The effects of weaning on the domestic horse (Equus caballus)

Applied Animal Behaviour Science 110 (2008) 42–57 www.elsevier.com/locate/applanim

The effects of weaning on the domestic horse (Equus caballus) Natalie K. Waran *, Nancy Clarke, Mark Farnworth Animal Welfare Group, School of Natural Sciences, Unitec New Zealand, Carrington Road, Auckland, New Zealand Accepted 2 March 2007 Available online 9 May 2007

Abstract For free-living or feral horses weaning takes place naturally at around 8–9 months [Gill, E.L., 1988. Factors affecting body condition of New Forest Ponies. Ph.D. Thesis. Department of Biology, University of Southampton]. Some mares will continue to suckle their foal until shortly before the arrival of their next foal, gestation being approximately 342 days depending upon the breed of the horse [Ropiha, R.T., Mathews, G., Butterfield, R.M., 1969. The duration of pregnancy in Thoroughbred mares. Vet. Rec. 84, 552– 555]. Under domestic conditions, weaning tends to take place earlier, typically between 4 and 6 months of age. The weaning process has been identified as associated with potential psychological, physical and nutritional stressors that are of welfare concern. Following a review of the literature it is evident that there is a need for detailed research into what should constitute best practice with respect to foal and mare welfare. In addition, there is a need to understand the potential long-term impact of weaning on, for example, trainability and later maternal behaviour, and whether the stresses associated with early weaning have detrimental effects on the performance horse. There is also a lack of clear information concerning the most frequently observed weaning practices and the reasons why certain weaning methods are chosen. Some variables should be closely managed during weaning in order to minimise stress responses. These include: early creep feeding to familiarise the young animal with the food it will be exposed to during weaning, feeding a high fibre diet and keeping the animal in extensive conditions using a gradual approach to weaning. However, we conclude that there may not be one best method for weaning, since the chosen method must take into account a number of factors including: available resources, the housing environment, the individual foal’s stage of development, the strength of the mare–foal attachment, the foal’s ability to cope with changes in social conditions and the ability of the horse owner to implement the chosen method. We do however suggest that the fewest stress responses appear to occur where foals are weaned gradually and allowed to have social contact either with other foals or with older horses. # 2007 Elsevier B.V. All rights reserved. Keywords: Behaviour; Foal; Horse; Stress; Weaning; Welfare

* Corresponding author. Tel.: +64 9 815 4321. E-mail address: [email protected] (N.K. Waran). 0168-1591/$ – see front matter # 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.applanim.2007.03.024

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1. Introduction The feral horse is a non-territorial member of the family Equidae (Keiper, 1985) and in terms of the mother–young relationship, is often described as a follower species. Under natural conditions, it is thought that the mare becomes bonded to the foal shortly following parturition, whereas the foal begins to develop an attachment towards the mare more latterly within 2–3 days of birth (Tyler, 1972) and becomes largely responsible for maintaining physical proximity to the mare after 1 week of age (Carson and Wood-Gush, 1983; Crowell-Davis, 1986; Wolff and Hausberger, 1994). From 2 to 3 months of age, the degree to which the foal interacts with the mare declines and the percentage of time spent with other foals and yearlings increases (Tyler, 1972; Crowell-Davis, 1986). At weaning the primary social bonding occurs in kinship groups. Within peer groups, close and persistent pair bonds may develop between individuals, particularly between mares. Even after weaning has occurred the mare and foal retain an integral social bond and the foal will often remain in the natal group until sexual maturity (Tyler, 1972). Under domestic conditions, weaning has been identified as associated with potential psychological, physical and nutritional stressors. It is a time when the young foal experiences one or all of the following changes: maternal deprivation, social isolation, environmental and social change, more intense human intervention, abrupt nutritional challenges and further changes in both feeding and management practices (Nicol, 1999). Many or all of these factors are interdependent and have the potential to induce stress. For the domestic horse, weaning normally occurs between 4 and 6 months of age; the exact timing of weaning depending upon the physical maturity of the foal during the time weaning is considered, as well as its general health, condition and the preferences of the breeding establishment. There are a number of ways for managing weaning in the domestic situation and methods can be divided into variations of what are termed, abrupt and gradual weaning approaches. Typically, weaning involves an abrupt change in diet as well as the complete termination of the mother– young relationship. Often the mare and foal are placed in stalls or stables in complete visual, auditory and olfactory isolation from each other. Variations include the use of separate paddocks rather than enclosed stalls or stables, the complete removal of the mare from the premises or the complete isolation of the foal from all environmental and social stimuli for a period of days. A more gradual separation of the mare and foal may be employed by horse operations as an alternative to complete separation. Under this system the mare and foal are separated for a certain period of time each day. The length and number of separations are increased until finally the foal is never returned to the mare. Gradual weaning for single foals may also be achieved by placing the mare and foal in adjacent but separate areas which preclude suckling. This is suggested to cause less stress to the mare and foal than abrupt separation as it allows for physical contact and comfort but ensures the termination of milk feeding. It is suggested that this partial separation should continue for a few days whilst the foal learns to be more independent and the dam learns to be less protective. The obvious problems with this method include injury due to foals attempting to jump out of their area and into the area alongside their dam. Some weaning practices may be implemented to allow for maintenance of social bonds. These are used, where it is possible, to wean more than one foal simultaneously. The first system of ‘paired weaning’ involves separating pairs of weanlings from their dams simultaneously and together. The second uses as system of ‘‘interval weaning’’ (Holland et al., 1996) whereby the mares in a stable social unit of mares and foals on pasture are removed one by one over time, with the dams of the older foals being removed first. Using this method foals are able to remain in

