(Re)training & Behaviour Modification for Horses with a History of Chronic Stress
Review Article, by: Mila Bon, Nov. 2012.
1 Introduction
Horses that have been exposed to chronic stress (i.e. they come from a place of abuse and/or neglect, have endured chronic pain, or less obvious, former race horses, riding school horses or show horses that ended up at a horse rescue) may show a wide range of ‘problem’ behaviours that, depending on the level and duration of their prior situation can be quite persistent, unexpected, misplaced, redirected, intensified and above all, dangerous. For these horses it is often difficult to assess their physical health properly, as for animals previously exposed to chronic stress, subsequent exposure to mild acute aversive stimuli (like physical pressure during examination) will produce a heightened stress response (O’Connor, 2004). It is therefore important, not only for the health and future of the horse itself, but also for the safety of the handlers, caretakers and equine professionals, that behaviour modification is part of the rehabilitation process. Much research has been conducted about equine behaviour, ethology and learning theory. Slowly but surely this knowledge is trickling down to the individual horse owner. However, many horses that have been ‘rescued’ and offered a second chance still struggle with their new situation and so do their new owners who might resort to punishment of ‘misbehaving’ stressed horse. This review will bring more clarity about the long lasting behaviour and welfare implications of chronic stress on horses as well as offer insight on how the brain could be affected, so this knowledge can be used to design a specific behaviour modification program.
2 What is Stress?
Stress is anything that disrupts the homeostatic balance of an organism (the concept of homeostasis was developed in 1932 by Walter Cannon and describes the need of the body to maintain a relatively constant internal environment). Injury, illness, pain, fear, hunger, thirst and environmental factors can all put an organism under stress, but also feeding practises, handling, training, transport, performing, weaning, deprivation of free movement, social deprivation, social incompatibleness with herd mates, neglect, abuse, cruelty, just to name some factors that often result in a horse becoming stressed. Stress is the natural response of the body in overcoming adverse situations. It can be defined as a “Natural Adaptation Syndrome” and is always the same, no matter if the stressor is physical, physiological, psychological, chemical or social (Selye, 1955). Physiological data and particularly the evaluation of the activity of the Hypothalamic-Pituitary-Adrenal (HPA)-axis are a standard approach to estimate stress and welfare in farm animals (Hausberger et al., 2012). The body reacts to stress with the activation of the (HPA)-axis which leads to variation in serum cortisol levels, which are secreted in order to restore the homeostatic balance after which the body will try to adapt to the stressor. If no adequate time is given to the body to adapt to the stressor and exposure happens again, overcompensation will take place and stress is increased (Selye, 1955).
3 Identifying Stress
A scale of behavioural indicators of stress for use with domestic horses, developed by Young et al. (2012) offers a rapid reliable tool without invasive physiological measures Principal component analysis (PCA) of behavioural and physiological data of various breeds of mares and geldings kept in similar management routines at 4 different locations were the basis for the scale that was further developed by a professional panel. Although in chapter 1 of the book “The Biology of Animal Stress” by Moberg and Mench (2000), Moberg warns that the stress response is a cascade of biological events, the nature of which may vary between animals and relying on one, or even two, of these biological defence responses to measure stress is not a reliable approach.
3.1 Acute Short Term Stress
Stress can be seen as neutral, during which learning is enhanced, negative, during which there is no stress, or positive, during which the body is overcompensating due to insufficient time lapse between the onset of the stress and the adaptation to the stress of the body (De Graaf Roelsema, 2007). Active emotional coping is a characteristic of acute short term stress (McGreevy and McLean, 2010). Acute stress manifests hyper-reactively as conflict behaviours ranging from increased muscle tonus and body tension to aggression, bolting, rearing, bucking, shying and freezing (McLean and McGreevy, 2004). Restraint, transportation or isolation are forms of acute stressors that may disturb biological events that rely on critical timing for success (for instance ovulation). The catecholamines (hormones produced by the adrenal glands) secreted during stress convert the glycogen to readily utilizable glucose or other metabolic products required for gluconeogenesis (for more insight, see interactive animations at Concepts in Biochemistry). Once the stressor is alleviated, the glycogen stores are quickly replenished by gluconeogenesis (helps to keep blood glucose levels within critical limits) to pre-stress levels. Acute stress is usually considered to be a relatively brief exposure to a single stressor, although the biological cost of a single stressor may be of sufficient magnitude to alter biological functions and induce distress. When there are inadequate biological resources in reserve to meet this challenge, resources must be diverted away from other biological functions in order to cope (Moberg and Mench, 2000). Low levels of stress can be positive as raised attention and awareness provide optimal learning conditions (Moberg and Mench, 2000), but only up to a certain point, after which the stress will become inhibiting, according to Yerkes-Dodson’s Law, (1908) which is considered valid (Moberg and Mench, 2000), although it has to be noted that the arousal theory emerged several decades later according to Winton (1987).
Yerkes-Dodson’s Law, (1908). “As difficultness of visual discrimination increases that strength of electrical stimulus which is most favourable to habit-formation approaches the threshold. The easier the habit the stronger that stimulus which most quickly forces its acquisition; the more difficult the habit the weaker that stimulus which most quickly forces its acquisition.”
