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Effects of enrichment items on activity and social interactions in domestic horses (Equus caballus)
Applied Animal Behaviour Science 129 (2011) 100–110
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Applied Animal Behaviour Science journal homepage: www.elsevier.com/locate/applanim
Effects of enrichment items on activity and social interactions in domestic horses (Equus caballus) Grete Helen Meisfjord Jørgensen ∗ , Silje Hanche-Olsen Liestøl, Knut Egil Bøe Norwegian University of Life Sciences, Department of Animal and Aquacultural Sciences, P.O. box 5003, 1432 Ås, Norway
a r t i c l e
i n f o
Article history: Accepted 2 November 2010 Available online 3 December 2010 Keywords: Horse Activity Behaviour Item Enrichment Social interactions
a b s t r a c t The aim of this study was to investigate the use of items intended to provide enrichment during turnout, both for individual and group kept horses in an attempt to reduce the amount of passive behaviours. The study was divided into two parts, where study 1 involved eight horses rotated through eight individual paddocks, each containing one of seven enrichment items and one paddock being kept without item, functioning as a control. The horses’ item-directed behaviours; passive behaviours or other non-item related activities were scored using instantaneous sampling, every minute for 1 h at the beginning and the end of the turnout period. Study 2 involved six horse groups (3–6 horses) and the same scoring methods and ethogram as in study 1. The four items that the horses interacted the most with during study 1 (straw STRA, ball filled with concentrates CBALL, branches BRAN and scratching pole POLE) are investigated in study 2. In addition, the amount of social interactions was recorded. Both horses kept individually (P < 0.05) and in groups (P < 0.0001) performed significantly more item-directed behaviours towards edible items like STRA and CBALL than other objects. There was, however, no overall relation between the numbers of item-directed behaviours and the number of passive behaviours observed, indicating that the enrichment items did not alone reduce the amount of passive behaviours during turnout periods. Such a reduction was, however, only apparent when horses spent more time eating green leaves growing on the paddock surface (R = −0.97 study 1, R = −0.67 study 2, P < 0.0001). Access to STRA in group kept horses also seemed to reduce the amount of agonistic behaviours (P < 0.0001). In conclusion, if grass is not available in paddocks, the provision of roughage reduces the amount of passive behaviours in singly kept horses and it also reduces the risk of agonistic interactions between horses kept in group. © 2010 Elsevier B.V. All rights reserved.
1. Introduction Turnout is generally regarded as positive for horses, as it gives opportunity for fresh air and voluntary exercise which is important for developing strong bones, joints and improving long term health in general (e.g. Dykgraaf et al., 2008; Rogers et al., 2008). However, experiments have shown that horses’ activities in such paddocks are rather
∗ Corresponding author. Tel.: +47 64 96 51 42; fax: +47 64 96 51 01. E-mail address: [email protected] (G.H.M. Jørgensen). 0168-1591/$ – see front matter © 2010 Elsevier B.V. All rights reserved. doi:10.1016/j.applanim.2010.11.004
limited and mostly linked to feed (Jørgensen and Bøe, 2007a). Longer periods of confinement increases the horses activity when turned out (Chaya et al., 2005), and when horses are actively exercised they become more passive during turnout (Jørgensen and Bøe, 2007a). Interestingly, horses display significantly more active behaviours when turned out in social groups compared to when kept individually (Jørgensen and Bøe, 2007b). Barren environments and social isolation have also been linked to many equine behavioural problems (Luescher et al., 1991; Waters et al., 2002) and stereotypies (e.g. weaving: Cooper et al., 2000). Despite this, the most common way of housing horses is
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still in individual tie-stalls or boxes inside barns (Bachmann and Stauffacher, 2002; Søndergaard et al., 2002). Welfare regulations in several countries demand that horses are given daily access to an outdoor paddock (e.g. Norway: Landbruks og matdepartementet, 2005), Denmark even recommends that young horses are kept in groups until they reach sexual maturity (Søndergaard et al., 2002). Even so, many horse owners prefer to keep their horses individually in paddocks during turnout, probably due to an unwarranted fear of injuries from social interactions (Grogan and McDonnell, 2005; Jørgensen et al., 2009). Several studies have linked low reactivity and passive behaviours to a passive coping strategy and apathy that is probably related to high rather than low stress sensitivity (Koolhaas et al., 1999; review: Koolhaas, 2008; Nagy et al., 2009). In horses this means that passive horses might be prone to developing stereotypic behaviours like crib-biting (Nagy et al., 2010). In an attempt to reduce boredom, apathy and the