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familiar surroundings with both similar-aged foals and familiar mares until the process is completed. There are however few controlled longitudinal studies that consider the impact weaning, under domestic conditions, has on long-term development and in particular the trainability of the horse nor have there been many studies reporting on the impact of the weaning process upon behavioural development of the horse in terms of its normal social responses, including future maternal behaviour. This review aims to bring together information from previous studies to help elucidate areas for future research and provide guidelines for best practice. 2. Behavioural effects of weaning Most research concerning the potentially stressful impact of weaning has focused on the potential effects of individual versus group weaning and abrupt versus gradual weaning upon the foal within non-pastoral production systems (Rogers et al., 2004). Irrespective of the weaning method used, vocal and locomotory responses to separation from the mare by the foal appear to be greatest in the first 30 min after weaning (McCall et al., 1985). Research examining potential sex differences between fillies and colts in terms of behavioural and physiological responses to both single and paired stall-weaning procedures indicate there to be no significant effect (Hoffman et al., 1995). Regardless of whether foals are weaned either singly or in pairs into stalls, behavioural responses to stress associated with the weaning procedure appear to decline over time (Hoffman et al., 1995). 2.1. Individual versus group weaning The short-term effects of both individual and group weaning procedures upon the foal have been examined by a number of researchers. Foals weaned singly vocalise and display locomotor behaviour significantly more frequently in comparison to foals that are placed in pairs following weaning (Houpt et al., 1984). Compared to single stall weaned foals, those weaned into stalls as established pairs, vocalise less but correspondingly engage in elevated levels of aggressive behaviour, indicated by flattening of the ears, biting and making threats to kick (Hoffman et al., 1995). Therefore, although the primary cause of stress to individually stall weaned foals is likely to be isolation, aggressive interactions between stall companions may prove to be the most stress-inducing factor for foals weaned into pairs (Hoffman et al., 1995). This may be unlike other domesticated hoof-stock, such as pigs, where increased aggression following weaning is likely to result from competition for food with unfamiliar pen-mates rather than separation from the dam per se (see Gonyou, 2001). It is possible that individually stalled foals may experience greater levels of stress post-weaning but not demonstrate obvious indicative changes in behaviour (such as higher levels of aggression) which would allow accurate cross comparison with pair weaned foals. As the study by Hoffman et al. (1995) only measured the foals’ behaviour for 2 weeks following weaning, further research is needed to assess the impact this may have on their long-term social behaviour development. In group-weaned foals, the social rank remains the same both pre and post artificial weaning (Araba and Crowell-Davis, 1994) which may be more similar to the natural situation. Group weaned foals have been found to associate preferentially with the foal of their dam’s most preferred conspecific both pre and post weaning where the mare is removed from the herd (Weeks et al., 2000). Therefore, careful consideration of the social hierarchy of the mares and foals living in a group is necessary to ensure that foals that are