3.2 Chronic Stress
Exposure to chronic variable stress (or even a single exposure to an acute stressor, like for instance inescapable tail shock) results in changes in basal corticosterone (CORT) levels that alter the responses of the HPA-axis function which then increases the release of CORT while the regulating systems (negative feedback to stop the production of CORT) are either not working or inadequate, resulting in exaggerated stress responses and these may remain persistent for a long period of time (O’Connor, 2004). An animal experiencing repeated exposure to stressors, without any opportunity to replenish its biological resources, could accumulate sufficient biological cost to affect other biological functions. The result of this accumulated biological cost would be a state of distress (Moberg and Mench, 2000). Unpleasant experiences /discomfort/pain produces negative affect that automatically stimulates aggressive thoughts, emotionally and behavioural tendencies linked in memory (CNT –Cognitive Neo-association Theory), thus cues present during an averse event become associated with the event and with the cognitive and emotional responses triggered (Fureix et al., 2010).This indicates that it is not deemed uncommon for chronically stressed animals to be aggressive towards humans. However, when highly aversive stimuli are totally inescapable, learned helplessness will set in and the horse will no longer try to cope, it will simply give up and become dull. Learned helplessness will result in deterioration of cognitive, emotional and motivational attributes and neurosis may develop (McGreevy and McClean, 2009). According to Hausberger et al. (2012) the frequency of adult play in riding school horses correlates with a global scoring of chronic stress. Frequency of play also correlates with aggressiveness towards humans and oxidative stress values. In their study on the significance of adult play it showed that the ‘players’ in the study appeared more withdrawn from environmental stimuli when in their box, had more vertebral disorders and higher oxidative stress values. They concluded that adult play in horses links to poor horse welfare. In the study “Towards an Ethological Animal Model of Depression? A Study on Horses” by Fureix et al., (2012) similar findings showed that the observed horses that showed an expression of “behavioural despair” characterized by a withdrawn posture (with gaze, head and ear fixity) while in their home environment, reacted more emotionally in challenging situations. Withdrawn posture is different from resting pos ture as a straight line could be drawn from the poll to the withers where the angle nape-withers-back is 180º and the neck is not arched (standing with eyes open, stretched neck, similar height between neck and back, no ear movement, no visible eye movement). The withdrawn horses also showed a lower response in tactile stimuli. Fureix et al., 2012 concluded that horse “depression” corresponds to a multifaceted syndrome: apathy and loss of interest, lower reactivity but higher anxiety. The lower cortisol levels are partly in agreement with horses submitted to stress-inducing management conditions, although lower cortisol levels are not considered a reliable biomarker for some authors. Descriptions of “apathetic” horses all correspond to social, spatial and/or feeding restrictions as well as stress-inducing work and negative experiences linked to training, but the results of this study suggested genetic inputs as well.
4 Laterality, Lateral Vision and the 2 Hemispheres
4.1 The 2 Hemispheres
As with all vertebrates, the left hemisphere of the brain of the horse controls most of the right side of its body and the right hemisphere controls most of the left side of its body. However, the brain function is asymmetrical, as the right hemisphere is concerned with expression of emotion and control of quick responses, while the left hemisphere controls well established patterns of behaviour in non-stressful situations. In short: The left hemisphere controls proactive behaviour and the right controls reactive behaviour (Rogers, 2010).
4.2 Lateral Vision
Input from the left eye is processed by the right hemisphere and therefore horses might respond more fearful, or more aggressive when observing a novel stimulus from the left. When observing a novel stimulus from the right, the horse might be much more inquisitive, as input from the right eye is processed by the left hemisphere. Horses only have a small area of binocular vision, but a study on stimulus detection and discrimination showed that horses have a good lateral vision due to the presence of a visual streak and only have a hard time discriminating between objects that appear towards the rear (Hanggi, 2012). Line of sight restrictions (i.e. blinders, short reins, hyperflexion) in order to prevent a flight response may lead to greater stress as the horse will not be able to identify objects in its environment (Hanggi, 2012).
4.3 Lateralility
Laterality (left or right sidedness) is widely observed in vertebrates. Most horses prefer to stand with the left forelimb extended in advance of the right when grazing (McGreevy, 2005). Asymmetry of left and right hemisphere is prevalent in flight responses. Horses exposed to an averse novel stimulus on the left side respond with the right hemisphere and the flight distance measured was greater than a novel averse stimulus on the right side. Austin, (2007) hypothesized that if horses are less reactive to novelty on the right, they might learn faster and will be more relaxed if they were handled from the right.
4.4 The Influence of Stress on Behavioural Lateralisation
When the horse experiences a balanced existence, the two hemispheres compliment each other and can process information simultaneously, although the environment and/or breed difference may cause a slight dominance in either left or right hemisphere. However, an animal suffering from stress would rely on processing with the right hemisphere and chronic stress may maintain the dominance of processing by the right hemisphere (Rogers, 2010).
5 The Influence of Breed Difference
The ‘Horse Personality Questionnaire’ by Lloyd et al., (2007), used six components to describe horse personality: dominance, anxiousness, excitability, protection, sociability and inquisitiveness. Anxiousness and excitability showed the highest level of variation between breeds and these two components are linked with stress and anxiety (Lloyd et al., 2008; Mills et al., 2002). The Thoroughbred, Arabian and Welsh are significantly more anxious and excitable than Draft, Shetland, Highland, Appaloosa and Quarter Horse breeds, according to this study. That this group stands apart from the rest is by no means a coincidence, as all 5 foundation stallions of the Thoroughbred were Arabians and Arabian stallions were at one point in time roaming free with the Welsh to improve the breed and at a later time there was an infusion of Thoroughbred and Arabian blood to create the Welsh section B, C and D (Swinney, 2006) who can all be traced back to the Darley Arabian, one of the Foundation Stallions of the Thoroughbred. The ancient Arabian horses were bred for hunting of gazelle, but mostly desert warfare, with surprise attacks and quick retreats as described in detail by Lady Anne Blunt in “Bedouin Tribes of the Euphrates” (1879). They needed to be highly reactive and have a heightened flight response. Selective breeding has tailored these behaviours even more so for the Thoroughbred as noted in McGreevy and Thomson (2006). Scoring lowest for anxiousness were Draft and Highland, lowest for excitability were Highland, Appaloosa and Shetland (Lloyd et al., 2007). Arabian, Thoroughbred and Welsh also scored highest in sociability, indicating that stress may be reduced by socialization and keeping paddock mates and pair bonds close by during training sessions.
