Prevalence and Factors Associated with Abnormal Behaviors in Chilean Racehorses: A Direct Observational Study

Prevalence and Factors Associated with Abnormal Behaviors in Chilean Racehorses: A Direct Observational Study

Journal of Equine Veterinary Science 33 (2013) 95-100 Journal of Equine Veterinary Science journal homepage: www.j-evs.com Original Research Preval...

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Journal of Equine Veterinary Science 33 (2013) 95-100

Journal of Equine Veterinary Science journal homepage: www.j-evs.com

Original Research

Prevalence and Factors Associated with Abnormal Behaviors in Chilean Racehorses: A Direct Observational Study Tamara Tadich MSc a, b , Constanza Weber MV b, Christine J. Nicol DPhil c a

Becario CONICYT, Programa Doctorado en Ciencias Veterinarias, Facultad de Ciencias Veterinarias, Universidad Austral de Chile, Valdivia, Chile Instituto de Ciencia Animal, Facultad de Ciencias Veterinarias, Universidad Austral de Chile, Valdivia, Chile c Centre for Behavioural Biology, University of Bristol, Langford, Bristol, UK b

a r t i c l e i n f o

a b s t r a c t

Article history: Received 7 March 2012 Received in revised form 13 May 2012 Accepted 23 May 2012 Available online 11 July 2012

Stereotypies are considered a cause and symptom of impaired welfare, and have been associated with suboptimal husbandry systems. The aim of this study was to estimate the prevalence of stereotypic and other abnormal behaviors in Chilean thoroughbreds by direct observation, and examine their associations with biological characteristics and management practices. Seven hundred forty-three racehorses were observed directly, every 5 minutes during 1 hour before and after feeding, to identify behavioral disorders. A questionnaire was administered to handlers to obtain information about the animal and husbandry practices. The total observed prevalence rate of horses with one or more abnormal behavior was 11.03%. The total observed prevalence rates of stereotypies and abnormal behaviors were 6.32% and 5.52%, respectively. Horses at racetrack B presented more abnormal behaviors than those at racetrack A (P ¼ .0092), and specifically, the prevalence of the oral group was higher (P ¼ .0013). Mares presented a higher percentage of stereotypies (P ¼ .0014), and the use of wood shaving bedding was positively associated with abnormal oral behaviors (P ¼ .0027). Visual contact with conspecifics was possible for 86% of horses; the remaining had no social contact. Their diet consisted of a mixture of 71% of oats and 29% of roughage in average, presented between one and three times daily. No significant associations were found between the presence of visual contact, number of daily rations, yard, and percentage of roughage delivered, and stereotypy presentation (P > .05). In 43% of the cases with stereotypy, horses were impeded from performing the behavior by physical methods, avoiding the real problem and acting as a risk for animal welfare. Ó 2013 Elsevier Inc. All rights reserved.

Keywords: Animal welfare Equine Stereotypic behavior Thoroughbred Husbandry

1. Introduction According to Mason [1], stereotypies are repetitive invariant behavior patterns with no obvious goal or function. Their development is associated with horses being managed in suboptimal environments, currently or in the past, under conditions that result in behavioral frustration,

Corresponding author at: Tamara Tadich, MSc, Becario CONICYT, Programa Doctorado en Ciencias Veterinarias, Facultad de Ciencias Veterinarias, Universidad Austral de Chile, Casilla 567, Valdivia, Chile. E-mail address: [email protected] (T. Tadich). 0737-0806/$ - see front matter Ó 2013 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.jevs.2012.05.059

unavoidable stress, fear, or lack of stimulation [1,2]. Horses are social herd-living animals that have evolved to feed on highly fibrous material during the majority of the day [3,4]; most husbandry systems for high-performance thoroughbreds differ greatly from this. Two fundamental changes have occurred owing to domestication that can contribute to the development of stereotypies: (1) social structure is disrupted and (2) free access to forage is substituted by controlled rations, usually high in concentrates [5]. Stereotypic behavior can develop when an animal is unable to execute a behavioral pattern that it is highly motivated to perform, such as feeding behavior, or when it is unable to avoid a stressful or fearful situation [1]. In the