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weaned into groups are matched appropriately with peers, which, in turn, may minimise the occurrence of inter-foal aggression post weaning. The long-term effects of individual versus group weaning have been researched to a lesser extent but can be examined differentially in terms of the foal’s social behaviour towards both humans and conspecifics. Research suggests that foals of more dominant mares have a higher predisposition to develop and then perform abnormal behaviour patterns later in life (Waters et al., 2002). Additionally, individually housed foals at weaning are deprived of contact with other horses, which could predispose them to impaired social and learning skills and the development of behavioural problems in later life. However, singly housed foals do appear to interact more readily with humans compared to foals that have access to other foals (Hughes et al., 2000; Søndergaard and Ladewig, 2004) which may be beneficial for later training, although this effect may not persist as the animals age (Søndergaard and Halekoh, 2003). Overall, the research indicates that compared to weaning foals into isolation, group weaning of foals is associated with a lower incidence of behavioural indicators of stress and, if combined with thoughtful group organisation to minimise aggression levels, may provide the equine industry with a more ‘welfare’ friendly weaning procedure. Greater consideration of the social group that each foal is to be weaned into could be used to buffer against the degree of stress associated with the individual foal’s experience of weaning. However, Ladewig et al. (2005) cited Williams (1974) in order to suggest that the absence of the mare can still have a significant enough effect on the foal’s development of social behaviour to override any mitigating influence that being raised in a group may serve. 2.2. Gradual versus abrupt weaning Where the impact of gradual group weaning has been studied in horses, allowing the foal to retain olfactory, visual and auditory access to the mare is concluded to impose less behavioural and physiological stress compared to that of abrupt weaning (McCall et al., 1987). Habituating the foal to separations through short-term mare–foal separations prior to weaning appears to have no effect on the subsequent behaviour or physiological responses of the mare or foal (Moons and Zanella, 2001) suggesting such procedures have little potential to reduce weaning related stress and serve to intensify maternal behaviour upon reunion with the foal post-separation (Moons et al., 2005). In reality, exposure to short separations prior to weaning has been found to intensify, and therefore sensitise the stress response as evidenced through the increase in salivary cortisol levels of foals experiencing weaning (Moons et al., 2005). One way to reduce this response may be to offer the foal an alternative attachment, such as the human handler. In fact the presence of a human handler in the foal’s stall during a short-term separation from the mare has been associated with significantly lower levels of both vocal and locomotory stress responses in the foal, as well as self-inflicted injuries. This practice may buffer against the stress associated with weaning and may also reduce the development of certain abnormal behaviours such as locomotor stereotypies in the long term (McGee and Smith, 2004). Relative to group weaning, Holland et al. (1996) compared the effect of abruptly removing all the mares from their foals at once, against removing one mare at a time. Although in this study, weaning evoked a significant behavioural response in both conditions, the abruptly group weaned foals appeared to have significantly elevated behavioural responses. However, research examining the impact of a single foal’s behavioural responses to weaning on the wider group of foals, and the potential welfare concerns, is also necessary. Ultimately, the existing research may not have included sufficient quantification of both behavioural and physiological responses to

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weaning in the foal, for a long enough period of time after weaning, to facilitate definite conclusions regarding the long-term effects of abrupt versus gradual weaning procedures upon foal welfare. 3. How important is mare–foal attachment in relation to weaning stress? The strength of the attachment and social bond between mother and foal may be measured through quantification of behaviours such as the frequency and duration of nursing bouts, mutual grooming, elements of normal maternal aggression and the prevalence of behaviour functioning to maintain proximity between mare and foal (Carson and Wood-Gush, 1983; Crowell-Davis and Weeks, 2005 in Mills and McDonnell, 2005). The degree to which mare and foal develop independence from one another appears not to be influenced by the foal’s gender (Crowell-Davis, 1985) but relates to the individual mare, her style of maternal behaviour (Crowell-Davis, 1986) and the foals attachment level (Carson and Wood-Gush, 1983). Mare–foal attachment behaviour of feral horses may not be comparable to that of the domestic horse in captive conditions. Selective breeding may have altered what would be considered to be ‘normal’ mare–foal attachment dynamics in the domestic horse. For example, the incidence of agonistic maternal behaviour and maternal rejection appears to be higher in captive domestic horses, with an evident breed bias among Arabian horses (Juarbe-Diaz et al., 1998). Studies have discussed the importance of ‘maternal imprinting’ where the mare, through visual, auditory and olfactory routes, identifies the foal as her own, and ‘maternal labelling’, when the mare licks and deposits salivary chemicals onto her foal, in mare–foal recognition (Wolski et al., 1980). These processes are thought to occur within the first 30 min following parturition (Crowell-Davis and Weeks, 2005 in Mills and McDonnell, 2005) and are part of the bonding of mare to the foal (Houpt, 2002). Under captive conditions, the foal’s attachment to the mare is not considered to be complete before the foal reaches 2 weeks of age, suggesting that formation of the foal’s bond with the mare is more dependent upon associative learning (Houpt, 2002). Artificial weaning enforces the cessation of the mare–foal relationship earlier and more rapidly than would occur naturally. This may have a long-term impact relating to the development of the foal’s social behaviour. Early work on infant rhesus monkeys has highlighted the importance of a mother figure in the development of ‘attachment’ related behaviour (Harlow, 1958). Such behaviour appears to be associated with the reciprocal activation of opiate systems within both mother and infant (Kalin et al., 1995). Stress responses in infants show high levels of variation dependent on the level of maternal attachment (Gunnar et al., 1981) and stress responses may be reduced by social facilitation with conspecifics (Gunnar et al., 1980). Underpinning ‘‘Attachment Theory’’ is the assertion that attachment to a primary caregiver figure is established during infancy through innate behavioural control systems and continues throughout an individual’s life (Bowlby, 1969). In a variety of species, separation of mother and infant induces simultaneous behavioural and physiological changes indicative of psychological stress in both parties which suggests there to be a reciprocal mother–infant attachment (Coe et al., 1978; Stanton and Levine, 1985; Ritchey and Hennesy, 1987). In examining the mare–foal attachment Houpt (2002) found that both mare and foal demonstrated higher levels of activity and vocalisation when separated, although the strength of mare–foal bond, and the apparent level of distress during periods of separation decreased as the foal’s age increased (Houpt, 2002). Henry et al. (2005) also highlighted the significance of the mare–foal bond in influencing the un-weaned foal’s behavioral reactions towards humans.