6 Methods that May Reduce Stress
6.1 Massage
A preliminary study on the effect of massage (effleurage was used as technique) to reduce stress in the horse by McBride et al., (2004), resulted in the conclusion that massage may be used to induce a more relaxed, calm state in the horse and may be beneficial to both horse and handler under low to medium stressful situations. The most preferred sites of allogrooming are the wither, mid-neck and croup and these sites were found to have the most positive behavioural responses and the largest drop in heart rate during treatment. Post treatment the largest drop in heart rate were found massaging the wither, mid-neck, poll/ears and croup respectively, although massaging of the poll/ears resulted in the largest variation in behavioural responses (due to some horses that are not comfortable with their ears being touched). Allogrooming of the withers, mid-neck and croup appears to have a ‘reward’ element that allows massage to be stress reducing as low frequency stimulation of the spinal cord region activates peripheral nerve fibers which synapse within the dorsal horn of the spinal cord and so activate the spinal cord, brain stem and hypothalamus which results in opioids release (McBride et al., 2004).
6.2 Socialization
VanDierendonck and Spruijt, (2012) investigated the rewarding properties of endogenous opioids with social relationships. They concluded that allogrooming should be considered as an ethological need for horses over 1 year of age as it meets all the criteria: 1) Performed by all individuals; 2) Self rewarding; 3) Have a rebound effect; 4) In absence of a proper substrate could lead to chronic stress. However, socialization may increase stress when non-voluntary groups are not of ‘preferred’ composition, groups are too large (limited size promotes harmony; Fureix et al. 2012), of high density, presenting a single food source for multiple horses, or individuals do not have the necessary social skills. Research further showed that it was unlikely that there were relevant breed differences, stating that domestic horses will always show the need to socially interact (VanDierendonck and Spruijt, 2012), although Lloyd et al., (2007) indicated that there are (minimal) breed differences in sociability. Søndergaard et al. (2011) concluded that horses are highly motivated for social contact which was measured by operant conditioning.
6.3 Environmental Enrichment
Environmental enrichment (for instance housing conditions, from stall to pasture) may help shift the degree of negative cognitive bias more towards positive cognitive bias as a response to the change of conditions, although this hemispheric shift in dominance may take a long time (Rogers, 2010). Riding in an environment that is more complex than an arena, a well established social group, increasing the variety of forage provided and even artificial appliances (like horse toys) can provide suitable enrichment for the stabled horse. The aim of these methods is to create an environment that mimics the horse’s natural habitat and allows it to express its natural adaptive behaviours (McGreevy and McLean, 2010).
6.4 Slow movements, low voice from handler
By comparing horses’ responses to variation in human approach Birk et al. (2011) concluded that the style of approach had a significant effect on flight distance in naïve as well as experienced horses. The direct approach (vigorous, eye contact, swinging a lead rope) versus indirect approach (relaxed, no eye contact, lead rope held still) of an unknown human approaching one of six adult experienced riding horses resulted in a mean flight distance of respectively 6.87 m and 2.32 m. Human vocal sounds express emotion and rise in frequency and volume when we are scared or excited Saslow (2002).
6.5 Short training sessions, under quiet familiar conditions
Winther Christensen et al. (2012) concluded that the motivation of a horse to respond to environmental stimuli is greater than its motivation to respond to human signals and that fearfulness and stress may interfere with learning because prolonged high concentrations of glucocorticoids can impair both memory and learning skills. Even with relatively short training sessions (7 min./day) significant increase in performance was noted in day to day training sessions in this study of learning performance in horses. Winther Christensen et al. (2012) also concluded that stress sensitivity predicted impaired learning performance under stressful conditions.
6.6 Positive Reinforcement
An evaluation of positive and negative reinforcement for horses with a history of chronic stress Innes and McBride, (2008) implicated that horses trained with positive reinforcement (PR) were more motivated, exhibited more exploratory type behaviours and were more likely to attain the correct operant response than chronically stressed horses trained with negative reinforcement. The study showed that the horses trained with PR came closer to novel objects and the observer from week 4 onwards, indicating that PR horses habituated faster and may have altered perception of the human observer during the course of the 8 week trial.
7 Methods that May Increase Stress
7.1 Unfamiliar conspecifics or social deprivation
Several studies have indicated that mixing unfamiliar animals is a stressful event for all individuals involved and may result in changes in behaviour and physiology, e.g. elevated plasma corticosteroid levels (Hartman et al., 2009). Research concluded that horses pre-exposed to each other did not show reduced aggression, but did show reduced contact aggression and contact aggression may be predicted by bite threats while in neighbouring stalls. However, horses need access to full contact in order to establish relationships. (Hartman et al., 2009). As the test subjects in this study were only pre-exposed for 5 minutes, a longer pre-exposure period might have a slighter more favourable outcome, especially on horses already stressed. Horses housed in neighbouring stalls that are not compatible and show aggression towards each other or one sided aggression are also experiencing stress (McGreevy, 2004) as they are not able to remove themselves from the situation as would be possible in paddock or field. However, deprivation of socialization results in chronic stress and promotes stereotypic behaviour (VanDierendonck and Spruijt, 2012). This indicates that even though socialization can be stressful, it is still preferred over deprivation of social contact and thus for already stressed horses simply more care needs to be taken to socialize them with conspecifics.
7.2 Sudden movements, loud voice from handler
Saslow (2002) stresses the importance of understanding of the perceptual world of horses. One problem that can arise using the human voice for cueing is that human vocal sounds also express emotion and rise in frequency and volume when we are scared or excited (angry, upset) and it takes a lot of practise for humans to speak in a calm voice when they are in fact not calm. A brief high frequency sound can not be located by a horse and may trigger a flight response. The horses’ visual information is also different than that of the human and seems to be functioning better for warning than stimulus identification according to Saslow (2002).
7.3 Preventing escape
When animals can not evade pain or averse stimuli they become distressed. The horse will be more engaged and hyper-reactive when stress is escapable, but stress can be disguised as redirected aggression, displacement activities or passivity when escape is prevented (McGreevy, 2010).
