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The ethological and physiological characteristics of cribbing and weaving horses
Applied Animal Behaviour Science 109 (2008) 68–76 www.elsevier.com/locate/applanim
The ethological and physiological characteristics of cribbing and weaving horses Heather A. Clegg a,*, Petra Buckley a, Michael A. Friend a, Paul D. McGreevy b a
School of Agricultural and Veterinary Sciences, Charles Sturt University, Wagga Wagga, NSW 2650, Australia b Faculty of Veterinary Science, University of Sydney, Sydney, NSW 2006, Australia Accepted 3 February 2007 Available online 8 March 2007
Abstract Data were gathered on the behavioural and physiological characteristics of five cribbers, six weavers and six non-stereotypic (control) mature Thoroughbred geldings for a period of 16 weeks. The horses were hired from their owners and stabled individually throughout the trial. Cribbers and weavers had been known to stereotype for at least 12 months prior to commencement of the study. Behavioural data were collected using video surveillance. Cribbers stereotyped most frequently (P < 0.001) in the period 2–8 h following delivery of concentrated food, reinforcing the suggestion that diet is implicated in cribbing behaviour. Weavers stereotyped most frequently (P < 0.001) during periods of high environmental activity such as during routine pre-feeding activities and in the hour prior to daily turnout, presumably when anticipation and stimulation were at their highest levels. Cribbers and weavers took longer than control horses to fully consume their ration, suggesting possible differences in motivation to feed, distress levels, satiety mechanisms or abdominal discomfort. Physiological data were collected throughout the trial and there were no differences in oro-caecal transit time, digestibility, plasma cortisol concentration or heart rate among the three behavioural groups. # 2007 Elsevier B.V. All rights reserved. Keywords: Horse; Stereotypy; Digestion; Gut transit; Stress
1. Introduction Stereotypies are repetitive, relatively invariant behaviour patterns with no apparent function (Fraser and Broom, 1990; Mason, 1991). Oral and locomotory stereotypies are common among
* Corresponding author at: Charles Sturt University Equine Centre, P.O. Box 588, Wagga, Wagga, NSW 2650, Australia. Tel.: +61 2 6933 4320; fax: +61 2 6933 2796. E-mail address: [email protected] (H.A. Clegg). 0168-1591/$ – see front matter # 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.applanim.2007.02.001
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intensively managed horses, being reported in approximately 4 and 3% of the adult horse population, respectively (Nicol, 1999). However, their causes are not well understood. It has been proposed that these behavioural anomalies develop as a result of unnatural management systems and, as such, it is important that the influence of current management protocols on the expression of stereotypies is determined, to ensure that horses are managed in ways that do not compromise their welfare. Numerous management techniques have been blamed for the development of stereotypies in horses. These include confinement (Fraser and Broom, 1990; Broom and Kennedy, 1993), isolation from other horses (Nicol, 1999; Cooper et al., 2000; McAfee et al., 2002; Mills and Davenport, 2002), provision of small concentrated feeds (Gillham et al., 1994; McGreevy et al., 1995; Johnson et al., 1998; Nicol, 1999) and both a lack of stimulation (Kiley-Worthington, 1983; Broom and Kennedy, 1993; Waran and Henderson, 1998) and an over-abundance of environmental activity (Winskill et al., 1995; Cooper et al., 2000). Previous studies have produced conflicting descriptions of the ethological and physiological characteristics of stereotypic horses. The current study investigated time budgeting, stereotypy frequency, eating behaviour, digestive physiology (oro-caecal transit time, digestibility) and physiological stress parameters (plasma cortisol concentrations and heart rate) in cribbers and weavers, its aim being to quantify the characteristics of horses with established stereotypic behaviours. From anecdotal and published discussions (Kennedy et al., 1993; Gillham et al., 1994; McGreevy et al., 1995; McGreevy and Nicol, 1998a; Cooper et al., 2005), we hypothesised that cribbing is most frequent during and after feeding and that weaving peaks during periods of high activity such as prior to feeding and turnout. We also hypothesised that there would be no difference in plasma cortisol concentrations or mean heart rate between stereotypic and nonstereotypic horses, as found by McBride (1996), McGreevy and Nicol (1998b), Pell and McGreevy (1999) and McBride and Cuddeford (2001). No difference in digestibility (McGreevy et al., 2001) or oro-caecal transit time (McGreevy et al., 2001; McGreevy and Nicol, 1998a) between stereotypic and control horses was expected. Despite their having visual contact with stereotypers, we did not expect any non-stereotypic controls to mimic cribbing or weaving whilst in the study (McGreevy, 1999; McAfee et al., 2002; Mills and Davenport, 2002; Waters et al., 2002). 2. Methods 2.1. Horses Seventeen adult Thoroughbred geldings were hired from their owners for use in this study. The experimental group consisted of five cribbers, six weavers and six non-stereotypic controls, aged 10.29 1.96, 11.50 2.93 and 11.17 2.21 years, respectively. All cribbers and weavers were known by their owners to have stereotyped for at least 12 months prior to recruitment into the study. As the horses were from different owners, their management and feeding regimes prior to arrival at the University were varied. In order to minimise the residual effect of the different management systems, horses arrived a minimum of 7 days prior to commencement and underwent an additional 7-day acclimatisation to the stables and routine of the trials. At the commencement of the study, bodyweights ranged from 464 to 630 kg. Mean starting weights (S.E.) for the cribbers, weavers and non-stereotypic controls were 541.2 27.0, 503.3 16.1 and 539.0 19.4 kg, respectively. These were not significantly different. The study was conducted with the approval of the Charles Sturt University Animal Care and Ethics Committee.
