DANIEL S. MILLS, CLAIRE RICCI-BONOT, AND SOPHIE S. HALL

Animal Behaviour Cognition and Welfare Group, School of Life Sciences, University of Lincoln, Lincoln, UK

Equids fit a unique niche in their relationship with humans. In many contexts they are working animals kept for their utility and managed outside the immediate domestic environment; in this situation the mental health challenges facing them may be similar to those facing many farmed or production animals. But in other contexts, they are close companions with a strong emotional bond extended from their carers; in this situation the mental health challenges facing them may be similar to those facing companion animals. In either context, expectations of their role and potential are critical. Thus the World Health Organization’s (2014) definition of mental health as ‘a state of well-being in which every individual realizes his or her own potential, can cope with the normal stresses of life, can work productively and fruitfully, and is able to make a contribution to her or his community’ (emphasis added) is very easily transposed to the horse, with some clarification of some of the more anthropocentric features of the WHO definition. Accordingly, we suggest that, for the horse, mental health can be defined as ‘a state of well-being in which a horse can live in a way that does not compromise its potential performance, is able to cope with the inevitable stressors of its management and work so that it can fulfil an appropriate role; and for a horse involved in human-based activities this should be extended to include the ability to willingly participate in goal-based activities’. From this definition, we can identify several potential areas of physical and psychological threat to their mental health, namely:

However, it should be noted that the proposed definition also recognizes that there may be inevitable stressors, and so appropriate preventive measures may be as much about building the capacity of horses to cope with what is necessary as about avoidance of certain unnecessary activities. Central to this is a solid scientific understanding of not only what horses are capable of, but also their limitations; even when they may be able to cope, the effort required may come at some mental health cost. We therefore begin this chapter by considering the issues of coping and adaptation in relation to the cost they may impose, before reviewing specific types of challenges that should be of concern and how they might be addressed. We draw on the available scientific literature, but in places this may be lacking. In these cases we try to guide the reader on the basis of logical argument built on a compassionate interest in horses, giving them the benefit of the doubt when logic may indicate there are grounds for concern, rather than arguing, as some do, that the absence of scientific evidence means that all positions have equal merit or that the majority/popular view is necessarily the best view. Both of the latter positions have historically resulted in considerable suffering for horses.

17.1.1 Coping in the domestic environment and mental health

Coping implies that an animal is able to make the necessary changes in order to adapt and if a horse cannot cope, then it is clear that there is a problem. However, simply being seen to cope is not sufficient for good welfare or mental health. The effort required to adapt comes at a cost, and if this cannot be sustained then there is cause for concern as not only may the animal be unable to cope in the longer term, but the anticipated cost of trying to cope may compromise its mental health. This is because it is not just the nature of the challenge but also the individual’s evaluation of its ability to cope with that challenge (secondary appraisal, sensu Lazarus [1966]) which is an important component of the resulting emotional response (Folkman, 1984). The concept of secondary appraisal was originally developed within human psychology, but this does not make its consideration in other animals anthropomorphic since it is a general biological process that may exist at different psychological levels depending on the cognitive capacity of the species or individual concerned. Primary appraisal involves assessment of the type of challenge faced by an individual, while secondary appraisal involves evaluating what the individual can potentially do in order to adapt to this challenge and the extent to which it evaluates that this will succeed. An inability to identify an appropriate response to the challenge or a prediction that the effort needed is beyond the capacity of the individual in either the short term (e.g., response of excessive magnitude required, or response not possible due to current environmental constraints) or longer term (e.g., response required for longer than the animal predicts it can sustain) is likely to result in mental health problems. Inspired by Fraser et al. (1997), we elaborate three different types of circumstance that may lead to mental health issues in horses; namely:

17.1.2 Maladaptive versus malfunctional responses

Before elucidating these further in the second part of this chapter, we believe it is important to make an important distinction between the terms ‘maladaptive’ and ‘malfunctional’, which may be used in relation to coping strategies as it has important implications for both mental health and the nature of any additional interventions aimed at helping the animal. If a strategy is invoked on the basis of evolutionary rules of thumb then it is a functional strategy, but if it does not result in the animal coping well it has not fulfilled its adaptive role and so may be considered maladaptive (Mills, 2003). From a welfare and mental health perspective it can be expected that the animal will continue to perceive a need to try to adapt and so both mental health and welfare may be compromised. Accordingly, medication used in this context should not be seen as ‘correcting’ a mental pathology. The challenge faced by the animal still exists, and so the possibility that the intervention has simply suppressed the signs of failure to cope (e.g., through the nonspecific suppression of physiological arousal) also needs to be considered. Only if psychological arousal is reduced so the animal is no longer aware of the challenge will it improve welfare, but its effects on mental health still remain questionable, as the animal has not improved its intrinsic ability to cope with the situation. In a natural setting, animals typically have a lot of autonomy, whereas this is often reduced in captivity as boundaries are imposed by the animal’s keepers. Evolution has resulted largely in the development of strategies to deal with immediate rather than prolonged threats to well-being. Therefore, it is not surprising that another common type of threat to horse mental health comes not from the quality of the challenge, but rather its prolonged nature. This can result in organizational changes in brain micro-architecture (such as changes in neuronal sensitivity) which in the natural setting may be adaptive but are not helpful in the domestic setting. Again, we would argue that these are functional changes and not pathological.

In a limited number of contexts, such as in dementia-related conditions, coping fails because the strategy is not following the evolutionary rules of thumb, due to an organic lesion limiting normal regulatory processes (e.g., loss of neuronal function). In this situation the system may be considered both malfunctional and maladaptive. Treatments which restore both normal function and facilitate coping will improve both welfare and mental health. Accordingly, in contrast to the medical perspective of human psychiatry, we argue that few of the mental health issues affecting horses should be thought of as diseases or disorders. This difference in perspective should not be used to imply that they are any less important, only that the role of medicine (or veterinary medicine) is perhaps somewhat different to how it may sometimes be portrayed.

An example outside of mental health may help to illustrate this subtle but important difference between maladaptive versus malfunctioning processes. If a horse develops diarrhea because the gut is hyperperistaltic and reduces the normal transit time in order to eject an irritant, then the gut is still operating in a functional way, even if the horse becomes dehydrated for a while as a result. The gut is not diseased as such. However, if the lining of the gut is so damaged that it is unable to absorb water and diarrhea results, then this has arisen as a result of a malfunction of the gut. In both cases the horse has the signs of diarrhea, but in only one is there a pathology of the gut. The same can be said of mental states.

17.2 Evolutionarily Natural Challenges Impacting on Mental Health

17.2.1 Fears, frustrations, and anxieties

Fears are natural responses to perceived threats, whereas anxieties are anticipations of potential danger and thus involve a greater degree of uncertainty (Forkman et al., 2007). The natural adaptive response to a fear-eliciting stimulus is for the individual to protect itself, preferably by taking flight (for which the horse is well adapted) but also through self-defense if flight is not possible and the threat comes from a social source. A horse may also freeze in fear, especially if there is no clear escape from the situation. This may help to avoid attention from a threat like a predator and conserve resources until escape becomes either necessary or possible or the event passes. By contrast, when anxious the horse can be expected to engage in responses directed toward gathering more information in order to reduce the uncertainty of the situation. This often takes the form of behavioral inhibition (not to be confused with the complete immobility of fear) where the eyes, ears, and nose are used to discover more about the situation. Thus, the horse may snort, flick its ears, or move its head around to focus on various aspects of the environment.

The term anxiety is also popularly used to describe another situation that may arise in captivity, i.e., when an animal is uncertain about what it should do about a situation. However, this is related to motivational conflict and has a less reliable association with fear. Three forms of motivational conflict are generally recognized:

In these conflict situations, the animal typically engages in ambivalent behavior rather than behavioral inhibition (possibly alongside increased sensory activity). We suggest that other displacement behaviors may also occur at this time. These take the form of simple acts which may appear functionally unrelated to resolving the problem, but their expression may be important as they may serve to reduce the arousal arising from the failure to consummate the goal of the conflicting behaviors (Scopa et al., 2018). In the horse, common displacement behaviors seen in such situations include foot stamping, tail swishing, headshaking, the sudden ‘snatching’ of grass, and possibly flehmen (lip curling) (Górecka-Bruzda et al., 2015). Any of these conflicts may be misunderstood and misrepresented by horse-people as ‘stubbornness’ on the part of the horse and used to justify the use of physical punishments which can turn a minor conflict into an active avoidance (e.g., in the form of shying), which may result in a vicious cycle of handler punishment and more major mental health issues as the supportive bond with its primary carer breaks down. Through classical conditioning this may even result in problems with tacking up, as these are predictable preludes to the problems that occur under saddle. Thus, poor rider understanding of natural horse behavior and the inappropriate use of aversives are major sources of equine mental health concern. Therefore, riders should be educated that although undesirable from a riding perspective such behaviors may ultimately have a positive effect on the horse’s performance and displays of these behaviors should not be punished.

Different species are thought to have inherent predispositions to the type of stimuli that they find aversive (unconditioned fears), and horses are naturally neophobic (Leiner and Fendt, 2011). This may include some of the stimulus properties associated with predation or harm, such as sudden changes in movement around the horse or, given that its primary defense mechanism is based on flight, any circumstance that potentially limits this or the ability to detect such circumstances. Accordingly, horses may naturally avoid confined or dark spaces (especially if moving from a brightly lit area) or any action that may restrict their locomotion (foot or more general body restraint). Experience can shape anxiety and fear responses in both a positive and negative way. If an anxious horse is punished for hesitation when anxious, such as when loading into a trailer (a stimulus set that horses can be expected to naturally avoid – see Fig. 17.1), this will exacerbate the mental challenge. Likewise, fear may develop to novel or even benign stimuli through an association with punishment or pain (conditioned fears), including handlers who become frequently associated with the use of aversives. By the same measure, many simple fears can be resolved by associating them with positive experiences. In this regard, giving the horse time to resolve any conflict is as important as ensuring that there is a clear reward available for responding as we wish. These counterconditioning exercises are typically combined with desensitization, in which the fear evoking stimulus is presented according to an intensity gradient which seeks to avoid an intense avoidance response (Gough, 1997).

As a herd animal, social transmission of fear reactions may be expected to occur between individuals (Nicol, 1995), and so fear responses may arise within an individual even if it perceives no direct threat. However, the tendency for such emotional contagion may also be used to good effect to help reduce fear responses, with younger animals exhibiting a reduced response to a potentially anxiogenic stimulus in the presence of less reactive older ones (Rørvang and Christensen, 2018).

Rewards or relative rewards may also be used to help motivational conflicts by ensuring that there is a clearly preferable response. In the case of avoidance–avoidance conflict, there may need to be a focus on reducing the perceived aversiveness of one of the options outside of the problem situation, so that conflict does not arise in the future.

Aspects relating to rider positioning/style include the use of the bit, rein tension, and consistency. Misuse of the bit has been associated with behavioral signs of discomfort as well as physical damage (Cook, 2003). When pressure from a bit, applied through rein tension, is not appropriately released or ‘softened’, horses often display conflict behaviors, fear, and general body tension (Visser et al., 2009; Christensen et al., 2011), which they learn to avoid rather than habituate to. Horses are usually trained to associate changes in pressure with a behavioral response (e.g., increase pressure on the mouth to slow, increased pressure on their sides to move forward), removing the pressure (e.g., releasing rein contact) acts as a reinforcer, increasing the likelihood the response will occur again (McGreevy, 2007). If the pressure is not consistently reduced sometimes the horse will not be reinforced for displaying the rider-desired behavior, resulting in confusion for the horse, which may lead to unwanted ‘evasive’ behaviors.

Further misuse of the bit is seen in the delivery of inconsistent communication between the rider’s hand and leg, i.e., kicking and pulling, or ‘crank and yank’ as it is referred to. This conflicting signal is seen in riders across the disciplines (McLean, 2003), and again is likely to result in a confused horse which shows evasive, fearful, or ‘learned helplessness’ type behaviors.