7.4 Limited forage / Limited locomotion / Lack of Socialisation
When an animal cannot control its environment and when it cannot escape events it finds unpleasant, it often behaves in ways that suggest frustration. They become withdrawn from their environment and exhibit learned helplessness. The horse needs to be able to express most of its natural behaviours (McGreevy and McClean, 292 2010). This means forage, locomotion and socialisation.
7.5 Negative Reinforcement
In answer to the question if learning performance in horses relates to fearfulness, baseline stress hormone and social rank, Winther Christensen et al. (2012) found that negative reinforcement (NR) had a significant negative correlation between performance and heart rate (HR) in a novel environment (considered stressful). This was not the case for the horses trained with positive reinforcement (PR). An evaluation of positive and negative reinforcement for horses with a history of chronic stress (Innes and McBride, 2008) implicated that negative reinforcement (NR) has the potential to cause acute stress and therefore be an unproductive strategy of training for already stressed horses. Training techniques that employ NR through the application of physical pressure to animals previously exposed to chronic stress will produce heightened stress responses, even if the pressure is very mild. The study showed that the horses trained with NR remained more reactive and spent a higher percentage of time pawing with the fore foot during the 8 week trial period, but the results did not indicate that negative reinforcement overly compromised the animals’ welfare. This is a valuable determination as it is almost impossible to train a horse with only possible reinforcement while in the saddle.
8 Identifying Behavioural Patterns
Recent UK research in techniques to identify behavioural patterns stated that 82% of leisure horses have one or more behaviour problem, unrecognized by their owner as on their own they often have little effect on the horses’ performance or the horse-human relationship and therefore often overlooked. Individual horses have different ways to express themselves through their behaviour, but by using statistical techniques in identifying patterns in random behavioural problems it is possible to find the underlying cause and resolve this, instead of trying to change the resulting behaviour without addressing the cause (Hockenhull and Creighton, 2012).
9 Applying Learning Theory
McGreevy and McLean (2010) observed that passive emotional coping frequently characterizes chronic stress resulting in disengagement, decreased vigilance, hypo-reactivity and quiescence. The heart rate and blood pressure may lower and the horse frequently appears dull. In such situations, trainers may mistakenly believe that the horse is now more accepting of current events, but in reality it is a result of inescapable stress and lack of control. Conflicts in motivation are of great significance in any analysis of horse-training, because of the horse’s inability to resolve the stressful situation. Learning ability of a horse is profoundly influenced by emotionality, thus the aim of correct training in this case is to diminish all painful and uncomfortable interventions (McGreevy and McLean, 2010)
Ethological challenges include interventions that cause horses both social and environmental distress, like leaving the social group, taking the lead in company of established leaders, being close to aggressive conspecifics, traversing objects etc. and so overcoming horses’ innate responses and ignoring their preferences. With fearful horses round pen training can precipitate chronic stress if used to condition horses into constant states of hyper reactivity. Deceleration effect of the reins can lead to conflict behaviours and stress including bucking, shying and rearing (McGreevy and McLean, 2007). Horses that are unclear in their acceleration and deceleration responses show a positive correlation with hyper reactive and conflict behaviours (McLean, 2005), suggesting that re-training of basic responses must form part of the rehabilitation process. For optimal learning, unrealistic large incremental improvements must not be expected and shaping must use consecutive steps so that the horse is not overwhelmed (McGreevy and McLean, 2007).
10 Conclusion
(Re)training and behaviour modification for horses with a history of chronic stress may only be successful when the trainer/handler/owner is aware that physiological changes due to previous exposure to chronic stress may result in very persistent ‘abnormal’ behaviour being displayed long after (months or longer) the cause of the stress has been eliminated. Over the past 2 decades scientific research has shown that the way humans
have been training, treating and housing horses is not in line with their ethological needs resulting in many problem behaviours as well as health problems and wastage. As of yet this information has not resulted in many changes and it seems horse owners are very set in their ways and still need to be convinced that just because things have been done the same for hundreds of years, that does not mean it has been done right. British research by Hockenhull and Creighton, (2012) showed that 82% of leisure horses in the UK have one or more behavioural problems (and we have no reason to assume it would be any different in the rest of the western world). Add to that the current economical situation, the ban on horse slaughter in the US, aging demographic in the western horse industry with 25% over the age of 60 (according to the 2010 Equine Canada profile study), overproduction of un-broke young horses and it should not be a surprise that rescues are bursting at the seams with ‘problem’ horses. More knowledge is required to (re)train and rehabilitate a chronically stressed horse than horses that do not come with this baggage. The fact that so many horses end up with behavioural issues in the first place indicates that lack of knowledge lies at the root of this problem. The biggest hurdle that rescues have to face is a financial one, even more reason to try to educate their volunteers into knowledgeable ‘trainers’ that know how to assess and treat horses with a history of chronic stress, so that they will be adoptable within a reasonable timeframe. Love for, and patience with these horses are a good way to slowly gaining their trust, but knowledge of the difficulties that may arise due to their history is a must, as a stressed horse can kick faster than any human can get out of the way.
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http://resolver.scholarsportal.info.subzero.lib.uoguelph.ca/resolve/01681591/v78i2-4/209_utpwoh
Søndergaard, E., Bak Jensen, M, Nicol, C., 2011. Motivation for social contact in horses measured by operant conditioning. Applied Animal Behaviour Scence (July 2011), 132 (3-4), pg. 131-137.
Swinney, N.J., 2006. Horse Breeds of the World. Hamlyn, a division of Octopus Publishing Group Ltd., London, UK.Emilia Lobo Literature Review Advanced Equine Behaviour 2012-Nov-30 Page: 22 of 24
VanDierendonck, M., Spruijt, B., 2012. Coping in groups of domestic horses – Review from a social and neurobiological perspective. Applied Animal Behaviour Science 138 (2012) 194-202.