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Individual differences in both the foal’s temperament and strength of its attachment to the mare, and the mare’s reaction to the separation (Henry et al., 2005), could significantly influence the foal’s behavioural and physiological response to weaning. This highlights the importance of investigating the relationship between observable behaviours and the potential underlying emotional responses of both the mare and foal during and after the weaning process. The application of ‘Attachment Theory’ (Bowlby, 1969) to the mare–foal dyad may be one way forward for revealing quantitative insights into the impact the weaning experience could have on both the short and long-term behavioural development of the individual foal. The most appropriate weaning method for each individual mare–foal dyad could then be determined. 4. The physical effects of weaning Within a few weeks of birth most foals with access to extensive conditions begin to graze small amounts of forage although, until they are completely independent, they continue to receive most of their nutritional requirements from the dam (Ladewig et al., 2005). Due to the common practice of early weaning, the foal experiences the premature cessation of milk feeding (Price et al., 2003). If this process occurs early in development it is possible that the gut of the young horse is not fully matured and is therefore less able to cope with feed substitutes. Given the nature of the human–horse relationship there is surprisingly little data regarding the changes in morphology of the gut at weaning. Weaning is a significant period in the life of any domesticated species and generally occurs at a point when the animal is still growing rapidly and in need of significant nutritional input. The use of abrupt weaning methods has been shown to cause weight loss in various species such as rabbits (Bonanno et al., 2004) and lambs (Bimczok et al., 2005) which persists for a significant period of time. In the foal, weaning is associated with a significant, if often temporary, check in weight gain (Cuddeford, 1996) compared to foals that continue to be nursed (Cymbaluk and Laarveld, 1996) and this is irrespective of the method of weaning, with the first 10 days being cited as the most significant period of weight loss (Rogers et al., 2004). However, it is suggested that if weaning is carried out gradually it may reduce the period of weight loss associated with weaning for up to 10 weeks post-weaning (Price et al., 2003). Although in one study weight loss in foals after weaning was not associated with method of weaning there was considerable variation between individuals (Rogers et al., 2004). This may suggest that a foal’s ability to cope with weaning and nutritional change may not only be closely linked to the stress of weaning, but to the individual animal’s reactivity to the situation. This, in turn, may result from pre-weaning mare–foal attachments or stress reactivity and activation levels of the HPA axis. For example, Wolff and Hausberger (1994) established that there were significant inter-individual differences between foals, in relation to their maternal bonding and independence which may explain individual responses to weaning including differences in weight loss between foals. Diet changes not only lead to weight loss in foals but there is also a significant reduction in insulin growth factor I (IGF-I) between foals that are nursed by their mare and those that are fed replacer foods. IGF-I is required for optimal gut and somatic development (Cymbaluk and Laarveld, 1996). This difference in growth hormone was evident through weaning but was also found to persist for over a year following weaning. This certainly merits further investigation in relation to the different weaning methods that are currently employed. In terms of growth there are also significant negative effects on bone mineral content (BMC) if foals are weaned at 17 weeks, but not if weaned at 19 and 24 weeks. The causes of such changes