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2.2. Stables Horses were housed in stables (4 m 4 m), consisting of wooden paneling 1.2 m high, topped with vertical steel bars (15 mm diameter, 10 cm apart) extending a further 1.2 m. Gaps between the bars allowed olfactory, visual and tactile contact with neighbouring horses on three sides. Doors consisted of sliding front panels, preventing horses from putting their heads outside the stables. Boxes had concrete floors with sawdust as bedding and water was provided ad libitum in 60 L plastic garbage bins. All horizontal surfaces of the stables were made of metal. Since metal surfaces are rarely preferred as substrates for cribbing, a wooden bar (approximately 60 cm long, 10 cm 8 cm) was fixed to a side wall of each stable to facilitate and focus crib-biting. A standard video surveillance camera was mounted above each stable and linked to a sequential switcher and time-lapse video recorder. 2.3. Experimental design Experimental work was carried out as two identical 16-week replicates [Replicate 1 (R1) and Replicate 2 (R2)], including four cribbers, three weavers and three controls in R1 and one cribber, three weavers and three controls in R2. The horses were fed a diet of whole oats, wheaten chaff, lucerne chaff and lucerne hay, in accordance with the National Research Council (1989) guidelines at an energy concentration of 2.4 Mcal digestible energy/kg dry matter. Feed was delivered in two equal rations at 10:00 and 17:00 h each day. Horses spent 22 h per day in their stables, in accordance with usual confinement of a stabled race horse (McGreevy, 2004). For 2 h each afternoon (commencing at 13:30 h) they were given free exercise in a paddock, during which period no data were collected. Behavioural observations, sampling for plasma cortisol concentration and heart rate monitoring were carried out on all horses throughout the duration of the trial. Oro-caecal transit time and digestibility were measured only in cribbers and control horses at the end of the 4th, 8th, 12th and 16th weeks, as digestive processes have been implicated in the development and performance of cribbing behaviour (Gillham et al., 1994; McGreevy et al., 1995; Redbo et al., 1998; Waters et al., 2002; Bachmann et al., 2003). 2.4. Behavioural measurements Video surveillance was carried out on all horses for the 22 h they spent in the stables each day, for the duration of the 16 weeks of the study. A sequential switcher was attached to the camera system, meaning that each horse was filmed for 30 s in every 5 min period. The complete footage was analysed and a tally system was used to record the behavioural observations. Frequency of each behaviour type was recorded, along with the hourly distribution of cribbing and weaving. Distribution data were analysed to determine the effect of stable activity (pre-feeding, post-feeding, pre-turnout) on cribbing and weaving frequency. Table 1 gives a summary of the behaviours that were measured. Food intake was calculated by removing and weighing of any feed remaining in the stable prior to delivery of the morning ration. Water buckets were filled each afternoon, and the volume of water required to refill them on the following afternoon was measured to give an indication of how much water had been consumed. 2.5. Physiological measurements Venous blood samples for cortisol measurement were taken from each horse every second morning at 09:00 h. Plasma cortisol assays were carried out using cortisol RIA assay kits (Active Cortisol RIA DSL2100, Diagnostic Systems Laboratories, Texas, USA). Average daily heart rate (excluding turnout time) was measured for each horse throughout the duration of the trial, using heart rate monitors (Polar Accurex PlusTM, Polar ElectroTM, Finland) attached to regular lunge rollers. Bodyweight was measured every week, using a walk-on weighbridge, after removal from the paddock and prior to delivery of the evening meal at 17:00 h.
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Table 1 Behaviours of stabled horses, measured during analysis of video footage, with definitions for the purpose of this study Behavioural label
Definition for the purpose of this study
Cribbing
Horse latching onto a solid object with its incisors, arching its neck and pulling backwards. Each single repetition of this behaviour was counted as one repetition on the tally Repetitive swinging of the horse’s head and neck from side to side. Each time the horse returned to the left extreme of their swinging motion was counted as one repetition on the tally Standing with head down and muzzle in feed bin Standing with head down and lips sifting through bedding Standing with head down and muzzle in water bucket Lying down, either laterally or sternally Tail raised with posturing for defaecation Tail raised with posturing for urination Rubbing of any body parts on the walls of the stable
Weaving
Eating Foraging Drinking Recumbency Defaecation Urination Rubbing
Oro-caecal transit time was measured using the method developed for use in horses by McGreevy and Nicol (1998a). Horses were orally dosed with a sulphasalazine paste (Salazopyrin, Kabi Pharmacia Ltd., Milton Keynes, UK) at a rate of 50 mg/kg, followed immediately by delivery of the morning feed ration. After a baseline pre-feeding blood sample was withdrawn, sequential samples were withdrawn from each horse every 30 min for the following 7 h, to determine when absorption of the sulphasalazine, which can only occur from the caecum, could first be detected. Sulphapyridine was detected by HPLC, as described by McGreevy and Nicol (1998a). The threshold of first appearance was set at the point where the ratio of sulphapyridine to internal standard (sulphamethazine) reached 0.02. Digestibility was determined by measuring n-alkane concentrations in feed and faeces, using the method described by Mayes et al. (1986) and modified by Dove (1992). Horses were accustomed to wearing faecal collection harnesses (EquisanTM, Australia) during the 7-day acclimatisation period, and wore these throughout the trial (excluding turnout time). Grab-samples of faeces were removed from the faecal collection harness every 6 h for a period of 48 h during weeks 4, 8, 12 and 16. Feed and faecal samples were subsequently frozen at 4 8C, then oven dried to a constant weight at 60 8C prior to grinding through a 1 mm sieve using a cyclone sample mill. Determination of alkane concentrations was carried out using the alkane extraction method described by Dove (1992). Values for C31 were used in the analysis, as the concentration of this alkane is high in feed and faeces. C31 concentrations also had the greatest correlation between feed values and faecal values. Raw data were corrected for faecal recovery, using the recovery value of 94.0 2.8% reported by O’Keefe and McMeniman (1998). 2.6. Statistical approach Analysis was performed using software by Statistical Analysis Systems (Version 8, SAS Institute Inc., Cary NC). All P values are based on Type III sum of squares. Behavioural data are presented as frequency of occurrence. Daily frequency of stereotypy was determined using multivariate analysis of variance for repeated measures. Observations of stereotypy in each horse were treated as repeated measures. The data were checked for normality. If they were not normal, a non-parametric test which is appropriate for data not normally distributed (Wilcoxin rank sum test) was applied. All data were analysed in two stages. In stage 1, all observations were treated as independent and the data were analysed using ANOVA to indicate any effect of behavioural group. Where no group effects were indicated for a particular variable, no further analysis of that variable was conducted. If stage 1 analysis indicated a probable group effect, then further analysis was conducted in stage 2, to accommodate the fact that the observations were not truly independent (up to four observations were made on each horse, for weeks 1–4, weeks 5–8, weeks 9–12 and weeks 13–16 of the trial). Thus, in stage 2
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repeated observations made on the same animal were pooled, and the analysis was repeated. The results of stage 2 analysis are reported in this paper. Arithmetic means are presented standard error.