Young, T., Creighton, E., Smith, T., Hosie, C., 2012. A novel scale of behavioural indicators of stress for use with domestic horses. Applied Animal Behaviour Science (August 2012), 140 (1-2), pg. 33-43. Available at: http://resolver.scholarsportal.info.subzero.lib.uoguelph.ca/resolve/01681591/v140i1-2/33_ansobisfuwdh
Winther Christensen, J., Peerstrup Ahrendt, L., Lintrup, R., Gaillard, C., Palme, R., Malmkvist, J., 2012. Does learning performance in horses relate to fearfulness, baseline stress hormone and social rank? Applied Animal Behaviour Science 140 (2012) 44-52.
Winton, W., 1987. Do Introductory Textbooks Present the Yerkes-Dodson Law Correctly? American Psychologist, Vol 42(2), Feb 1987, 202-203.
Other sources:
2010 Canadian Equine Industry Profile Study Available at: http://equinecanada.ca/industry/index.php?option=com_content&view=section&id=103&Itemid=559&lang=en
Concepts In Biochemistry: http://www.wiley.com/college/boyer/0470003790/animations/gluconeogenesis/gluconeogenesis.htm
1 Introduction
Horses that have been exposed to chronic stress (i.e. they come from a place of abuse and/or neglect, have endured chronic pain, or less obvious, former race horses, riding school horses or show horses that ended up at a horse rescue) may show a wide range of ‘problem’ behaviours that, depending on the level and duration of their prior situation can be quite persistent, unexpected, misplaced, redirected, intensified and above all, dangerous. For these horses it is often difficult to assess their physical health properly, as for animals previously exposed to chronic stress, subsequent exposure to mild acute aversive stimuli (like physical pressure during examination) will produce a heightened stress response (O’Connor, 2004). It is therefore important, not only for the health and future of the horse itself, but also for the safety of the handlers, caretakers and equine professionals, that behaviour modification is part of the rehabilitation process. Much research has been conducted about equine behaviour, ethology and learning theory. Slowly but surely this knowledge is trickling down to the individual horse owner. However, many horses that have been ‘rescued’ and offered a second chance still struggle with their new situation and so do their new owners who might resort to punishment of ‘misbehaving’ stressed horse. This review will bring more clarity about the long lasting behaviour and welfare implications of chronic stress on horses as well as offer insight on how the brain could be affected, so this knowledge can be used to design a specific behaviour modification program.
2 What is Stress?
Stress is anything that disrupts the homeostatic balance of an organism (the concept of homeostasis was developed in 1932 by Walter Cannon and describes the need of the body to maintain a relatively constant internal environment). Injury, illness, pain, fear, hunger, thirst and environmental factors can all put an organism under stress, but also feeding practises, handling, training, transport, performing, weaning, deprivation of free movement, social deprivation, social incompatibleness with herd mates, neglect, abuse, cruelty, just to name some factors that often result in a horse becoming stressed. Stress is the natural response of the body in overcoming adverse situations. It can be defined as a “Natural Adaptation Syndrome” and is always the same, no matter if the stressor is physical, physiological, psychological, chemical or social (Selye, 1955). Physiological data and particularly the evaluation of the activity of the Hypothalamic-Pituitary-Adrenal (HPA)-axis are a standard approach to estimate stress and welfare in farm animals (Hausberger et al., 2012). The body reacts to stress with the activation of the (HPA)-axis which leads to variation in serum cortisol levels, which are secreted in order to restore the homeostatic balance after which the body will try to adapt to the stressor. If no adequate time is given to the body to adapt to the stressor and exposure happens again, overcompensation will take place and stress is increased (Selye, 1955).
3 Identifying Stress
A scale of behavioural indicators of stress for use with domestic horses, developed by Young et al. (2012) offers a rapid reliable tool without invasive physiological measures Principal component analysis (PCA) of behavioural and physiological data of various breeds of mares and geldings kept in similar management routines at 4 different locations were the basis for the scale that was further developed by a professional panel. Although in chapter 1 of the book “The Biology of Animal Stress” by Moberg and Mench (2000), Moberg warns that the stress response is a cascade of biological events, the nature of which may vary between animals and relying on one, or even two, of these biological defence responses to measure stress is not a reliable approach.
3.1 Acute Short Term Stress
Stress can be seen as neutral, during which learning is enhanced, negative, during which there is no stress, or positive, during which the body is overcompensating due to insufficient time lapse between the onset of the stress and the adaptation to the stress of the body (De Graaf Roelsema, 2007). Active emotional coping is a characteristic of acute short term stress (McGreevy and McLean, 2010). Acute stress manifests hyper-reactively as conflict behaviours ranging from increased muscle tonus and body tension to aggression, bolting, rearing, bucking, shying and freezing (McLean and McGreevy, 2004). Restraint, transportation or isolation are forms of acute stressors that may disturb biological events that rely on critical timing for success (for instance ovulation). The catecholamines (hormones produced by the adrenal glands) secreted during stress convert the glycogen to readily utilizable glucose or other metabolic products required for gluconeogenesis (for more insight, see interactive animations at Concepts in Biochemistry). Once the stressor is alleviated, the glycogen stores are quickly replenished by gluconeogenesis (helps to keep blood glucose levels within critical limits) to pre-stress levels. Acute stress is usually considered to be a relatively brief exposure to a single stressor, although the biological cost of a single stressor may be of sufficient magnitude to alter biological functions and induce distress. When there are inadequate biological resources in reserve to meet this challenge, resources must be diverted away from other biological functions in order to cope (Moberg and Mench, 2000). Low levels of stress can be positive as raised attention and awareness provide optimal learning conditions (Moberg and Mench, 2000), but only up to a certain point, after which the stress will become inhibiting, according to Yerkes-Dodson’s Law, (1908) which is considered valid (Moberg and Mench, 2000), although it has to be noted that the arousal theory emerged several decades later according to Winton (1987).