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have been associated with both housing and diet alteration at time of weaning (Reichmann et al., 2004). It is possible that such changes may be more related to housing practices, since foals kept in enclosed conditions may experience less exercise, causing a lowered BMC. This is supported by the evidence from one study where increases in calcium concentration in food did not appear to prevent a drop in BMC in adult horses being de-conditioned (not exercised) (Porr et al., 1998). Foals often begin to take small amounts of grass a few weeks after birth (Carson and WoodGush, 1983), and may take nutritional supplements if provided. Indeed Hoffman et al. (1995) found that the provision of concentrate before abrupt weaning may allow foals to better cope with weaning behaviourally and hormonally. Abrupt early weaning often includes a sudden change in diet. Such rapid changes in diet composition at weaning are shown to affect gut hypersensitivity in both piglets and calves (Dre´au and Lalle`s, 1999), although there are no specific studies of this in horses. It is however, known that soybean products can elicit allergic responses in the immature gut with pigs being especially vulnerable as they are relatively immature at weaning (Madec et al., 1998). Despite being hindgut fermenters it is possible that similar responses are seen in the gut of early weaned or orphaned foals as they progress from a predominantly liquid diet to grain based weanling diets. It is suggested, however, that the composition of diet at weaning may affect behavioural development. Nicol et al. (2005) found that foals fed a high fat and fibre diet were calmer immediately after weaning and generally more able to deal with a series of temperament tests compared to foals fed a starch and sugar diet. Little is known about effects on the immune system related to the early weaning of foals. Early weaning in rats has been associated with modification of the HPA axis and it has been noted that gradual separation reduced systemic levels of corticosterone, indicating an early and acute event may affect adult responses to stress (Cook, 1999). Indeed high levels of stress, particularly social stress, have been linked to immunosuppression in rats (Stefanski and Gru¨ner, 2006), which has implications for management practices regarding early weaning of foals. For foals, measures of cortisol taken 28h after weaning show a significant increase (Malinowski et al., 1990), with a subsequent decrease in immune response of foals weaned in pairs as opposed to those weaned singly or those who remained with the dam (Malinowski et al., 1990). Interestingly, this differs from the results reported by Holland et al. (1996) who, after finding there to be no rise in cortisol levels particular to weaning method, suggested that any effects related to weaning were mainly behavioural. The difference between the studies probably relates to differences in the methodology used in each study, including the severity of the weaning protocol as it was applied in practice to each of the foals, and the effect of individual responses to weaning, which means that larger sample sizes may be required to address this issue more thoroughly. It appears therefore that there is a need for more information concerning the impact of weaning on immune responses of individuals following different weaning protocols. 5. Weaning and the development of stereotypic behaviour in the foal Stereotypies are behaviours defined as ‘‘repetitive, relatively invariant sequences of behaviour with no obvious goal or function’’ (Mason, 1991) and level of stereotypy can be used as an indicator of an animal’s welfare (Broom and Johnson, 1993) or be characterised as a coping mechanism allowing the animal to deal with a sub-optimal environment (Waters et al., 2002; Cooper and Albentosa, 2005) although this has been disputed (Rushen, 1993). Whilst the causation of stereotypic behaviour is of great scientific interest, research continues to suggest the existence of an array of different factors that contribute to the development of such behaviours in a variety of different animal species. Interestingly, these abnormal behaviours have never been

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documented in feral horse populations (Tyler, 1972; Boy and Duncan, 1979; Duncan, 1980; Duncan, 1985). However, estimations of the prevalence of stereotypy and abnormal behaviours in the domestic horse have reported incidences ranging from 15% (Luescher et al., 1991) to 37.4% for all horses exhibiting any abnormal behaviour (Waters et al., 2002). More specifically up to 4.2% of domestic horses are reported to engage in crib-biting alone (Prince, 1994). Interdisciplinary estimates lie between 19.5% for endurance horses and 32.5% for dressage horses (McGreevy et al., 1995a). Equine stereotypic behaviour can be divided into two sub-categories with potentially distinct aetiologies, namely locomotive stereotypies and oral stereotypies. Research indicates that horses which already display one form of stereotypy, show a higher propensity to develop further related forms of stereotypic behaviour, although the risk of a horse engaging in oral and locomotor stereotypies may be independent of each other, where as the converse may be true for the two forms of locomotor stereotypy (Mills et al., 2002). Therefore, for the purposes of this review, research concerning the development of both oral and locomotor forms of stereotypic behaviour in relation to weaning is considered separately. General factors which are considered to be associated with the development of stereotypic behaviour include housing and management practices, particularly those that impact upon the performance of natural feeding and social behaviours (Nicol, 2000). For some time the potential influence of weaning on the development of stereotypies has been of particular concern (Kiley-Worthington, 1983, 1987). More recently, it has been suggested that within 1 month of weaning the majority of equine stereotypies may already be in the early stages of development (Nicol, 1999). 5.1. Oral stereotypies Oral stereotypies in the horse include crib-biting and wind-sucking and are often evident in stabled and domestic horses. Crib-biting and wind-sucking differ only in the fact that crib-biting is directed towards objects that are grasped with the incisors and wind-sucking is not (Nicol and Badnell-Waters, 2005). The development of abnormal behaviours in foals may occur prior to weaning but increases directly following weaning. Compared with those that do not, foals which develop abnormal oral behaviours after weaning spend more time suckling from the dam and twice as much time teat nuzzling (Nicol and Badnell-Waters, 2005). Thus, thwarting the foal’s performance of consummatory behaviours at weaning may lead to the development of oral stereotypies (Hughes and Duncan, 1988). In a 4-year prospective study Waters et al. (2002) established the incidence of crib-biting to be 10.5% in both Thoroughbred and part Thoroughbred horses by the median age of 20 weeks. It is thought that both crib-biting and wind-sucking may be closely linked with provision of a highly concentrated diet with little forage (Waters et al., 2002; Bachmann et al., 2003b) and may serve to increase the performance of crib-biting by a factor of four (McGreevy et al., 1995b). Such changes in diet are often to be seen at weaning and are accompanied by other stressors which may exacerbate the development of abnormal behaviours (Nicol, 1999). Oral stereotypies are often exhibited after the provision of a meal, which, it is suggested, compensates for low gut fill and reduced consummatory behaviour (Prince, 1994; Cooper and Albentosa, 2005). Cooper et al. (2005) found that increasing the frequency of meal provision served to reduce the level of oral stereotypies but not locomotory stereotypies. It also suggested that less frequent provision of food, such as occurs following weaning, may increase stomach acidity to levels where the horse