3. Results 3.1. Behaviour Cribbers were observed to crib-bite 147.0 33.1 times per daily period of observation. Since horses were each only observed for 10% of the 22 h that they were in the stables each day (132 min of observation per day in total), the actual cribbing frequency is likely to have been approximately 1470 events per horse per day, assuming behaviour was evenly distributed throughout each 5 min block. Weavers were observed to weave 53.0 12.4 times per daily period of observation, equating to a daily weaving frequency of approximately 530 events per horse. No stereotypic behaviour was observed in any of the control horses for the duration of the study. Analysis of the distribution of cribbing behaviour before and after the delivery of concentrated food revealed a significant change (P < 0.001) in frequency over this period, with 2.6 0.9 events observed in the hour prior to feeding, compared with 4.3 0.8 observed events per hour in the 2 h immediately following feeding, and 10.0 1.7 observed events per hour in the period 2– 4 h following feeding. Cribbing frequency continued to increase slightly for up to 8 h following
Fig. 1. Daily distribution of stereotypy frequency in stabled horses (bars show S.E.). a, b, c, A, B, C: means on a line with different superscripts differ (P < 0.001).
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Table 2 Summary of ethological responses of stabled horses by behavioural group Ethological response
Controls (mean S.E.)
Cribbers (mean S.E.)
Weavers (mean S.E.)
P value
Stereotypy frequency (events/daily observation period) Eating frequency (events/daily observation period) Time taken to consume ration (h) Foraging frequency (events/daily observation period) Drinking frequency (events/daily observation period) Water intake (L/day) Recumbency (events/daily observation period) Rubbing frequency (events/daily observation period) Urination (events/daily observation period) Defaecation (events/daily observation period)
0.0 0.0 44.1 2.14 5.38 0.41 a 28.4 2.85 1.32 0.45 17.25 0.75 22.42 2.97 0.20 0.07 0.72 0.10 0.72 0.11
147.0 33.1 51.5 2.68 9.01 0.94 b 16.6 2.51 1.56 0.59 18.75 2.32 17.33 2.88 0.68 0.19 0.60 0.12 0.68 0.11
53.0 12.4 59.8 3.28 9.6 1.07 b 19.8 3.33 0.89 0.25 15.4 2.12 18.98 2.28 0.18 0.05 0.75 0.11 0.85 0.11
0.079 0.121 <0.001 0.252 0.549 0.458 0.533 0.181 0.594 0.669
Means in a row with different letters differ. Daily observation period refers to 132 min of observation per day
delivery of the meal, with a peak of 11.6 2.1 observed events in the period 6–8 h following delivery of the ration. Cribbing frequency gradually declined until it reached baseline levels again prior to delivery of the morning concentrated ration (Fig. 1). Observed hourly weaving behaviour was significantly more frequent (P < 0.001) in the hour prior to delivery of the morning ration (16.4 3.0 events per hour, at which time the researcher was present, taking blood samples and emptying faecal collection bags), when compared with the rest of the day (1.62 0.51 events per hour). Weaving frequency in the hour prior to turnout was also significantly greater (P < 0.05), at 5.9 2.4 observed events per hour, than the frequency observed during the rest of the day (Fig. 1). All horses consumed their entire daily ration. There were no significant differences in eating frequency among behavioural groups. However, cribbers and weavers took significantly longer to consume their ration than controls (Table 2). Cribbers and weavers were observed to eat for a period of up to 2 h following delivery of the ration, followed by repeated breaks from eating for periods of up to 3 h. There was no effect of behavioural group on water intake, temporal distribution and frequency of drinking, frequency of foraging, recumbency, rubbing, urinating or defaecating (Table 2). 3.2. Physiology Plasma cortisol concentration (mg/dL) and average heart rate were not significantly different between cribbers, weavers and controls (Table 3). There was a trend (P < 0.1) towards a faster Table 3 Summary of physiological responses by behavioural group Physiological response
Controls (mean S.E.)
Cribbers (mean S.E.)
Weavers (mean S.E.)
P value
Plasma cortisol concentration (mg/dL) Heart rate (beats/min) OCTT (min) Digestibility Weight gain (kgs)
0.79 0.05 38.47 0.71 137.0 8.0a 0.52 0.04 46.0 11.9
0.80 0.06 39.49 0.59 110.0 6.3b 0.58 0.17 41.7 7.14
0.83 0.06 38.04 0.65 – – 32.4 5.74
0.184 0.333 <0.1 0.332 0.580
Means in a row with different superscripts differ.
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oro-caecal transit time in cribbers than in normal horses. There was no significant effect of behaviour type on digestibility or weight gain (Table 3). 4. Discussion No stereotypic behaviour was observed in any of the control horses in this study, despite visual contact with stereotypic horses. This short-term finding supports the research of Marsden (1995) and McGreevy (1999), which suggest that horses do not learn these behaviours by mimicry. The timing of the most concentrated periods of weaving, in the hour prior to feeding and prior to afternoon turnout, adds weight to the suggestion that weaving is more directly related to barrier frustration prompted by excitement or anticipation of an event, rather than to dietary factors or lack of environmental stimulation. As the horses in this study were housed in stables that allowed social contact between neighbouring horses at all times, visual isolation from conspecifics seems unlikely as a proximate cause of weaving in these horses. The finding that cribbers stereotype most frequently during and particularly following consumption of meals supports the results of other researchers (Kennedy et al., 1993; Gillham et al., 1994; McGreevy et al., 1995; McGreevy and Nicol, 1998a; Cooper et al., 2005). However, the peak cribbing frequency in the current study began 2–4 h post-feeding and reached its highest point 6–8 h post-feeding, which is a longer time-frame than previously reported. This suggests that gastric pain was not the sole source of any visceral discomfort that cribbers underwent in the current study. If cribbing is indeed a response to visceral discomfort, it appears more probable from the current data, that it is related to fermentative acidosis in the hindgut, since the commencement of the period of maximal post-feeding cribbing (between 2 and 8 h post-feeding) coincided temporally with the initial arrival of ingesta in the caecum (approximately 110 min post-feeding). Interspersion of eating with bouts of crib-biting may be related to attempts to normalise digestion in the foregut. Pauses in eating by cribbers and weavers and lengthy periods taken to fully consume the ration may also reflect abdominal discomfort, such as that which might be caused by gastric ulceration (Nicol, 1999) or hindgut acidosis (Johnson et al., 1998). Equally, cribbers and weavers may have a reduced motivation or ‘‘behavioural need’’ to feed that resulted in slower eating. This hypothesis would contrast with those put forward by previous authors (Hughes and Duncan, 1988; Broom and Kennedy, 1993; Wu¨rbel et al., 1998; Henderson and Waran, 2001), who suggested that there may be a behavioural need for feeding and/or foraging behaviour to be expressed, leading to the development of oral movements such as cribbing in horses under intensive management. Slower eating can also be associated with either subclinical dysphagia or satiation (McGreevy, 2004). It has been proposed that, in foals at least, cribbing may be a homeostatic response to food reaching the inflamed gastric lining found to be common amongst cribbers (Nicol, 1999; Nicol et al., 2002). However, the peak of cribbing frequency in the current study began 2–4 h postfeeding and reached its highest point 6–8 h post-feeding. This suggests that gastric pain was not the primary source of any putative visceral discomfort in cribbers. That said, it is also possible that there is a cumulative effect of concentrated food reaching the inflamed gastric lining, resulting in greater discomfort as the horse continues to eat for up to 9 h after delivery of the ration. Cribbers tended to have a shorter oro-caecal transit time than control horses. This differs from the findings of McGreevy and Nicol (1998b), who have suggested that cribbing may help to shorten oro-caecal transit time in horses that would otherwise have a slow rate of passage through