In the wild state it would be unusual for fear-, anxiety-, and frustration-related problems not to be resolved relatively quickly by these actions, but that does not mean that they are not of concern. As mentioned previously, if the stimuli are particularly intense, frequent, or enduring they may threaten the animal’s mental health even if the immediate situation is resolved, as the animal may adapt by being more vigilant of danger. This then may take its toll over time as resources are diverted from other activities to maintain a heightened state of arousal (Forkman et al., 2007; Leiner and Fendt, 2011). If, however, the responses do not result in successful adaptation in terms of eliminating the stressor, then there may be other, less natural, consequences; these are considered in the section on novel domestic challenges (Section 17.4), since this is not the natural outcome.

17.2.2 Separation anxiety

Separation anxiety is the normal response of a dependant to prolonged separation from its carer (attachment figure) (Bowlby, 1973). While it can result in fear, anxiety, and frustration as the individual seeks to reinstate contact with its carer, its particular relationship with an attachment figure and dependent neurophysiological associations with opiate systems make it a special case for consideration (Panksepp, 1998). From a veterinary behavioral perspective, true separation anxiety is not just frustration or anxiety at being alone, but rather a specific aversion to the absence or loss of the attachment figure which results in a panic-like response (from an evolutionary perspective the loss of one’s mother is a life or death situation for a mammalian infant). Horses are a highly social species, i.e., show great mutual dependency, and we speculate, on the basis of clinical behavioral observations, that this probably means that similar bonds may have the potential to form with both humans who take on a care-giving role as well as members of the same species. Although there is a lack of academic research on this emotional process in horses, it has been noted anecdotally that it may be more common when the relationship with the handler is inconsistent, such as when intermittent punishment is used in training (McLean and McLean, 2008). This is in agreement with the human literature indicating that attachment problems arise as a result of a dysfunctional style of attachment rather than through over-attachment, which is commonly spoken about in relation to other species.

17.2.3 Pain

Although a review of chronic pain is outside the scope of this chapter, it is important to appreciate that it is both common in horses (Landman et al., 2004; Fonseca et al., 2006) and often goes unrecognized by owners (Lesimple et al., 2013). As with humans, chronic pain, and especially back pain, is often associated with a range of mental health issues including depression (Fureix et al., 2012) and increased aggressivity including toward humans (Fureix et al., 2010), as well as more subtle signs such as reduced attention to the environment (Rochais et al., 2016). If these problems remain unrecognized, it may result in inappropriate behavior by the owner toward the horse, as they may misrepresent these changes as stubbornness and resistance to perform the desired work. The use of punishment in an attempt to correct the perceived ‘problem’ can result in further mental health issues, associated with anxiety, etc., as described above. Behavioral indicators of chronic pain may not be very reliable, but increasing attention is being paid to the potential value of distinctive facial expressions (Dalla Costa et al., 2014; De Grauw and Van Loon, 2016).

17.3 Unmet Evolutionary Expectations Impacting on Mental Health

There are several potential challenges arising from the evolutionary mismatch between the biases created in the equine brain to aid survival in their natural habitat and the domestic environment of many horses (genome lag; Fraser et al., 1997). These typically arise from the well-intentioned and appropriate care provided by owners to ensure their basic needs are met.

17.3.1 Boredom

Boredom may be defined as a negative affective state associated with the interpretation of one’s environment as lacking interest, because it is highly predictable and controllable (Fureix and Meagher, 2015; Burn, 2017). It does not necessarily imply that there is a lack of stimulation, but that the stimulation which is available is perceived as irrelevant (Burn, 2017); in particular, the lack of unexpected positive reinforcement may be a cause for concern.

In the absence of varied stimulation, we suggest that animals may engage in exploratory tasks that may be problematic, such as wood chewing and walking around their restricted enclosure. With repetition, the changes that occur with complex movement become more predictable and so the behavior may become simpler in its form (Fentress and Gadbois, 2001), a process that appears to be facilitated by dopaminergic activity in striatal structures within the brain (Cools, 1992). This may lead to repetitive simplified behaviors such as box-walking, wood chewing, and possibly some other behaviors in the horse, which are often (and we suggest erroneously) referred to as compulsive disorders or stereotypies. Unlike these disorders, however, these repetitive behaviors are not associated with either a specific anxiety or frustration (see Section 17.4 for a discussion of these issues). This hypothesis deserves empirical evaluation, and it would be predicted that individuals expressing this form of repetitive behavior problem would not only live in an unstimulating environment, but also show increased apathy at other times, compared to the increased arousal associated with specific frustrations (discussed in the next section).