risk of developing stereotypic behaviours, different objects, toys or feedstuffs are now commercially available. Only a few of these have been scientifically tested and only individually stabled horses where then used (Winskill et al., 1996; Henderson and Waran, 2001). A study on horses’ use of the “Edinburgh Foodball” revealed a reduction in concentrate ingestion, movement, nosing of bedding material and standing compared to control observations (Winskill et al., 1996). A significant reduction in time spent performing stereotypic behaviours was also found when testing the same feeding device on stabled horses displaying some form of stereotypic behaviour (Henderson and Waran, 2001). Newberry (1995) defined environmental enrichment as: “an improvement in the biological functioning of captive animals resulting from modifications to their environment”. There is, however, no standard criteria for assessing whether access to an object or item functions as enrichment for the animal in question. Studies on environmental enrichments for other domestic animals emphasize that such enrichments should stimulate foraging and exploratory behaviour (e.g. pigs: Van de Weerd et al., 2003) and further studies on pigs report a higher degree of manipulation of edible items like straw compared to other commercial objects like a “Bite Rite” chewing toy (Van de Weerd et al., 2005, 2006). Environmental enrichments could be divided into four sub-categories: foraging opportunities, structural complexity, sensory stimulation/novelty, and social companionship (Newberry, 1995). In addition to provision of forage, the complexity of diets are important (Thorne et al., 2005) and objects could be provided that enable animals to groom or scratch in places they cannot reach themselves, as shown by the use of mechanical brushes for cattle (DeVries et al., 2007). The aim of this experiment was to investigate the use of enrichment items during turnout, both for singly and group kept horses. We hypothesized that horses would react differently to edible items compared to other nonedible items. From this we predicted that:
- Horses would show more item-directed behaviours towards edible items.
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- Horses would display less passive behaviours when given edible items. We also hypothesized that horses in groups would react differently to items of “enrichment” than individually kept horses, and predicted that: - Horses in groups would pay less attention to items than horses kept individually. 2. Materials and methods Two different studies were performed. The first and preliminary study aimed to discover which items individually kept horses would interact with, while in study 2 the four most popular items from the preliminary study were tested in six different groups of horses. 2.1. Study 1—horses kept individually Experiments were done during October and November 2008 in the south-eastern parts of Norway. A large stable located in Akershus County with singly kept horses was recruited by direct contact initiated by the researchers. 2.1.1. Experimental design A total of eight horses were individually turned out into eight paddocks and given access to one of the enrichment items for 1 day (7 h), before being randomly rotated to another paddock with another item the next day, functioning as their own control. This was repeated for 8 days until all horses have had access to all paddocks, functioning as their own control. The enrichment items used were divided into two categories; edible items: peat soil (PEAT), straw (STRA), a pile of branches (BRAN), a ball filled with concentrates (CBALL) or objects: a cone (CONE), a ball (BALL), a scratching pole (POLE), while the last paddock was barren, without enrichment items for control (CONT). 2.1.2. Animals and feeding Eight riding horses (7 warmblood horses and 1 sport pony, 4 mares and 4 geldings), aged 6–18 years old (mean age 11 years) were randomly selected from the population of 25 privately owned horses at the stable. Both before and during the experiment, all horses were regularly ridden in disciplines like dressage, jumping or trekking 1–2 h per day and were kept individually in standard sized boxes (3 m × 3 m) inside an insulated building during night (15:00–08:00). Every day after morning feeding, horses were turned out into the paddocks for 7 h (8:00–15:00). The horses were fed an individually adjusted diet of hay (4 times/day) and concentrate feed (2 times/day). Two of these hay meals were administered while the horses were outside in the paddocks, between observation periods. All horses were wearing blankets and halters during turnout and no horses displayed any form of stereotypic behaviours. 2.1.3. Paddocks The paddocks measured in average >10 m × >20 m (range 231–465 m2 ), and no physical contact was possi-
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Fig. 1. Experimental periods (horizontal arrows) and observation times (vertical arrows). Control observations are shown in yellow arrows. The order of items was random, this is only an example. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of the article.)