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the foregut, resulting in a decrease in their oro-caecal transit time to within a normal range. In the current study, it is possible that cribbing may have shortened oro-caecal transit time even more than has been reported previously. The absence of any difference in plasma cortisol concentrations and average heart rates between cribbers, weavers and control horses supports the findings of McBride (1996), McGreevy and Nicol (1998a), Pell and McGreevy (1999), and McBride and Cuddeford (2001). No comment can be made from this study regarding whether stereotyping has a long term stressreducing effect, as the horses involved were mature and had been observed stereotyping for at least 12 months prior to the study. A longitudinal study of circulating cortisol concentrations in a large population of young horses, with commencement prior to stereotypy development, would be more likely to reveal any effects of stereotypy development on physiological stress responses. 5. Conclusion It appears from the current study that stereotypy in mature, established cribbers is linked to feed consumption and that weaving is linked to anticipation or periods of high environmental activity. The temporal coincidence between arrival of ingesta in the caecum and commencement of the peak cribbing period suggests that there may be a link between cribbing and caecal fermentation. The theory that cribbing occurs in stabled horses as a result of a behavioural need to feed is questioned by this research, particularly as cribbing occurred while feed was still available. In order to obtain a clearer understanding of the ontogeny and functional significance of stereotypies in horses, the authors suggest the use of longitudinal physiological and behavioural studies using large groups of age-matched young horses, so that any digestive or stress-related effects can be elucidated during the emergence of stereotypic behaviours. Acknowledgements The authors would like to acknowledge the financial contribution of the NSW Racing Research Fund. Prof. Martin Sillence, Kellie Munn, Dr Hugh Dove and Terry Flynn are thanked for their technical assistance with sample and data analysis. Thanks also to the owners for the loan of the horses studied in this research. References Bachmann, I., Audige, L., Stauffacher, M., 2003. Risk factors associated with behavioural disorders of crib-biting, weaving and box-walking in Swiss horses. Equine Vet. J. 35, 158–163. Broom, D.M., Kennedy, M.J., 1993. Stereotypies in horses: their relation to welfare and causation. Equine Vet. Educ. 5, 151–154. Cooper, J.J., McDonald, L., Mills, D.S., 2000. The effects of increasing visual horizons on stereotypic weaving: implications for the social housing of stabled horses. Appl. Anim. Behav. Sci. 69, 67–83. Cooper, J.J., Mcall, N., Johnson, S., Davidson, H.P.B., 2005. The short-term effects of increasing meal frequency on stereotypic behaviour of stabled horses. Appl. Anim. Behav. Sci. 90, 351–364. Dove, H., 1992. Using the n-alkanes of plant cuticular wax to estimate the species composition of herbage mixtures. Aust. J. Agric. Res. 43, 1711–1724. Fraser, A.F., Broom, D.M., 1990. Farm Animal Behaviour and Welfare. Bailliere Tindall, London. Gillham, S.B., Dodman, N.H., Shuster, L., Kream, R., Rand, W., 1994. The effect of diet on cribbing behaviour and plasma b-endorphin in horses. Appl. Anim. Behav. Sci. 41, 147–153. Henderson, J.V., Waran, N.K., 2001. Reducing equine stereotypies using an EquiballTM. Anim. Welf. 10, 73–80.
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Hughes, B.O., Duncan, I.J.H., 1988. The notion of ethological ‘‘need’’, models of motivation and animal welfare. Anim. Behav. 36, 1696–1707. Johnson, K.G., Tyrrell, J.B., Rowe, J.B., Pethick, D.W., 1998. Behavioural changes in stabled horses given nontherapeutic levels of virginiamycin. Equine Vet. J. 30, 139–143. Kennedy, M.J., Schwabe, A.E., Broom, D.M., 1993. Crib-biting and wind-sucking stereotypies in the horse. Equine Vet. Educ. 5, 142–147. Kiley-Worthington, M., 1983. Stereotypies in horses. Equine Pract. 5, 34–40. Mason, G.J., 1991. Stereotypies: a critical review. Anim. Behav. 41, 1015–1037. Marsden, M.D., 1995. An investigation of the heredity of susceptibility of stereotypic behaviour patterns (stable vices) in the horse. Equine Vet. J. 27, 415. Mayes, R.W., Lamb, C.S., Colgrove, P.M., 1986. The use of dosed and herbage n-alkanes as markers for the determination of herbage intake. J. Agric. Sci. 107, 161–170. McAfee, L.M., Mills, D.S., Cooper, J.J., 2002. The use of mirrors for the control of stereotypic weaving behaviour in the stabled horse. Appl. Anim. Behav. Sci. 78, 159–173. McBride, S.D., 1996. A comparison of physical and pharmacological treatments for stereotyped behaviour in the horse. In: Proceedings of the 30th International Congress, International Society Applied Ethology, p. 26. McBride, S.D., Cuddeford, D., 2001. The putative welfare-reducing effects of preventing equine stereotypic behaviour. Anim. Welf. 10, 173–189. McGreevy, P.D., 1999. Eight case reports of crib-biting foals. Equine Vet. J. Suppl. 28, 66 The Role of the Horse in Europe. McGreevy, P.D., 2004. Equine Behavior: A Guide for Veterinarians and Equine Scientists. W.B. Saunders, London. McGreevy, P.D., Nicol, C.J., 1998a. The effect of short-term prevention on the subsequent rate of crib-biting in Thoroughbred horses. Equine Vet. J. Suppl., Equine Clin. Behav. 27, 30–34. McGreevy, P.D., Nicol, C.J., 1998b. Physiological and behavioural consequences associated with short-term prevention of crib-biting in horses. Physiol. Behav. 65, 15–23. McGreevy, P.D., Richardson, J.D., Nicol, C.J., Lane, J.G., 1995. A radiographic and endoscopic study of horses performing an oral based stereotypy. Equine Vet. J. 27, 92–95. McGreevy, P.D., Webster, A.J.F., Nicol, C.J., 2001. A study of the behaviour, digestive efficiency and gut transit times of crib-biting horses. Vet. Rec. 148, 592–596. Mills, D.S., Davenport, K., 2002. The effect of a neighbouring conspecific versus the use of a mirror for the control of stereotypic weaving behaviour in the stabled horse. Anim. Sci. 74, 95–101. National Research Council, 1989. Nutrient Requirements of Horses, 5th ed. National Academy Press, Washington, DC, USA. Nicol, C.J., 1999. Stereotypies and their relation to management. In: Harris, P.A., Gomarsall, G., Davidson, H.P.B., Green, R. (Eds.), Proceedings of the BEVA Specialist Days on Behaviour and Nutrition. Newmarket, UK, Equine Vet. J., 11– 14. Nicol, C.J., Davidson, H.P.D., Harris, P.A., Waters, A.J., Wilson, A.D., 2002. Study of crib-biting and gastric inflammation and ulceration in young horses. Vet. Rec. 151, 658–662. O’Keefe, N.M., McMeniman, N.P., 1998. The recovery of natural and dosed n-alkanes from the horse. Anim. Prod. Aust. 22, 337. Pell, S.M., McGreevy, P.D., 1999. A study of cortisol and beta-endorphin levels in stereotypic and normal Thoroughbreds. Appl. Anim. Behav. Sci. 64, 81–90. Redbo, I., Redbo-Tortensson, P., Odberg, F.O., 1998. Factors affecting behavioural disturbances in race-horses. Anim. Sci. 66, 81–90. Waran, N.K., Henderson, J., 1998. Stable vices: what are they, and can we prevent them? Equine Pract. 