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may experience discomfort. As such the behaviours could develop to be a coping-mechanism to reduce the level of discomfort to the horse (Nicol and Badnell-Waters, 2005). It has been demonstrated that crib-biting foals showed a greater degree of ulceration and inflammation in their stomachs than foals which did not display abnormal oral behaviour (Nicol et al., 2002). This suggests that some foals may be particularly sensitive to the changes occurring at weaning, leading to gut discomfort and the development of abnormal oral activities as a possible coping mechanism. In adult horses the provision of an antacid diet not only improved the stomach condition of stereotyping horses but also led to a reduction in the behaviour (Mills and Macleod, 2002), lending further support to the theory that oral stereotypies are related to gut discomfort caused by diet changes incompatible with the physical needs of the horse. 5.2. Locomotor stereotypies Locomotor stereotypies are those which involve some form of locomotion, that is ‘voluntary movement of the entire body’ (McDonnell, 2003) or certain parts of it. The most commonly investigated forms of locomotor stereotypic behaviour are weaving and box walking (Nicol, 1999). Weaving is most typically performed over a stable door or even field gate, but can also take place anywhere within any form of equine enclosure. Although under-researched, the prevalence of weaving among adult horse populations equates to between 3% (Pell and McGreevy, 1999) and 9.5% (Zeitler-Feicht, 2004) and is more commonly performed by horses with lower levels of social contact (McGreevy et al., 1995b; Redbo et al., 1998). This may indicate that weaving arises as a result of social frustration. On the other hand box walking (McDonnell, 2003) may occur in the stable or in the field at a later stage of development. Box walking in adult horses occurs at a rate of between 2% (Pell and McGreevy, 1999) and 7% (Zeitler-Feicht, 2004), but is most common in horses used for endurance riding (McGreevy et al., 1995a). Studies have revealed a strong association between the type of housing, namely stable design, and the incidence of stereotypic behaviour in both adult and weanling horses. A higher incidence of locomotor stereotypic behaviour is strongly linked with housing where contact between neighbouring adult horses is minimised (McGreevy et al., 1995b). A more recent postal survey has identified certain management and housing factors that may serve to prevent against the development of stereotypic behaviour in adult horses. These include permitting inter-equine tactile contact, daily free movement within in paddocks or pastures and the provision of a high roughage diet that has a minimal concentrate component (Bachmann et al., 2003a). Heleski et al. (2002) examined the influence of housing and social environment on the behaviour of foals after weaning. Individually stall weaned foals were compared with foals weaned in groups of three into paddocks for 56 days post weaning. The paddock weaned foals’ behavioural time budgets were found to more closely resemble those of feral horses, compared to the individually stall weaned foals (Heleski et al., 2002). Although the paddock weaned foals spent significantly more time engaged in locomotory behaviours, individually stall weaned foals spent significantly more time engaged in seemingly abnormal locomotory behaviours, including stall kicking, pawing and bouts of rearing and bucking (Heleski et al., 2002). The interpretive value of this study in relation to paddock versus stall weaning is however problematic due to the mixing of both environmental and social variables in the design. However, in a 4-year longitudinal study, Waters et al. (2002) examined the effects of abrupt box weaning (where foals were isolated from other horses), abrupt barn weaning (where foals were kept in small groups), abrupt paddock weaning (where foals were kept in small groups which also included either one or two mares) and natural weaning. In accordance with the incidence of stereotypic behaviour in