ble between horses. The ground consisted of mainly clay and topsoil, but despite the fact that all paddocks were in daily use, some very small plants (mainly common horsetail, Equisetum arvense) could be found. 2.1.4. Treatment items A detailed description of the seven enrichment items can be found in Table 1, and we chose to divide the items into two categories according to if they were edible or not. The items were placed in the middle of each paddock, allowing horses to approach them from all directions. The PEAT and POLE were permanent items in their designated paddocks, while all other items were given just before observations started each day and removed at the end of the last observational period. One day of observations for the POLE item was lost due to it being broken. 2.1.5. Behavioural observations The horses’ behaviour and contact with the items were scored instantaneously every minute for 1 h (morning: 10:00 to 11:00) at the beginning of the turnout period and 1 h at the end of the turnout period (afternoon: 14:00 to 15:00) each day. A total of 19 mutually exclusive behaviours were recorded, and these were later organized into the 3 categories according to item or non-item directed behaviours (Table 2). Weather, temperature and surface conditions were recorded at the start of every observation period. 2.2. Study 2—horses kept in groups
turned out into the experimental enclosures for 3 days in order to get acclimatized to the new social situations. Then the horse groups were exposed to one of four enrichment items at a time in their enclosure; STRA, CBALL, BRAN and POLE, in a randomized order and each experimental period lasted 4 days (Fig. 1). A fifth experimental period at the end of the experiment served as control (CONT) with no additional item. 2.2.2. Animals and feeding In groups 1, 2, 5 and 6 the horses were singly stabled indoors during night and turned out in groups, 6–7 h per day, while groups 3 and 4 were kept outdoors in their paddock 24 h a day. All horses within each group were familiar with each other and had been together for at least 3 weeks prior to the study. Groups 1 and 2 consisted of only geldings whereas groups 3–6 contained both mares and geldings. No stallions were used in the study, and groups consisted of mostly adult horses (mean age 11.3 years) ranging from 2 to 29 years old. Horse breeds varied from Norwegian Døla horses (∼500 kg) to Icelandic horses (∼300 kg), and they were used and exercised as normal during the experimental period, but only after the observations and turnout time were completed. Most of the horses wore halters and blankets during turnout, depending on the weather. Groups 3 and 4 had permanent access to shelter and were fed (3 times/day) from hayracks mounted on the shelter wall; while the rest of the groups were fed meals of hay on the ground (one meal was given during turnout while morning and evening meals were given inside the stable). Feed rations consisted mostly of several kilograms of hay per horse and concentrates were given only to supplement the energy from the roughage. All horses were able to feed at the same time, and had ad libitum access to water.
A total of 13 stable owners contacted the researchers and wished to participate in our study, after we had advertised through a popular Norwegian horse webpage (www.hest.no). Three of these stables were selected on the following criteria: (1) have privately owned horses that were kept in groups of three individuals or more, for at least 6 h daily and (2) stable located less than 1 h drive from the Norwegian University of Life Science. On each of the three farms, two groups of horses were selected at random.
2.2.3. Experimental enclosures The mean enclosure space was 1577 m2 /horse ranging from 262 to 5833 m2 /horse and the surface mainly consisted of topsoil and clay that became somewhat muddy after heavy rains.
2.2.1. Experimental design During the experiment, in November; the number of horses in the original groups was reduced so that each of the six groups now consisted of three or four horses, except for group number four that had six horses. Horse groups were
2.2.4. Behavioural observations The behaviour of the horses was recorded live by an observer the first (day 1) and last day (day 4) of each experimental period for 1 h (between 08:00 and 12:00) using instantaneous sampling every minute. One 1-h baseline
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Table 1 Description of the enrichment items used. Additional item
Description
Brand
Size
CONE
Red, soft plastic, marked with Gaffa tape in two horizontal stripes around the body of the cone to make a different appearance.
Hööks Hestesport
31 cm tall, standing on a 19 cm × 19 cm plate
BALL
Hard plastic ball with two small holes of 1.5 cm in diameter.
Canac activity ball
25 cm in diameter
POLE
A wooden fencing pole 8.0 cm in diameter, 1.40 m tall was driven well into the ground. A rubber scratching mat was fixed around the upper parts of the pole and a short haired, stiff brush was fixed on top of the pole with the bristle facing up.
Scratching mat from Hööks Hestesport (30 cm x 50 cm)
1.10 m tall
PEAT
40 l were placed in a pile directly on the ground.
Herbia
5.0 l added each day
STRA
Straw of barley placed directly on the ground.
BRAN
The branches were between 1.0 and 3.5 cm in diameter at the point where they were cut, measuring 1.0–2.0 m long.
Norway spruce (Picea abies) Birch (Betula) Sallow (Salix caprea)
2 branches of Spruce and 3 branches of Birch and Sallow. Fresh each day
CBALL
Same as BALL, but filled with 0.5 kg standard concentrate feed for horses.