20, 6–7. Waters, A.J., Nicol, C.J., French, N.P., 2002. Factors influencing the development of stereotypic and redirected behaviors in young horses: the findings of a four year prospective epidemiological study. Equine Vet. J. 34, 572–579. Winskill, L., Waran, N.K., Channing, C., Young, R., 1995. Stereotypies in the stabled horse: causes, treatments and prevention. Curr. Sci. 69, 310–316. Wu¨rbel, H., Chapman, R., Rutland, C., 1998. Effect of feed and environmental enrichment on development of stereotypic wire-gnawing in laboratory mice. Appl. Anim. Behav. Sci. 60, 69–81.
The ethological and physiological characteristics of cribbing and weaving horses Heather A. Clegg a,*, Petra Buckley a, Michael A. Friend a, Paul D. McGreevy b a
School of Agricultural and Veterinary Sciences, Charles Sturt University, Wagga Wagga, NSW 2650, Australia b Faculty of Veterinary Science, University of Sydney, Sydney, NSW 2006, Australia Accepted 3 February 2007 Available online 8 March 2007
Abstract Data were gathered on the behavioural and physiological characteristics of five cribbers, six weavers and six non-stereotypic (control) mature Thoroughbred geldings for a period of 16 weeks. The horses were hired from their owners and stabled individually throughout the trial. Cribbers and weavers had been known to stereotype for at least 12 months prior to commencement of the study. Behavioural data were collected using video surveillance. Cribbers stereotyped most frequently (P < 0.001) in the period 2–8 h following delivery of concentrated food, reinforcing the suggestion that diet is implicated in cribbing behaviour. Weavers stereotyped most frequently (P < 0.001) during periods of high environmental activity such as during routine pre-feeding activities and in the hour prior to daily turnout, presumably when anticipation and stimulation were at their highest levels. Cribbers and weavers took longer than control horses to fully consume their ration, suggesting possible differences in motivation to feed, distress levels, satiety mechanisms or abdominal discomfort. Physiological data were collected throughout the trial and there were no differences in oro-caecal transit time, digestibility, plasma cortisol concentration or heart rate among the three behavioural groups. # 2007 Elsevier B.V. All rights reserved. Keywords: Horse; Stereotypy; Digestion; Gut transit; Stress
1. Introduction Stereotypies are repetitive, relatively invariant behaviour patterns with no apparent function (Fraser and Broom, 1990; Mason, 1991). Oral and locomotory stereotypies are common among
* Corresponding author at: Charles Sturt University Equine Centre, P.O. Box 588, Wagga, Wagga, NSW 2650, Australia. Tel.: +61 2 6933 4320; fax: +61 2 6933 2796. E-mail address: [email protected] (H.A. Clegg). 0168-1591/$ – see front matter # 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.applanim.2007.02.001
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intensively managed horses, being reported in approximately 4 and 3% of the adult horse population, respectively (Nicol, 1999). However, their causes are not well understood. It has been proposed that these behavioural anomalies develop as a result of unnatural management systems and, as such, it is important that the influence of current management protocols on the expression of stereotypies is determined, to ensure that horses are managed in ways that do not compromise their welfare. Numerous management techniques have been blamed for the development of stereotypies in horses. These include confinement (Fraser and Broom, 1990; Broom and Kennedy, 1993), isolation from other horses (Nicol, 1999; Cooper et al., 2000; McAfee et al., 2002; Mills and Davenport, 2002), provision of small concentrated feeds (Gillham et al., 1994; McGreevy et al., 1995; Johnson et al., 1998; Nicol, 1999) and both a lack of stimulation (Kiley-Worthington, 1983; Broom and Kennedy, 1993; Waran and Henderson, 1998) and an over-abundance of environmental activity (Winskill et al., 1995; Cooper et al., 2000). Previous studies have produced conflicting descriptions of the ethological and physiological characteristics of stereotypic horses. The current study investigated time budgeting, stereotypy frequency, eating behaviour, digestive physiology (oro-caecal transit time, digestibility) and physiological stress parameters (plasma cortisol concentrations and heart rate) in cribbers and weavers, its aim being to quantify the characteristics of horses with established stereotypic behaviours. From anecdotal and published discussions (Kennedy et al., 1993; Gillham et al., 1994; McGreevy et al., 1995; McGreevy and Nicol, 1998a; Cooper et al., 2005), we hypothesised that cribbing is most frequent during and after feeding and that weaving peaks during periods of high activity such as prior to feeding and turnout. We also hypothesised that there would be no difference in plasma cortisol concentrations or mean heart rate between stereotypic and nonstereotypic horses, as found by McBride (1996), McGreevy and Nicol (1998b), Pell and McGreevy (1999) and McBride and Cuddeford (2001). No difference in digestibility (McGreevy et al., 2001) or oro-caecal transit time (McGreevy et al., 2001; McGreevy and Nicol, 1998a) between stereotypic and control horses was expected. Despite their having visual contact with stereotypers, we did not expect any non-stereotypic controls to mimic cribbing or weaving whilst in the study (McGreevy, 1999; McAfee et al., 2002; Mills and Davenport, 2002; Waters et al., 2002). 2. Methods 2.1. Horses Seventeen adult Thoroughbred geldings were hired from their owners for use in this study. The experimental group consisted of five cribbers, six weavers and six non-stereotypic controls, aged 10.29 1.96, 11.50 2.93 and 11.17 2.21 years, respectively. All cribbers and weavers were known by their owners to have stereotyped for at least 12 months prior to recruitment into the study. As the horses were from different owners, their management and feeding regimes prior to arrival at the University were varied. In order to minimise the residual effect of the different management systems, horses arrived a minimum of 7 days prior to commencement and underwent an additional 7-day acclimatisation to the stables and routine of the trials. At the commencement of the study, bodyweights ranged from 464 to 630 kg. Mean starting weights (S.E.) for the cribbers, weavers and non-stereotypic controls were 541.2 27.0, 503.3 16.1 and 539.0 19.4 kg, respectively. These were not significantly different. The study was conducted with the approval of the Charles Sturt University Animal Care and Ethics Committee.