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horse, the most described and studied stereotypies are crib-biting/wind sucking, weaving, and box walking [2,6-8], and although it is not considered as a stereotypy, wood chewing is also of interest because it may precede or be associated with crib-biting [2,7,9]. Studies conducted in the United Kingdom have reported prevalence rates of between 3.8% and 9.4% for crib-biting/wind sucking, 2.6% and 8.3% for weaving, and 1.2% and 5.5% for box walking [10,11], and recently, in the United States, Albright et al. [12] reported a prevalence rate of 4.5% for crib-biting among different breeds. Numerous husbandry practices have been identified as risk factors for the development of these behaviors, including confinement, isolation from other horses, feeding practices, bedding material, and weaning method, among others [9,7,13-18]. The role of biological characteristics such as breed, sex, and sire has also been studied [12,19-21], and neurological explanations have also been proposed [22-24]. The development of stereotypic behavior is widely thought to be an indicator of impaired welfare, indicating that the horse has problems adapting to the environmental factors to which it is exposed [6,11,25]. However, the extent to which persistent or established stereotypies are an indicator of impaired welfare is much less certain [26]. Thoroughbreds are three times more likely to develop stereotypies than other breeds [12,21]. This may reflect a genetic susceptibility, a response to intensive management, or a combination of both. The horse-racing industry is growing in Chile, but there are no policies in relation to the housing and management of these horses, which is important taking into account that, unlike in many other countries, racehorses in Chile spend their entire competitive life housed at the racetrack yards. Establishing the prevalence of stereotyped and other abnormal behaviors in this population of thoroughbreds could provide important information about the extent to which their housing and management is ensuring their welfare. Most information currently available on the prevalence and risk factors of equine stereotypies derives from questionnaire-based cross-sectional studies. There can be problems with the accuracy and reliability of information obtained through questionnaires. To avoid this problem, the current study

determined the prevalence of stereotyped and other abnormal behaviors in thoroughbreds in Chile using direct researcher observations. Our objective was to obtain accurate information from a uniform population, contributing comparative data to build a better picture of the factors influencing stereotypies in horses.

2. Materials and Methods Seven hundred forty-three thoroughbred racehorses of different ages and sex, housed at two racetracks (A and B) in Santiago, Chile, were observed during autumn and winter seasons. At racetrack A, 417 horses were observed within 14 yards, and at racetrack B, 326 horses were observed within 13 yards. The visits to the racetracks were performed during the morning, observing the horses by scan sampling, every 5 minutes, during the 30 minutes before and 30 minutes after their food ration was delivered, adding a total of 12 scans per horse. If a horse exhibited one of the abnormal behaviors in any of the scanning times, it was counted as one. Each day, a different yard within the racetrack was visited; each yard had between 10 and 60 individual boxes where horses belonging to different owners are permanently housed. An individual record sheet was used to register the presence of the abnormal behaviors, and a questionnaire was administered to the person in charge of the horses. Each behavioral disorder was defined in an ethogram (Table 1). Information about sex, age, social contact between boxes (none, visual, or visual and tactile), bed type (straw, wood shavings, or other), feeding (roughage and concentrate quantity and delivery times), and training routine was collected. The use of methods to impede or prevent stereotypic behaviors was also registered. Data were analyzed using descriptive statistics, prevalence rates were calculated, and the association between each factor and the presence of the behaviors observed was determined using the c2 test; 2  2 contingency tables were used with the Statistix 8 software (Tallahassee, Florida). The level of significance was established at P < .05.

Table 1 Ethogram of the stereotypies and other abnormal behaviors observed Behavior

Description

Crib-biting/wind sucking

The horse may or not support the upper front teeth against any solid material. It tenses the muscles of the neck, forcing air into the cranial portion of the esophagus, making a characteristic noise. The horse can lick the object before and after the fixing. The animal moves the head from side to side. This rhythmic movement can involve neck, forelimbs, and even hind limbs. Most of the times it is performed standing with the head out of the stable, but it can also be done standing in the middle of it. The horse wanders in circles inside the box, walking, trotting, or galloping. If there is more space, it can make more complex circuits. Reiterative movements from the head up and down. Knocks with the hind limb hoofs against the wall of the stable. One forelimb a little lifted, then quickly extended forward, followed by a caudal movement, dragging the toe like a digging movement. The horse chews and ingests wood, fixing to objects (like the stall door or protruding planks) to pull out wood pieces and eat them. To eat the own feces or the ones from other individuals. The horse ingests the bed material of its stable. To lick or bite any object without nutritional purpose.