Yerkes-Dodson’s Law, (1908). “As difficultness of visual discrimination increases that strength of electrical stimulus which is most favourable to habit-formation approaches the threshold. The easier the habit the stronger that stimulus which most quickly forces its acquisition; the more difficult the habit the weaker that stimulus which most quickly forces its acquisition.”
3.2 Chronic Stress
Exposure to chronic variable stress (or even a single exposure to an acute stressor, like for instance inescapable tail shock) results in changes in basal corticosterone (CORT) levels that alter the responses of the HPA-axis function which then increases the release of CORT while the regulating systems (negative feedback to stop the production of CORT) are either not working or inadequate, resulting in exaggerated stress responses and these may remain persistent for a long period of time (O’Connor, 2004). An animal experiencing repeated exposure to stressors, without any opportunity to replenish its biological resources, could accumulate sufficient biological cost to affect other biological functions. The result of this accumulated biological cost would be a state of distress (Moberg and Mench, 2000). Unpleasant experiences /discomfort/pain produces negative affect that automatically stimulates aggressive thoughts, emotionally and behavioural tendencies linked in memory (CNT –Cognitive Neo-association Theory), thus cues present during an averse event become associated with the event and with the cognitive and emotional responses triggered (Fureix et al., 2010).This indicates that it is not deemed uncommon for chronically stressed animals to be aggressive towards humans. However, when highly aversive stimuli are totally inescapable, learned helplessness will set in and the horse will no longer try to cope, it will simply give up and become dull. Learned helplessness will result in deterioration of cognitive, emotional and motivational attributes and neurosis may develop (McGreevy and McClean, 2009). According to Hausberger et al. (2012) the frequency of adult play in riding school horses correlates with a global scoring of chronic stress. Frequency of play also correlates with aggressiveness towards humans and oxidative stress values. In their study on the significance of adult play it showed that the ‘players’ in the study appeared more withdrawn from environmental stimuli when in their box, had more vertebral disorders and higher oxidative stress values. They concluded that adult play in horses links to poor horse welfare. In the study “Towards an Ethological Animal Model of Depression? A Study on Horses” by Fureix et al., (2012) similar findings showed that the observed horses that showed an expression of “behavioural despair” characterized by a withdrawn posture (with gaze, head and ear fixity) while in their home environment, reacted more emotionally in challenging situations. Withdrawn posture is different from resting pos ture as a straight line could be drawn from the poll to the withers where the angle nape-withers-back is 180º and the neck is not arched (standing with eyes open, stretched neck, similar height between neck and back, no ear movement, no visible eye movement). The withdrawn horses also showed a lower response in tactile stimuli. Fureix et al., 2012 concluded that horse “depression” corresponds to a multifaceted syndrome: apathy and loss of interest, lower reactivity but higher anxiety. The lower cortisol levels are partly in agreement with horses submitted to stress-inducing management conditions, although lower cortisol levels are not considered a reliable biomarker for some authors. Descriptions of “apathetic” horses all correspond to social, spatial and/or feeding restrictions as well as stress-inducing work and negative experiences linked to training, but the results of this study suggested genetic inputs as well.
4 Laterality, Lateral Vision and the 2 Hemispheres
4.1 The 2 Hemispheres
As with all vertebrates, the left hemisphere of the brain of the horse controls most of the right side of its body and the right hemisphere controls most of the left side of its body. However, the brain function is asymmetrical, as the right hemisphere is concerned with expression of emotion and control of quick responses, while the left hemisphere controls well established patterns of behaviour in non-stressful situations. In short: The left hemisphere controls proactive behaviour and the right controls reactive behaviour (Rogers, 2010).
4.2 Lateral Vision
Input from the left eye is processed by the right hemisphere and therefore horses might respond more fearful, or more aggressive when observing a novel stimulus from the left. When observing a novel stimulus from the right, the horse might be much more inquisitive, as input from the right eye is processed by the left hemisphere. Horses only have a small area of binocular vision, but a study on stimulus detection and discrimination showed that horses have a good lateral vision due to the presence of a visual streak and only have a hard time discriminating between objects that appear towards the rear (Hanggi, 2012). Line of sight restrictions (i.e. blinders, short reins, hyperflexion) in order to prevent a flight response may lead to greater stress as the horse will not be able to identify objects in its environment (Hanggi, 2012).
4.3 Lateralility
Laterality (left or right sidedness) is widely observed in vertebrates. Most horses prefer to stand with the left forelimb extended in advance of the right when grazing (McGreevy, 2005). Asymmetry of left and right hemisphere is prevalent in flight responses. Horses exposed to an averse novel stimulus on the left side respond with the right hemisphere and the flight distance measured was greater than a novel averse stimulus on the right side. Austin, (2007) hypothesized that if horses are less reactive to novelty on the right, they might learn faster and will be more relaxed if they were handled from the right.
4.4 The Influence of Stress on Behavioural Lateralisation
When the horse experiences a balanced existence, the two hemispheres compliment each other and can process information simultaneously, although the environment and/or breed difference may cause a slight dominance in either left or right hemisphere. However, an animal suffering from stress would rely on processing with the right hemisphere and chronic stress may maintain the dominance of processing by the right hemisphere (Rogers, 2010).
5 The Influence of Breed Difference
The ‘Horse Personality Questionnaire’ by Lloyd et al., (2007), used six components to describe horse personality: dominance, anxiousness, excitability, protection, sociability and inquisitiveness. Anxiousness and excitability showed the highest level of variation between breeds and these two components are linked with stress and anxiety (Lloyd et al., 2008; Mills et al., 2002). The Thoroughbred, Arabian and Welsh are significantly more anxious and excitable than Draft, Shetland, Highland, Appaloosa and Quarter Horse breeds, according to this study. That this group stands apart from the rest is by no means a coincidence, as all 5 foundation stallions of the Thoroughbred were Arabians and Arabian stallions were at one point in time roaming free with the Welsh to improve the breed and at a later time there was an infusion of Thoroughbred and Arabian blood to create the Welsh section B, C and D (Swinney, 2006) who can all be traced back to the Darley Arabian, one of the Foundation Stallions of the Thoroughbred. The ancient Arabian horses were bred for hunting of gazelle, but mostly desert warfare, with surprise attacks and quick retreats as described in detail by Lady Anne Blunt in “Bedouin Tribes of the Euphrates” (1879). They needed to be highly reactive and have a heightened flight response. Selective breeding has tailored these behaviours even more so for the Thoroughbred as noted in McGreevy and Thomson (2006). Scoring lowest for anxiousness were Draft and Highland, lowest for excitability were Highland, Appaloosa and Shetland (Lloyd et al., 2007). Arabian, Thoroughbred and Welsh also scored highest in sociability, indicating that stress may be reduced by socialization and keeping paddock mates and pair bonds close by during training sessions.