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adult horses in relation to certain management and housing factors (McGreevy et al., 1995b; Bachmann et al., 2003a), foals that, post-weaning, were housed singly in stables or in groups in barns were more at risk of developing abnormal behaviour compared to those that kept in groups at grass or weaned naturally. Keeping foals at grass, as opposed to in barns, was identified as a key factor to be associated with a lower incidence of abnormal behaviour (Waters et al., 2002). In terms of specific locomotor stereotypic behaviour, weaving was evident in 4.6% of the foals by 15 months of age, whilst 2.3% of the foals engaged in box walking by 16 months of age (Waters et al., 2002). It could simply be that locomotory forms of stereotypic behaviour are more likely to develop as a response to weaning stress in individually stall weaned foals compared to groups of paddock reared foals because the latter have more opportunities to engage in more natural forms of locomotor activity. However, the impact of weaning on the development of both oral and locomotor stereotypic behaviour in young horses, and how these two sub-categories of behaviour may be linked requires further investigation. 6. The impact of weaning on the trainability of horses It is possible that the timing, as well as the frequency and amount of handling of the foal will influence responses to human handlers later in life. It is also highly probable that the age at which training starts influences the degree to which the trained behaviour is flexible later in life. For example, horses handled and trained from an early age, such as young thoroughbreds in the racing industry, are well habituated to many aspects of their environment. However, they are often considered to be more difficult to retrain to perform different patterns of behaviour later in life, than those initially trained at 4 or 5 years of age (Waran and Casey, 2005). This may, potentially, be a reflection of the type of early training rather than the age at which it takes place. Handling and training around weaning may therefore be advantageous in terms of strengthening the bond between human and horse at a time when the animal may be highly receptive to certain stimuli. However, it must be considered that any response of the foal may be mediated by the mare’s response to human approach pre-weaning (Henry et al., 2005). Intensive foal handling during the first 48 h of life, often called imprint training (Miller, 1998), may enhance the ability of the animal to perform behaviours required for performance later in life. There are only a few studies regarding the efficacy of this method on later trainability (Simpson, 2002; Williams et al., 2002) and in general these demonstrate that imprint training has no obvious benefits in terms of improved responses to situations and stimuli later in life. In addition there are questions regarding the possible negative impact such intensive handling could have on the young foal (see McGreevy, 2004). This does not necessarily mean that early handling may not be beneficial. It has been suggested that since the environment experienced by the young animal during the first months of life has considerable influence on adult behaviour (e.g. in dogs (Appleby et al., 2002)), the introduction of novelty, various handling regimes, management procedures and learning procedures during early training should be beneficial for improving the ability of the horse to learn and be trained when more physically mature. Being a social species it is likely that the horse has a need to learn about equine social behaviour during early life. In other social species (such as the dog), the socialisation period is identified as a time when the animal’s ability to learn about the components of its normal social environment and the basic aspects of social behaviour is particularly sensitive. It is suggested that there is also a similar period of enhanced socialisation and habituation in the horse, which affects trainability later in life, although there has so far been little systematic study in this area (Waran and Casey, 2005).