Weaving

Box walking Nodding Stall kicking Pawing Wood chewing Coprophagia Bed eating Eating or licking objects

Definitions adapted from McDonnell [27] and Tadich and Araya [5].

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Because of the low prevalence found for each behavior, and to apply the c2, the behaviors were categorized into oral and locomotor groups. The “oral group” included cribbiting/wind sucking, wood chewing, coprophagia, bed eating, and eating or licking objects. The “locomotor group” comprised weaving, box walking, nodding, box kicking, and pawing. If one horse performed more than one behavior, these were considered separately for the statistical analysis.

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Regarding the type of bedding used, only two categories were found. In 85% of the cases, wood shavings were used; the rest of the stables (15%) had straw as bedding material. The social contact between horses was “only visual” in 86% of the cases, and these horses were able to see horses in the stalls across and were kept with their own stall windows open; the remaining 14% did not have any kind of contact because their stalls were located in areas that did not have any stalls across, or their windows were closed. In relation to feeding practices, all horses were fed with oats and roughage (alfalfa hay). The rations given to the horses consisted, on average, of 71% of oats (7.9  2 kg) and only 29% of roughage (3.2  1.3 kg) daily. Food was delivered one, two, or three times a day, depending on the yard’s system or the preoccupation of the person in charge of the horse, twice daily being the most common practice. During the time spent outside the stable, horses were training, walking outside being led by handlers, or in their daily grooming routine. The average time spent outside was 86 minutes; this corresponds to 6% of the day. In 43% of the cases with stereotypy, the horse was impeded from performing the behavior, mostly using physical methods. Of these methods, 45.2% were used for locomotor behaviors and included hanging bottles inside the stables to hinder the weaving movement, use of tyres to minimize space for box walking, and, in more extreme cases, leaving the horses tied up inside the box; 22.5% were used to counter oral behaviors, including antiecrib-biting muzzles. Nonphysical methods used against both locomotor and oral behaviors included incorporation of goats inside the stalls for company, especially for nervous horses (22.5%), and the use of magnetic blankets supposed to help calm the horses (9.7%).

3. Results Behavioral observations were made at the two most important racetracks of the country, which together house approximately 2,500 horses. In Chile, as in most Latin American countries, horses arrive to the racetracks yards after auction at 2 years of age and live there during their competitive life; this results in all horses being under very similar husbandry practices. 3.1. Descriptive Results Of the 743 horses observed, 82 (11.03%) performed some kind of abnormal behavior. Of those that performed abnormal behaviors, 5 horses (6%) performed more than one and only 1 horse performed 3 abnormal behaviors (weaving þ wood chewing þ bed eating); none of the cribbiters was observed performing wood chewing. The total observed prevalence rate of stereotypies was 6.32%, and that of other abnormal behaviors was 5.52% (Table 2). The three different stereotypies were present at similar percentages; however, for other abnormal behaviors, the most prevalent one was wood chewing, with a prevalence rate of 2.02% (Table 2). At racetrack A, weaving was the most prevalent stereotypy, whereas at racetrack B, it was crib-biting; in both racetracks, wood chewing was the most common other abnormal behavior. Only at racetrack B, horses were observed performing bed eating, pawing, and eating or licking objects (Table 2). Horses were distributed according to sex and age. Most horses (92%) ranged between 2 and 5 years of age, weaving being the most prevalent behavior within this range (2.34%), as seen in Table 3. When distributed according to sex, mares represent the largest group (40%) as compared with stallions (32%) and geldings (28%); mares also showed a higher total percentage of behavioral disorders (6.7%). Table 4 summarizes the distribution of all behaviors observed according to sex.