6 Methods that May Reduce Stress
6.1 Massage
A preliminary study on the effect of massage (effleurage was used as technique) to reduce stress in the horse by McBride et al., (2004), resulted in the conclusion that massage may be used to induce a more relaxed, calm state in the horse and may be beneficial to both horse and handler under low to medium stressful situations. The most preferred sites of allogrooming are the wither, mid-neck and croup and these sites were found to have the most positive behavioural responses and the largest drop in heart rate during treatment. Post treatment the largest drop in heart rate were found massaging the wither, mid-neck, poll/ears and croup respectively, although massaging of the poll/ears resulted in the largest variation in behavioural responses (due to some horses that are not comfortable with their ears being touched). Allogrooming of the withers, mid-neck and croup appears to have a ‘reward’ element that allows massage to be stress reducing as low frequency stimulation of the spinal cord region activates peripheral nerve fibers which synapse within the dorsal horn of the spinal cord and so activate the spinal cord, brain stem and hypothalamus which results in opioids release (McBride et al., 2004).
6.2 Socialization
VanDierendonck and Spruijt, (2012) investigated the rewarding properties of endogenous opioids with social relationships. They concluded that allogrooming should be considered as an ethological need for horses over 1 year of age as it meets all the criteria: 1) Performed by all individuals; 2) Self rewarding; 3) Have a rebound effect; 4) In absence of a proper substrate could lead to chronic stress. However, socialization may increase stress when non-voluntary groups are not of ‘preferred’ composition, groups are too large (limited size promotes harmony; Fureix et al. 2012), of high density, presenting a single food source for multiple horses, or individuals do not have the necessary social skills. Research further showed that it was unlikely that there were relevant breed differences, stating that domestic horses will always show the need to socially interact (VanDierendonck and Spruijt, 2012), although Lloyd et al., (2007) indicated that there are (minimal) breed differences in sociability. Søndergaard et al. (2011) concluded that horses are highly motivated for social contact which was measured by operant conditioning.
6.3 Environmental Enrichment
Environmental enrichment (for instance housing conditions, from stall to pasture) may help shift the degree of negative cognitive bias more towards positive cognitive bias as a response to the change of conditions, although this hemispheric shift in dominance may take a long time (Rogers, 2010). Riding in an environment that is more complex than an arena, a well established social group, increasing the variety of forage provided and even artificial appliances (like horse toys) can provide suitable enrichment for the stabled horse. The aim of these methods is to create an environment that mimics the horse’s natural habitat and allows it to express its natural adaptive behaviours (McGreevy and McLean, 2010).
6.4 Slow movements, low voice from handler
By comparing horses’ responses to variation in human approach Birk et al. (2011) concluded that the style of approach had a significant effect on flight distance in naïve as well as experienced horses. The direct approach (vigorous, eye contact, swinging a lead rope) versus indirect approach (relaxed, no eye contact, lead rope held still) of an unknown human approaching one of six adult experienced riding horses resulted in a mean flight distance of respectively 6.87 m and 2.32 m. Human vocal sounds express emotion and rise in frequency and volume when we are scared or excited Saslow (2002).
6.5 Short training sessions, under quiet familiar conditions
Winther Christensen et al. (2012) concluded that the motivation of a horse to respond to environmental stimuli is greater than its motivation to respond to human signals and that fearfulness and stress may interfere with learning because prolonged high concentrations of glucocorticoids can impair both memory and learning skills. Even with relatively short training sessions (7 min./day) significant increase in performance was noted in day to day training sessions in this study of learning performance in horses. Winther Christensen et al. (2012) also concluded that stress sensitivity predicted impaired learning performance under stressful conditions.
6.6 Positive Reinforcement
An evaluation of positive and negative reinforcement for horses with a history of chronic stress Innes and McBride, (2008) implicated that horses trained with positive reinforcement (PR) were more motivated, exhibited more exploratory type behaviours and were more likely to attain the correct operant response than chronically stressed horses trained with negative reinforcement. The study showed that the horses trained with PR came closer to novel objects and the observer from week 4 onwards, indicating that PR horses habituated faster and may have altered perception of the human observer during the course of the 8 week trial.
7 Methods that May Increase Stress
7.1 Unfamiliar conspecifics or social deprivation
Several studies have indicated that mixing unfamiliar animals is a stressful event for all individuals involved and may result in changes in behaviour and physiology, e.g. elevated plasma corticosteroid levels (Hartman et al., 2009). Research concluded that horses pre-exposed to each other did not show reduced aggression, but did show reduced contact aggression and contact aggression may be predicted by bite threats while in neighbouring stalls. However, horses need access to full contact in order to establish relationships. (Hartman et al., 2009). As the test subjects in this study were only pre-exposed for 5 minutes, a longer pre-exposure period might have a slighter more favourable outcome, especially on horses already stressed. Horses housed in neighbouring stalls that are not compatible and show aggression towards each other or one sided aggression are also experiencing stress (McGreevy, 2004) as they are not able to remove themselves from the situation as would be possible in paddock or field. However, deprivation of socialization results in chronic stress and promotes stereotypic behaviour (VanDierendonck and Spruijt, 2012). This indicates that even though socialization can be stressful, it is still preferred over deprivation of social contact and thus for already stressed horses simply more care needs to be taken to socialize them with conspecifics.