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2.2. Stables Horses were housed in stables (4 m 4 m), consisting of wooden paneling 1.2 m high, topped with vertical steel bars (15 mm diameter, 10 cm apart) extending a further 1.2 m. Gaps between the bars allowed olfactory, visual and tactile contact with neighbouring horses on three sides. Doors consisted of sliding front panels, preventing horses from putting their heads outside the stables. Boxes had concrete floors with sawdust as bedding and water was provided ad libitum in 60 L plastic garbage bins. All horizontal surfaces of the stables were made of metal. Since metal surfaces are rarely preferred as substrates for cribbing, a wooden bar (approximately 60 cm long, 10 cm 8 cm) was fixed to a side wall of each stable to facilitate and focus crib-biting. A standard video surveillance camera was mounted above each stable and linked to a sequential switcher and time-lapse video recorder. 2.3. Experimental design Experimental work was carried out as two identical 16-week replicates [Replicate 1 (R1) and Replicate 2 (R2)], including four cribbers, three weavers and three controls in R1 and one cribber, three weavers and three controls in R2. The horses were fed a diet of whole oats, wheaten chaff, lucerne chaff and lucerne hay, in accordance with the National Research Council (1989) guidelines at an energy concentration of 2.4 Mcal digestible energy/kg dry matter. Feed was delivered in two equal rations at 10:00 and 17:00 h each day. Horses spent 22 h per day in their stables, in accordance with usual confinement of a stabled race horse (McGreevy, 2004). For 2 h each afternoon (commencing at 13:30 h) they were given free exercise in a paddock, during which period no data were collected. Behavioural observations, sampling for plasma cortisol concentration and heart rate monitoring were carried out on all horses throughout the duration of the trial. Oro-caecal transit time and digestibility were measured only in cribbers and control horses at the end of the 4th, 8th, 12th and 16th weeks, as digestive processes have been implicated in the development and performance of cribbing behaviour (Gillham et al., 1994; McGreevy et al., 1995; Redbo et al., 1998; Waters et al., 2002; Bachmann et al., 2003). 2.4. Behavioural measurements Video surveillance was carried out on all horses for the 22 h they spent in the stables each day, for the duration of the 16 weeks of the study. A sequential switcher was attached to the camera system, meaning that each horse was filmed for 30 s in every 5 min period. The complete footage was analysed and a tally system was used to record the behavioural observations. Frequency of each behaviour type was recorded, along with the hourly distribution of cribbing and weaving. Distribution data were analysed to determine the effect of stable activity (pre-feeding, post-feeding, pre-turnout) on cribbing and weaving frequency. Table 1 gives a summary of the behaviours that were measured. Food intake was calculated by removing and weighing of any feed remaining in the stable prior to delivery of the morning ration. Water buckets were filled each afternoon, and the volume of water required to refill them on the following afternoon was measured to give an indication of how much water had been consumed. 2.5. Physiological measurements Venous blood samples for cortisol measurement were taken from each horse every second morning at 09:00 h. Plasma cortisol assays were carried out using cortisol RIA assay kits (Active Cortisol RIA DSL2100, Diagnostic Systems Laboratories, Texas, USA). Average daily heart rate (excluding turnout time) was measured for each horse throughout the duration of the trial, using heart rate monitors (Polar Accurex PlusTM, Polar ElectroTM, Finland) attached to regular lunge rollers. Bodyweight was measured every week, using a walk-on weighbridge, after removal from the paddock and prior to delivery of the evening meal at 17:00 h.