3.2. Chi-square Results The c2 association test was used; for this purpose, abnormal behaviors were analyzed as total (stereotypies and other abnormal behaviors) or according to group as oral or locomotor. Racetrack B had overall significantly more abnormal behaviors than racetrack A (c2 ¼ 6.79, P ¼ .0092), and specifically, the prevalence of oral group behaviors was higher (c2 ¼ 10.29, P ¼ .0013). When mares were compared with stallions and geldings as one group, an overall positive association was found between the presence of abnormal behaviors and sex (c2 ¼ 10.1435, P ¼ .0014). When analyzing this factor

Table 2 Percentage of stereotyped and other abnormal behaviors for each racetrack and for the 743 thoroughbred racehorses in Chile Abnormal Behaviors

Behavior

Racetrack A

Racetrack B

Racetrack A þ B

Total

Stereotypies

Crib-biting/wind sucking Weaving Box walking Nodding Wood chewing Box kicking Coprophagia Bed eating Pawing Eating or licking objects

1.2 2.4 1.9 0.5 1.9 0.9 0.2 0 0 0

3.4 1.8 2.1 0.6 2.1 0.6 1.2 1.8 0.6 0.9

2.15 2.15 2.02 0.54 2.02 0.81 0.67 0.81 0.27 0.40

6.32

Other abnormal behaviors

5.52

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Table 3 Distribution of the horses according to age, in relation to the presentation of stereotypic and other abnormal behaviors Total Crib-biting/ Weaving Box Others* Wind Sucking Walking

Age (Years)

2-5 n 683 % 92 6-10 n 36 % 5 No information n 24 % 3 Total n 743 % 100

15 2.2

16 2.3

13 1.9

36 5.42

1 2.78

0 0.00

2 5.56

4 11.11

0 0.00

0 0.00

0 0.00

1 4.17

16 2.15

16 2.15

15 2.02

41 5.52

* Others correspond to nodding, wood chewing, box kicking, coprophagia, bed eating, pawing, and eating or licking objects.

according to racetrack, both racetracks presented the same situation: at racetrack A, the association found was of c2 ¼ 4.96 (P ¼ .026) for overall abnormal behaviors, whereas at racetrack B, mares had a higher prevalence of overall abnormal behaviors (c2 ¼ 21.24, P ¼ .000) and also oral (c2 ¼ 11.29, P ¼ .0008) and locomotor behaviors (c2 ¼ 8.3, P ¼ .004). For both racetracks, a positive association was found between the use of wood shavings and the presentation of abnormal behaviors of the oral group (c2 ¼ 8.9818, P ¼ .0027). No significant associations were found between the presence of visual contact, number of rations given daily, percentage of the ration consisting of roughage, and yards, and the presence of stereotypies (P > .05 in all cases). 4. Discussion The main objective of this study was the generation of information on abnormal behaviors in Chilean racehorses, this being, to our knowledge, the first report on the prevalence of equine stereotypies in Latin America, by direct observation. The results also allowed us to understand some of the current practices being used in the national racehorse industry.

Table 4 Distribution of horses according to sex, in relation to the presentation of stereotypic and other abnormal behaviors Sex Mare n % Stallions n % Geldings n % Total n %

Total

Crib-biting

Weaving

Box Walking

Others*

296 40

7 2.36

9 3.04

11 3.72

22 7.43

238 32

6 2.52

6 2.52

1 0.42

13 5.46

209 28

3 1.44

1 0.48

3 1.44

6 2.87

743 100

16 2.15

16 2.15

15 2.02

41 5.52

* Others correspond to nodding, wood chewing, box kicking, coprophagia, bed eating, pawing, and eating or licking objects.