Owners often misunderstand the reason for repetitive behaviors and blame the horse, as is implied in the commonly used term ‘vice’ to describe them. This may then be used to justify attempts at resolution based either on suppression or punishment (Hothersall and Casey, 2012) (e.g., muzzles, or the use of shock collars [Houpt, 2018]), which may have their own mental health implications. However, these problems should be alleviated by simple environmental enrichment, which may take the form of a more visually complex physical environment (Cooper et al., 2000) or increased social contact (Yarnell et al., 2015). For example, increased paddock size has been shown to reduce the amount of time spent standing passively as well as increase foraging activity (Jørgensen and Bøe, 2007), and a diet of varied forage may in itself be enriching (Goodwin et al., 2002; Thorne et al., 2005). The role of stable toys is less straightforward, as while they may increase the diversity of activity, their effects may be varied if careful consideration is not given to what the goal of the enrichment is (Jørgensen et al., 2011). In this way, they may also introduce specific frustrations that increase problem behavior in a proportion of individuals (Henderson and Waran, 2001).

17.4 Novel Domestic Challenges Impacting on Mental Health

Whereas in the previous section we considered problems that may arise in the domestic situation as a result of evolutionary tendencies not being fulfilled, there are some specific novel challenges associated with the domestic environment for which it should not be expected that horses have evolved adaptive coping strategies. As a result, the horse’s behaviors may appear ‘stupid’ or ‘stubborn’ to those who do not appreciate that they are governed by the evolutionary rules of thumb that evolved in their wild ancestors, since there has not been selection in captivity for adaptation to these traits. Of particular note here are the consequences of insoluble problems for the horse, inconsistent communication by the rider toward the horse, and the absence of social support often found in the domestic environment.

17.4.1 Insoluble tasks

Insoluble tasks faced by the horse, in which it is the sole agent involved (i.e., those not involving humans or other horses), are quite common. For example, the horse kept in a stable, where it can see other horses but not interact with them, will likely be motivated to try to approach them, but it cannot do so due to the stable door. The horse’s brain is not geared to simply accept this situation and so this can lead to chronic frustration of locomotion directed toward exiting the stable, and it is believed that this can lead to the repetitive behavior commonly referred to as weaving (Mills, 2005). Horses are commonly relieved of this frustration on an occasional basis by being turned out, and this might explain why the problem is easily resolved by enrichment, which may simply distract the horse from the specific frustration, such as the provision of a stable mirror (McAfee et al., 2002; Mills and Davenport, 2002), or, at least in the short term, a simple poster of another horse (Mills and Riezebos, 2005). While these represent acute recurring frustrations, not all domestic frustrations are like this; some appear to be more persistent, for example, crib-biting. Crib-biting is associated with changes in dopaminergic sensitivity (McBride and Hemmings, 2005; Wickens and Heleski, 2010) which are not apparent in weaving horses. Blinking may be used as a simple behavioral correlate of dopaminergic activity (Lethbridge et al., 2007). Interestingly, an extension of the latter study demonstrated that, when compared to carefully matched controls, horses who weave were found not to differ significantly in their blink rate whereas horses who crib-bite blink significantly more frequently (Fig. 17.2). This would suggest that the repetitive behavior associated with cribbing, but not weaving, is more like the stereotypies described in human mental health conditions such as schizophrenia, hyperactivity disorder, and autism, as well as stereotypies induced with dopaminergic agents in the laboratory (Jongkees and Colzato, 2016). The exact etiology of this change remains uncertain, but frustration of a high level of forage-based feeding is a consistent finding (Wickens and Heleski, 2010), suggesting that the change may occur as a result of the persistent failure to meet some physiological need associated with trickle feeding in the horse.

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