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Table 1 Behaviours of stabled horses, measured during analysis of video footage, with definitions for the purpose of this study Behavioural label
Definition for the purpose of this study
Cribbing
Horse latching onto a solid object with its incisors, arching its neck and pulling backwards. Each single repetition of this behaviour was counted as one repetition on the tally Repetitive swinging of the horse’s head and neck from side to side. Each time the horse returned to the left extreme of their swinging motion was counted as one repetition on the tally Standing with head down and muzzle in feed bin Standing with head down and lips sifting through bedding Standing with head down and muzzle in water bucket Lying down, either laterally or sternally Tail raised with posturing for defaecation Tail raised with posturing for urination Rubbing of any body parts on the walls of the stable
Weaving
Eating Foraging Drinking Recumbency Defaecation Urination Rubbing
Oro-caecal transit time was measured using the method developed for use in horses by McGreevy and Nicol (1998a). Horses were orally dosed with a sulphasalazine paste (Salazopyrin, Kabi Pharmacia Ltd., Milton Keynes, UK) at a rate of 50 mg/kg, followed immediately by delivery of the morning feed ration. After a baseline pre-feeding blood sample was withdrawn, sequential samples were withdrawn from each horse every 30 min for the following 7 h, to determine when absorption of the sulphasalazine, which can only occur from the caecum, could first be detected. Sulphapyridine was detected by HPLC, as described by McGreevy and Nicol (1998a). The threshold of first appearance was set at the point where the ratio of sulphapyridine to internal standard (sulphamethazine) reached 0.02. Digestibility was determined by measuring n-alkane concentrations in feed and faeces, using the method described by Mayes et al. (1986) and modified by Dove (1992). Horses were accustomed to wearing faecal collection harnesses (EquisanTM, Australia) during the 7-day acclimatisation period, and wore these throughout the trial (excluding turnout time). Grab-samples of faeces were removed from the faecal collection harness every 6 h for a period of 48 h during weeks 4, 8, 12 and 16. Feed and faecal samples were subsequently frozen at 4 8C, then oven dried to a constant weight at 60 8C prior to grinding through a 1 mm sieve using a cyclone sample mill. Determination of alkane concentrations was carried out using the alkane extraction method described by Dove (1992). Values for C31 were used in the analysis, as the concentration of this alkane is high in feed and faeces. C31 concentrations also had the greatest correlation between feed values and faecal values. Raw data were corrected for faecal recovery, using the recovery value of 94.0 2.8% reported by O’Keefe and McMeniman (1998). 2.6. Statistical approach Analysis was performed using software by Statistical Analysis Systems (Version 8, SAS Institute Inc., Cary NC). All P values are based on Type III sum of squares. Behavioural data are presented as frequency of occurrence. Daily frequency of stereotypy was determined using multivariate analysis of variance for repeated measures. Observations of stereotypy in each horse were treated as repeated measures. The data were checked for normality. If they were not normal, a non-parametric test which is appropriate for data not normally distributed (Wilcoxin rank sum test) was applied. All data were analysed in two stages. In stage 1, all observations were treated as independent and the data were analysed using ANOVA to indicate any effect of behavioural group. Where no group effects were indicated for a particular variable, no further analysis of that variable was conducted. If stage 1 analysis indicated a probable group effect, then further analysis was conducted in stage 2, to accommodate the fact that the observations were not truly independent (up to four observations were made on each horse, for weeks 1–4, weeks 5–8, weeks 9–12 and weeks 13–16 of the trial). Thus, in stage 2
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repeated observations made on the same animal were pooled, and the analysis was repeated. The results of stage 2 analysis are reported in this paper. Arithmetic means are presented standard error.
3. Results 3.1. Behaviour Cribbers were observed to crib-bite 147.0 33.1 times per daily period of observation. Since horses were each only observed for 10% of the 22 h that they were in the stables each day (132 min of observation per day in total), the actual cribbing frequency is likely to have been approximately 1470 events per horse per day, assuming behaviour was evenly distributed throughout each 5 min block. Weavers were observed to weave 53.0 12.4 times per daily period of observation, equating to a daily weaving frequency of approximately 530 events per horse. No stereotypic behaviour was observed in any of the control horses for the duration of the study. Analysis of the distribution of cribbing behaviour before and after the delivery of concentrated food revealed a significant change (P < 0.001) in frequency over this period, with 2.6 0.9 events observed in the hour prior to feeding, compared with 4.3 0.8 observed events per hour in the 2 h immediately following feeding, and 10.0 1.7 observed events per hour in the period 2– 4 h following feeding. Cribbing frequency continued to increase slightly for up to 8 h following
Fig. 1. Daily distribution of stereotypy frequency in stabled horses (bars show S.E.). a, b, c, A, B, C: means on a line with different superscripts differ (P < 0.001).
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Table 2 Summary of ethological responses of stabled horses by behavioural group Ethological response
Controls (mean S.E.)
Cribbers (mean S.E.)
Weavers (mean S.E.)
P value
Stereotypy frequency (events/daily observation period) Eating frequency (events/daily observation period) Time taken to consume ration (h) Foraging frequency (events/daily observation period) Drinking frequency (events/daily observation period) Water intake (L/day) Recumbency (events/daily observation period) Rubbing frequency (events/daily observation period) Urination (events/daily observation period) Defaecation (events/daily observation period)
0.0 0.0 44.1 2.14 5.38 0.41 a 28.4 2.85 1.32 0.45 17.25 0.75 22.42 2.97 0.20 0.07 0.72 0.10 0.72 0.11
147.0 33.1 51.5 2.68 9.01 0.94 b 16.6 2.51 1.56 0.59 18.75 2.32 17.33 2.88 0.68 0.19 0.60 0.12 0.68 0.11
53.0 12.4 59.8 3.28 9.6 1.07 b 19.8 3.33 0.89 0.25 15.4 2.12 18.98 2.28 0.18 0.05 0.75 0.11 0.85 0.11
0.079 0.121 <0.001 0.252 0.549 0.458 0.533 0.181 0.594 0.669
Means in a row with different letters differ. Daily observation period refers to 132 min of observation per day
delivery of the meal, with a peak of 11.6 2.1 observed events in the period 6–8 h following delivery of the ration. Cribbing frequency gradually declined until it reached baseline levels again prior to delivery of the morning concentrated ration (Fig. 1). Observed hourly weaving behaviour was significantly more frequent (P < 0.001) in the hour prior to delivery of the morning ration (16.4 3.0 events per hour, at which time the researcher was present, taking blood samples and emptying faecal collection bags), when compared with the rest of the day (1.62 0.51 events per hour). Weaving frequency in the hour prior to turnout was also significantly greater (P < 0.05), at 5.9 2.4 observed events per hour, than the frequency observed during the rest of the day (Fig. 1). All horses consumed their entire daily ration. There were no significant differences in eating frequency among behavioural groups. However, cribbers and weavers took significantly longer to consume their ration than controls (Table 2). Cribbers and weavers were observed to eat for a period of up to 2 h following delivery of the ration, followed by repeated breaks from eating for periods of up to 3 h. There was no effect of behavioural group on water intake, temporal distribution and frequency of drinking, frequency of foraging, recumbency, rubbing, urinating or defaecating (Table 2). 3.2. Physiology Plasma cortisol concentration (mg/dL) and average heart rate were not significantly different between cribbers, weavers and controls (Table 3). There was a trend (P < 0.1) towards a faster Table 3 Summary of physiological responses by behavioural group Physiological response
Controls (mean S.E.)
Cribbers (mean S.E.)
Weavers (mean S.E.)
P value
Plasma cortisol concentration (mg/dL) Heart rate (beats/min) OCTT (min) Digestibility Weight gain (kgs)
0.79 0.05 38.47 0.71 137.0 8.0a 0.52 0.04 46.0 11.9
0.80 0.06 39.49 0.59 110.0 6.3b 0.58 0.17 41.7 7.14
0.83 0.06 38.04 0.65 – – 32.4 5.74
0.184 0.333 <0.1 0.332 0.580
Means in a row with different superscripts differ.