Most of the horses were <5 years old, a young population compared with those reared for equestrian sports, such as show jumping and Chilean rodeo, but similar to race horses around the world. The prevalence rates of 6.32% for stereotypic behavior and 5.52% for other abnormal behavior are lower compared with some previous studies. Redbo et al. [6] obtained a prevalence rate of 9.3% for stereotypies and 16.3% for other abnormal behaviors, with wood chewing, as in this study, being the most prevalent. Pell and McGreevy [28] reported a prevalence rate of 11.8% for stereotypies in thoroughbreds reared in stables. Because the horses in this study live at the tracks, they will be subject to far less frequent transportation, a difference in management that may be partly responsible for these lower prevalence rates. However, the prevalence of stereotypies obtained in the current study is higher than the 3.5% reported by Bachmann et al. [21] for locomotor and oral stereotypies in a Swiss population of horses. The prevalence of the three individual stereotypies observed were similar (Table 2), with a prevalence for cribbiting somewhat lower than that reported by McGreevy et al. [10] and McBride and Long [11], and substantially lower than the 13.3% reported by Albright et al. [12] for thoroughbreds in the United States. All of these previous studies were performed through questionnaires, which can present difficulties. Owners can be reluctant to respond to questionnaires and may underestimate true prevalence [7]. An advantage of the current study was that the same observer made all the behavioral observations directly, as in the case of the longitudinal study performed by Waters et al. [7]. In the study by Waters et al. [7], the prevalence rates of crib-biting and weaving were higher than in the present study (10.5% and 4.6%, respectively), but a similar prevalence was reported for box walking (2.3%). One reason why Waters et al. [7] found higher prevalence rates of cribbiting and weaving than us could be the age at which these behaviors developed. The authors reported a median age at the onset of crib-biting and weaving of just 20 and 60 weeks, respectively, and considered the reasons why their prevalence in young horses might be higher than in adult competitive populations. One possibility raised by Nicol et al. [8] and Waters et al. [7] is that it is possible to reduce stereotypies in young horses by appropriate management changes. In the current study, this could have occurred before the horses being introduced to the racetracks. A second possibility is that young stereotypic horses could be dismissed earlier than “healthy” ones owing to poor performance. In the current study, this could have occurred if owners had detected problems early and decided not to race youngsters with stereotypies. Waters et al. [7] also point out that stereotypic foals may be more likely to be culled or present higher mortality rates and therefore do not appear in the mature horse population. Although both racetracks had very similar husbandry practices, the horses housed at racetrack B had significantly more abnormal behaviors (c2 ¼ 6.79, P ¼ .0092) than those at racetrack A, the abnormal oral behaviors being the most prevalent (c2 ¼ 10.29, P ¼ .0013). Wood chewing was the most prevalent nonstereotypic abnormal behavior observed overall and at each racetrack (2.02%, Table 2), with a prevalence similar to the 1.3% reported by Ahmadinejad and Habibi [29] for a population of 690 horses of

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different breed, sex, and age, and lower than the 3.8% reported by Christie et al. [15] in a population of 312 nonracing horses. Although this behavior may simply reflect motivation for feeding outside of meal times because of cues from gut fill, time since the last meal, or a drop in blood glucose [30], it is important to consider that it can precede or be associated with crib-biting behavior [7,9]. In the present study, 71.4% of the horses that were observed wood chewing received feed twice daily, and, on average, their feedstuff contained only 29% of roughage, both being management factors that could influence the presentation of this behavior. Mares were more likely to develop abnormal behaviors, both oral and locomotor, than either geldings or stallions. There are just a few investigations where the possible relation between sex and stereotypic behavior has been studied, and these produced different results. Mills et al. [31] found geldings more likely to perform stereotypies, possibly because high testosterone levels are protective in some way, because surgery increases the risk (perhaps through stress-related factors), or because there may have been a greater tendency to castrate male animals who develop a stereotypy at an early age to prevent them from passing on the behavioral tendency to their offspring. Luescher et al. [20] also reported a higher prevalence of crib-biting in geldings and stallions compared with mares, which in the case of stallions, according to Wickens and Heleski [18], could be related to the fact that they are frequently housed in individual enclosures to prevent accidental breeding and aggression. In the current study, all horses, including mares, were housed individually, with limited movement and social contact. There is no obvious explanation why the mares in the current study should be more likely to perform stereotypies. It might be related to hormonal factors, temperament, or an unidentified external factor (for example, how many mares/stallions/geldings were in the charge of the same person). A recent study on purebred Arab mares used for breeding showed a significant relationship with reproductive status, where nonfoaling mares had a greater tendency to perform stereotypic behavior than foaling mares; in this study, neither age nor sire affected the performance of these behaviors [32]. Horses involved in the present study were observed during the autumnewinter period, and these mares were not involved in breeding programs or hormonal therapy because they are only used for racing purposes while they are kept at the racetrack yards; thus, the influence of the estrous cycle in the development of their abnormal behaviors, especially locomotor ones, should be less. Wood shavings was the most frequent bedding material used, and it was a significant risk factor (c2 ¼ 8.9818; P ¼ .0027) in the presentation of abnormal oral behaviors compared with the use of straw. This was also reported by McGreevy et al. [10], who stated that the use of any bedding different from straw contributes to the development of abnormal oral behaviors. Straw may ameliorate some of the behavioral problems associated with restricted fiber diets, as horses occupy themselves more with straw than other bedding types [33]. However, this could be better achieved by feeding adequate quantities at higher frequencies of a more appropriate fiber source [10]. Goncalves et al. [34] warn that impaction colic often appears just after change