7.2 Sudden movements, loud voice from handler
Saslow (2002) stresses the importance of understanding of the perceptual world of horses. One problem that can arise using the human voice for cueing is that human vocal sounds also express emotion and rise in frequency and volume when we are scared or excited (angry, upset) and it takes a lot of practise for humans to speak in a calm voice when they are in fact not calm. A brief high frequency sound can not be located by a horse and may trigger a flight response. The horses’ visual information is also different than that of the human and seems to be functioning better for warning than stimulus identification according to Saslow (2002).
7.3 Preventing escape
When animals can not evade pain or averse stimuli they become distressed. The horse will be more engaged and hyper-reactive when stress is escapable, but stress can be disguised as redirected aggression, displacement activities or passivity when escape is prevented (McGreevy, 2010).
7.4 Limited forage / Limited locomotion / Lack of Socialisation
When an animal cannot control its environment and when it cannot escape events it finds unpleasant, it often behaves in ways that suggest frustration. They become withdrawn from their environment and exhibit learned helplessness. The horse needs to be able to express most of its natural behaviours (McGreevy and McClean, 292 2010). This means forage, locomotion and socialisation.
7.5 Negative Reinforcement
In answer to the question if learning performance in horses relates to fearfulness, baseline stress hormone and social rank, Winther Christensen et al. (2012) found that negative reinforcement (NR) had a significant negative correlation between performance and heart rate (HR) in a novel environment (considered stressful). This was not the case for the horses trained with positive reinforcement (PR). An evaluation of positive and negative reinforcement for horses with a history of chronic stress (Innes and McBride, 2008) implicated that negative reinforcement (NR) has the potential to cause acute stress and therefore be an unproductive strategy of training for already stressed horses. Training techniques that employ NR through the application of physical pressure to animals previously exposed to chronic stress will produce heightened stress responses, even if the pressure is very mild. The study showed that the horses trained with NR remained more reactive and spent a higher percentage of time pawing with the fore foot during the 8 week trial period, but the results did not indicate that negative reinforcement overly compromised the animals’ welfare. This is a valuable determination as it is almost impossible to train a horse with only possible reinforcement while in the saddle.
8 Identifying Behavioural Patterns
Recent UK research in techniques to identify behavioural patterns stated that 82% of leisure horses have one or more behaviour problem, unrecognized by their owner as on their own they often have little effect on the horses’ performance or the horse-human relationship and therefore often overlooked. Individual horses have different ways to express themselves through their behaviour, but by using statistical techniques in identifying patterns in random behavioural problems it is possible to find the underlying cause and resolve this, instead of trying to change the resulting behaviour without addressing the cause (Hockenhull and Creighton, 2012).
9 Applying Learning Theory
McGreevy and McLean (2010) observed that passive emotional coping frequently characterizes chronic stress resulting in disengagement, decreased vigilance, hypo-reactivity and quiescence. The heart rate and blood pressure may lower and the horse frequently appears dull. In such situations, trainers may mistakenly believe that the horse is now more accepting of current events, but in reality it is a result of inescapable stress and lack of control. Conflicts in motivation are of great significance in any analysis of horse-training, because of the horse’s inability to resolve the stressful situation. Learning ability of a horse is profoundly influenced by emotionality, thus the aim of correct training in this case is to diminish all painful and uncomfortable interventions (McGreevy and McLean, 2010)
Ethological challenges include interventions that cause horses both social and environmental distress, like leaving the social group, taking the lead in company of established leaders, being close to aggressive conspecifics, traversing objects etc. and so overcoming horses’ innate responses and ignoring their preferences. With fearful horses round pen training can precipitate chronic stress if used to condition horses into constant states of hyper reactivity. Deceleration effect of the reins can lead to conflict behaviours and stress including bucking, shying and rearing (McGreevy and McLean, 2007). Horses that are unclear in their acceleration and deceleration responses show a positive correlation with hyper reactive and conflict behaviours (McLean, 2005), suggesting that re-training of basic responses must form part of the rehabilitation process. For optimal learning, unrealistic large incremental improvements must not be expected and shaping must use consecutive steps so that the horse is not overwhelmed (McGreevy and McLean, 2007).
10 Conclusion
(Re)training and behaviour modification for horses with a history of chronic stress may only be successful when the trainer/handler/owner is aware that physiological changes due to previous exposure to chronic stress may result in very persistent ‘abnormal’ behaviour being displayed long after (months or longer) the cause of the stress has been eliminated. Over the past 2 decades scientific research has shown that the way humans
have been training, treating and housing horses is not in line with their ethological needs resulting in many problem behaviours as well as health problems and wastage. As of yet this information has not resulted in many changes and it seems horse owners are very set in their ways and still need to be convinced that just because things have been done the same for hundreds of years, that does not mean it has been done right. British research by Hockenhull and Creighton, (2012) showed that 82% of leisure horses in the UK have one or more behavioural problems (and we have no reason to assume it would be any different in the rest of the western world). Add to that the current economical situation, the ban on horse slaughter in the US, aging demographic in the western horse industry with 25% over the age of 60 (according to the 2010 Equine Canada profile study), overproduction of un-broke young horses and it should not be a surprise that rescues are bursting at the seams with ‘problem’ horses. More knowledge is required to (re)train and rehabilitate a chronically stressed horse than horses that do not come with this baggage. The fact that so many horses end up with behavioural issues in the first place indicates that lack of knowledge lies at the root of this problem. The biggest hurdle that rescues have to face is a financial one, even more reason to try to educate their volunteers into knowledgeable ‘trainers’ that know how to assess and treat horses with a history of chronic stress, so that they will be adoptable within a reasonable timeframe. Love for, and patience with these horses are a good way to slowly gaining their trust, but knowledge of the difficulties that may arise due to their history is a must, as a stressed horse can kick faster than any human can get out of the way.
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