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oro-caecal transit time in cribbers than in normal horses. There was no significant effect of behaviour type on digestibility or weight gain (Table 3). 4. Discussion No stereotypic behaviour was observed in any of the control horses in this study, despite visual contact with stereotypic horses. This short-term finding supports the research of Marsden (1995) and McGreevy (1999), which suggest that horses do not learn these behaviours by mimicry. The timing of the most concentrated periods of weaving, in the hour prior to feeding and prior to afternoon turnout, adds weight to the suggestion that weaving is more directly related to barrier frustration prompted by excitement or anticipation of an event, rather than to dietary factors or lack of environmental stimulation. As the horses in this study were housed in stables that allowed social contact between neighbouring horses at all times, visual isolation from conspecifics seems unlikely as a proximate cause of weaving in these horses. The finding that cribbers stereotype most frequently during and particularly following consumption of meals supports the results of other researchers (Kennedy et al., 1993; Gillham et al., 1994; McGreevy et al., 1995; McGreevy and Nicol, 1998a; Cooper et al., 2005). However, the peak cribbing frequency in the current study began 2–4 h post-feeding and reached its highest point 6–8 h post-feeding, which is a longer time-frame than previously reported. This suggests that gastric pain was not the sole source of any visceral discomfort that cribbers underwent in the current study. If cribbing is indeed a response to visceral discomfort, it appears more probable from the current data, that it is related to fermentative acidosis in the hindgut, since the commencement of the period of maximal post-feeding cribbing (between 2 and 8 h post-feeding) coincided temporally with the initial arrival of ingesta in the caecum (approximately 110 min post-feeding). Interspersion of eating with bouts of crib-biting may be related to attempts to normalise digestion in the foregut. Pauses in eating by cribbers and weavers and lengthy periods taken to fully consume the ration may also reflect abdominal discomfort, such as that which might be caused by gastric ulceration (Nicol, 1999) or hindgut acidosis (Johnson et al., 1998). Equally, cribbers and weavers may have a reduced motivation or ‘‘behavioural need’’ to feed that resulted in slower eating. This hypothesis would contrast with those put forward by previous authors (Hughes and Duncan, 1988; Broom and Kennedy, 1993; Wu¨rbel et al., 1998; Henderson and Waran, 2001), who suggested that there may be a behavioural need for feeding and/or foraging behaviour to be expressed, leading to the development of oral movements such as cribbing in horses under intensive management. Slower eating can also be associated with either subclinical dysphagia or satiation (McGreevy, 2004). It has been proposed that, in foals at least, cribbing may be a homeostatic response to food reaching the inflamed gastric lining found to be common amongst cribbers (Nicol, 1999; Nicol et al., 2002). However, the peak of cribbing frequency in the current study began 2–4 h postfeeding and reached its highest point 6–8 h post-feeding. This suggests that gastric pain was not the primary source of any putative visceral discomfort in cribbers. That said, it is also possible that there is a cumulative effect of concentrated food reaching the inflamed gastric lining, resulting in greater discomfort as the horse continues to eat for up to 9 h after delivery of the ration. Cribbers tended to have a shorter oro-caecal transit time than control horses. This differs from the findings of McGreevy and Nicol (1998b), who have suggested that cribbing may help to shorten oro-caecal transit time in horses that would otherwise have a slow rate of passage through
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the foregut, resulting in a decrease in their oro-caecal transit time to within a normal range. In the current study, it is possible that cribbing may have shortened oro-caecal transit time even more than has been reported previously. The absence of any difference in plasma cortisol concentrations and average heart rates between cribbers, weavers and control horses supports the findings of McBride (1996), McGreevy and Nicol (1998a), Pell and McGreevy (1999), and McBride and Cuddeford (2001). No comment can be made from this study regarding whether stereotyping has a long term stressreducing effect, as the horses involved were mature and had been observed stereotyping for at least 12 months prior to the study. A longitudinal study of circulating cortisol concentrations in a large population of young horses, with commencement prior to stereotypy development, would be more likely to reveal any effects of stereotypy development on physiological stress responses. 5. Conclusion It appears from the current study that stereotypy in mature, established cribbers is linked to feed consumption and that weaving is linked to anticipation or periods of high environmental activity. The temporal coincidence between arrival of ingesta in the caecum and commencement of the peak cribbing period suggests that there may be a link between cribbing and caecal fermentation. The theory that cribbing occurs in stabled horses as a result of a behavioural need to feed is questioned by this research, particularly as cribbing occurred while feed was still available. In order to obtain a clearer understanding of the ontogeny and functional significance of stereotypies in horses, the authors suggest the use of longitudinal physiological and behavioural studies using large groups of age-matched young horses, so that any digestive or stress-related effects can be elucidated during the emergence of stereotypic behaviours. Acknowledgements The authors would like to acknowledge the financial contribution of the NSW Racing Research Fund. Prof. Martin Sillence, Kellie Munn, Dr Hugh Dove and Terry Flynn are thanked for their technical assistance with sample and data analysis. Thanks also to the owners for the loan of the horses studied in this research. References Bachmann, I., Audige, L., Stauffacher, M., 2003. Risk factors associated with behavioural disorders of crib-biting, weaving and box-walking in Swiss horses. Equine Vet. J. 35, 158–163. Broom, D.M., Kennedy, M.J., 1993. Stereotypies in horses: their relation to welfare and causation. Equine Vet. Educ. 5, 151–154. Cooper, J.J., McDonald, L., Mills, D.S., 2000. The effects of increasing visual horizons on stereotypic weaving: implications for the social housing of stabled horses. Appl. Anim. Behav. Sci. 69, 67–83. Cooper, J.J., Mcall, N., Johnson, S., Davidson, H.P.B., 2005. The short-term effects of increasing meal frequency on stereotypic behaviour of stabled horses. Appl. Anim. Behav. Sci. 90, 351–364. Dove, H., 1992. Using the n-alkanes of plant cuticular wax to estimate the species composition of herbage mixtures. Aust. J. Agric. Res. 43, 1711–1724. Fraser, A.F., Broom, D.M., 1990. Farm Animal Behaviour and Welfare. Bailliere Tindall, London. Gillham, S.B., Dodman, N.H., Shuster, L., Kream, R., Rand, W., 1994. The effect of diet on cribbing behaviour and plasma b-endorphin in horses. Appl. Anim. Behav. Sci. 41, 147–153. Henderson, J.V., Waran, N.K., 2001. Reducing equine stereotypies using an EquiballTM. Anim. Welf. 10, 73–80.
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