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to straw bedding, particularly if there is no other source of fiber available, although Tinker et al. [35] were not able to establish an association between colic and any type of bedding. The relatively low proportion of roughage in the diet of the horses in this study seems to be counterproductive according to percentages recommended in the literature. Davidson and Harris [36] state that most horses, including the ones in hard work, should have a diet based on at least 50% of roughage. In contrast, for racehorses, a low percentage of fiber in the diet has been advised, provided always a minimum of 30% of roughage is included [37]. In this study, it was not possible to identify whether the ratio of forage to concentrate influences the development of abnormal behaviors, as the management of all horses was similar. It was also observed that 54% of the horses received food twice or three times a day. Nicol et al. [8] suggested that spreading delivery of feed over a longer time frame may reduce the incidence of stereotypies, whereas Cooper et al. [38] described a decline in oral stereotypies with an increase in locomotor stereotypies when meal frequency was increased. The time spent out of the box was practically the same for all horses, with an average of 86 minutes, so the possible influence of time spent stabled on the development of stereotypies could not be evaluated. McGreevy et al. [14] found that the risk of presentation of stereotypic behavior increased significantly when spending <4 hours outside the stall, and that endurance horses spend significantly more time out of their stalls than dressage and eventing horses [14]. Tadich et al. [39] reported that only 41% of Chilean Creole horses used for rodeo competition spend >6 hours inside stalls, although the prevalence rate of abnormal behavior registered was 11%, similar to the prevalence reported in the present study. Eighty-five percent of the horses had visual contact with other horses between boxes; the rest did not have any type of contact. No significant association was found between the presence of visual contact and the development of stereotypies, which does not agree with the results of McGreevy et al. [14], who reported that the absence of social contact is an important risk factor. Other studies have also reported that the incorporation of windows, mirrors [40], or images of other horses [41] significantly reduced locomotor stereotypies. Wild horses are gregarious animals, and social isolation represents a disturbing experience for them [42]. In other countries, boxes may be more isolating because of their linear distribution and the use of concrete solid walls, than in Chile, where most boxes are made of wood planks, so a little visual contact or feeling of companionship is probably always present. In 43% of the cases with stereotypy, attempts were made to prevent the horse from performing the behavior, generally by physically restrictive methods (with the exception of goats as companions). This avoids the real problem and becomes a risk for the welfare of the animal. If stereotypies are a response to specific challenges that have to be faced inside the box, then restriction of the behavior does not represent a solution, and may even cause secondary problems owing to increased stress [25,43,44]. In conclusion, our finding that 11.03% of the race horses directly observed in this study presented at least one

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abnormal behavior is relevant for animal welfare and suggests that some changes to management and husbandry would be beneficial. Acknowledgments The authors thank the people from the racetracks “Club Hípico de Santiago” and “Hipódromo de Chile,” specially Dr. Mariano Goic and Dr. Arnaldo Croxato, for their help by allowing data collection.

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