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Furthermore, no discernible research on the impact of weaning on the foal during any such sensitive period has taken place. Although it is not clear when the most sensitive period for socialisation may be, various studies have investigated with some success the efficacy of early handling at different developmental ages. For example Mal et al. (1994) demonstrated that handling throughout the first 42 days of life increased the success of halter training compared with handling later (43–84 days of age). Interestingly this is not supported by the results of studies by Visser et al. (2003) who found no difference in acceptance of early training when horses were handled at 5 months as compared with 3 years of age. The difference in these studies is likely to be due to the difference in the age when handling was started. Despite the potential for later training benefits, structured handling of foals around weaning has so far received very little scientific attention. Lansade et al. (2004) found that haltering, petting, picking up feet and leading foals immediately following weaning was related to less reactivity and increased ease of handling as compared with non-handled controls, with the effect lasting for up to 18 months following treatment. Interestingly they found that foals handled immediately after weaning showed stronger responses in terms of manageability than those foals handled 21 days following weaning. The authors suggest that the weaning period may be similar to the sensitive periods for learning found in other animals at early ages. They offer several reasons why this might be the case. One reason is that the stress induced by weaning serves to cause greater sensitivity to external stimuli (Bateson, 1979). This may manifest in so called ‘learned helplessness’ where the foal unable to control the consequences of abrupt separation, is less resistant to all external forces, and so more compliant when being handled. Another possibility is that attachment to the human as a surrogate (see Harlow, 1958) may have occurred. Studies of the impact of early handling do however appear to be contradictory, with some authors (e.g. Heird et al., 1981), suggesting that handling early in life (i.e. when the horse has been weaned at 8 months of age) increases learning success when tested later in life (i.e. at 14 months of age) whilst others (e.g. Visser et al., 2003) state that there is no difference in trainability in horses handled earlier rather than later in development. This may be due to differences between researchers in the criteria used to assess trainability. Structured handling at weaning (Heird et al., 1981) may positively affect the ability of the horse to perform better in learning studies later in life, but may have no impact upon trainability as measured by Visser et al. (2003). It is therefore not clear why there are differences between groups of horses handled at different stages of development, nor is it clear how frequently handling needs to be repeated during development and this is certainly an area for future study. 7. Discussion In summary, the factors that appear to influence the stress related to the period of weaning have been identified as falling into three main categories. The most obvious of these is the physical problems related to the responses of the young animal to the change in diet due to cessation of milk as the main nutritional source. These problems include: weight loss, growth depression, possible gut sensitivity and even bone growth. The second factor seems to involve responses to changes in the social environment due to maternal deprivation, frequent use of social isolation as part of the weaning process, inappropriate pairings with other foals or older animals, and placement in groups with unfamiliar individuals. The final factor involves the environment in which the animal is placed during the weaning phase and the effects that this has on the weanlings’ ability to perform certain behaviours. There are a number of environmental variables

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that may influence behaviour such as being placed in an indoor versus outdoor environment, amount of space and resources within the available space. Although there have been studies that have looked at some of the responses to each of the three factors as described above, there do not appear to have been large studies that look at the interrelationships between the factors and their long-term effects on the animals’ physical and mental development. In fact some researchers claim that the actual weaning technique employed has more of an impact on the behavioural development of the foal than the factor of the foal’s age at weaning (Waters et al., 2002) and this needs thorough examination. In addition although research appears to indicate that gradual interval weaning methods may cause fewer problems than abrupt weaning for the foal, it is not clear why this may be the case. It could be due to the importance of the social situation, or it could be due to the environment that tends to be most frequently used for interval weaning (usually outdoors). There is a need for more information regarding the relative importance of each aspect of the weaning experience to the individual. Although the behavioural responses of the foal to artificial weaning, such as the ‘whinnie’ vocalisation (Feist and McCullough, 1976) and increased locomotor behaviour (Mal et al., 1991) may be viewed as adaptive (Hoffman et al., 1995), in that they serve the function of re-establishing proximity between a separated mare and foal, their existence not only suggests artificial weaning to be a stressful experience (Apter and Householder, 1996) but also enables the quantification of weaning-related stress in the foal (Hoffman et al., 1995). Hence, the impact of the weaning process upon the behavioural and physiological development of the foal can be examined in terms of various factors such as age, how abruptly the foal is weaned (Holland et al., 1996), and whether the foal is weaned into isolation or into a group of conspecifics (Houpt et al., 1984; Hoffman et al., 1995; Heleski et al., 2002). Overall, the research concerning the potential impact of weaning upon the development of stereotypic behaviour in the foal does suggest that informed changes in feeding, housing and weaning practices could significantly lower the incidence of stereotypic behaviour developing in young horses. However, the impact that weaning and practices associated with weaning may have on the development of stereotypic behaviour in the foal does demand further investigation. As the performance of stereotypic behaviour may help an animal ‘cope’ with a stressful environment and is a welfare concern (McBride and Cuddeford, 2001; Waters et al., 2002) further research should aim to address the issue of how stereotypic behaviour should be managed in weanling foals within the horse industry. The dearth of information with respect to the potential long-term impact of weaning on for example, trainability and maternal behaviour, needs to be addressed if we are to be able to determine whether this early stress has detrimental long-term effects. There is also a lack of clear information concerning the most frequently observed weaning practices and what influences choice of weaning method. Attitudinal studies involving the equine industry in different parts of the world may provide information that could be useful for directing research and education of horse owners. 8. Conclusions In terms of current knowledge we can suggest that there is enough evidence to recommend that foals should be weaned into as natural an environment as possible with access to clean water and a high fibre (grass, hay or haylage) diet. Introducing young foals to the feed that they will be expected to consume following weaning (creep feed), should be started early prior to weaning and whilst with the dam. This buffers against neophobic responses and gut sensitivity that may

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