capelli et al., 2007 [41]

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Genes related to stress due to overtraining- Barrey et al., 2006 [88]

Genetics
syndrome Büttner et al., 2007 [89]
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Endurance

Cappelli et al., 2013 [90]

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Homeostasis problems that are a limiting

Health Dyson, 2002 [110]
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factor for sport performance, producing stress.

Plasma volume and intravascular protein Lindinger et al., 2000 [119]

Physiology
content increase due to sport performance. McKeever et al., 1987 [120]

725

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726 Table 2. Genes described in horses that are related to stress.

Gen Function and Discipline Reference

IL8: Interleukin 8.

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RBBP6: Retinoblastoma binding
Involved in exercise
protein 6 mRNA.
stress-induced response.
Capelli et al., 2007 [41]

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eIF4G3: Eukaryotic translation
Endurance horses.
initiation factor 4 gamma 3.

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Hsp90: Heat shock protein 90.

A larger number of down-regulated

genes were observed in the Group

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affected by stress. It is possible that
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some of these genes could be good RNA - transcription study Barrey et al., 2006 [88]

candidates to explain poor

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performances or some exercise

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pathologies.

CXCL22: Chemokine (C-X-C motif)

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1
ligand 2. Expressed on athletic

IL82: Interleukin 8 horses.

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IL1ẞ1: Interleukin 1 beta 2

Genes expressed during
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Capelli et al., 2013 [90]

1
IL1RII : Interleukin-1 receptor type II stress response after

IL181: Interleukin 18 (interferon- exercise.

gamma-inducing factor) Racing horses.

TLR41: Toll-like receptor 4

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CEBPẞ1,2: CCAAT/enhancer binding

protein (C/EBP), beta

Repeat-driven exonization may be a

stress response in the horse and

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Capomaccio et al., 2013
antisense transcription could be one of RNA - transcription study
[91]

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the main mechanism of transposon

regulation.

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727

728

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729 FIGURES

730 Figure 1. General diagram of the physiology of the stress response.

731

732

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1 HIGHLIGHTS

2 • Factors that make a horse a good sport performer can be influenced by stress

3 • Stress can bias the sporting ability of horses

4 • Stress responses are affected by the type of sporting activity/discipline

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5 • Horse temperament and behaviour affect stress responses and their sport performance

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6 • A strategy for breeding of sport horses should include consideration of stress

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