Canac activity ball
25 cm in diameter
Objects
Edible items
2.0 kg fresh each day
Picture
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Table 2 Ethogram of behaviours scored both during study 1 and 2. Categories and underlying behaviours
Description
Item directed behaviours Watching the item The horse is standing with eyes fixed on the item. Walking towards the The horse is moving towards the item, with item eyes fixed on the item. Sniffing the item The horse is standing with head very close to the item and is sniffing or blowing air (identified by the characteristic sound). Examining the item The horse is standing with muzzle in physical with muzzle contact with the item, but not chewing on it or making sniffing/blowing sounds. Chewing on the item The horse is standing close to the item and is chewing on it, parts of the item inside the mouth. Chewing The horse is not chewing on the item itself concentrates from (CBALL) but is eating concentrates that has CBALL fallen out of the CBALL. Pushing the item The horse is using its head or muzzle to push with muzzle/head the item so that it visibly moves. Touching the item The horse is in physical contact with the item with front legs with its front leg (often a scraping, pushing or digging motion). Rubbing body against The horse is rubbing parts of the body (head, POLE neck, chest, sides or rump) against the scratching pole. Keeping a distance to The horse is standing as far away from the the item item as possible, keeps eyes and ears fixed towards the item while head and tail are raised. Horse seems frightened. Passive behaviours Standing, not watching the item Lying
The horse is standing relaxed without directing any attention towards the item. The horse is lying on the ground.
Other non-item related activities Sniffing the ground The horse is standing or moving around with its muzzle in contact or very close to the ground. Eating The horse is eating/grazing or chewing on other things than the item. Drinking The horse stands with its muzzle in the water bucket. Rolling The horse lies on the ground and is rolling from side to side, rubbing its back and sides against the ground. Moving The horse is walking or running around in the paddock, not paying attention to the item. Eliminative The horse is urinating or defecating. behaviour Self grooming The horse is using its teeth, hoofs, legs or muzzle to scratch itself in other parts of the body. Other The horse is showing other behaviours not described in the ethogram (for example stereotypes).
observation was performed before, and one after groups were introduced to all enrichment items was pooled in order to provide control measures of horses’ activity and social behaviours (Fig. 1). We used the same ethogram as in study 1 (Table 2), but also added a category for any social interaction if this was seen during the scan. In addition, every event of social interactions was recorded continuously in a separate dataset using a modified ethogram from Christensen et al. (2002) (Table 3).
Table 3 Ethogram of social interactions (adjusted from Christensen et al., 2002). Behaviours
Description
Agonistic behaviours Displacement Approach of one horse causes another to move away (at least 3 m) so that distance is maintained or increased, without overt aggression (also termed retreat/avoidance, depending on whether receiver or sender is noted). Chase One horse chases another (trotting or galloping) with ears laid back. Mouth clapping Submissive behaviour. Opening and closing mouth with lips retracted. Typically, the head and neck are extended, and the ears oriented back or laterally (also termed snapping). Threat to bite Bite intention movement with ears back and neck extended, with no actual contact. Threat to kick Kick intention movement, performed by swinging rump or backing up, AND waving or stamping hind leg towards another horse, without making contact. Backing The horse backs towards another horse with ears laid back. Physical contact may or may not be obtained. Bite Opening and rapid closing of the jaws with actual contact to another horse’s body. The ears are back and lips retracted. Kick One or both hind legs lift off the ground and rapidly extend backwards towards another horse, with apparent intent to make contact. Push Pressing of the head, neck, shoulder, chest, or body against another horse, causing it to move one or more legs to regain balance. Friendly behaviours Head rest A horse rests its head on the rump or back of another horse. May involve a gentle rubbing of the head against the body of the other horse. Play Play directed at another individual, which may or may not reciprocate; includes low intensity play movements such as nipping, grasping, and pulling mane or tail. Play fight High intensity play, which is reciprocated by one or more partners; includes vigorous play movements such as rearing, boxing, circling, kneeling, and chasing. Social grooming Reciprocal coat care in which the partners stand beside one another, usually head-to-shoulder or head-to-tail, grooming each other’s neck, mane, rump, or tail by gently nipping, nuzzling, or rubbing.
The actor and receiver of these social interactions were noted, in order to detect individuals being mobbed or mobbing other group members. Because of few recordings, the actor social interactions were later pooled into agonistic behaviours and friendly behaviours. 2.3. Statistical analysis The distribution of each response variable was tested using goodness of fit analysis in JMP® 7.0 statistical software. The effect of different enrichment items on the behaviour of individual horses during study 1 was analysed using the Glimmix procedure with the following class variables: additional item (CONT, PEAT, STRA, CONE, BALL, CBALL, POLE or BRAN) and observation time (morning or afternoon in 1 day turnout period). The interaction between
Exact tests of differences between means could not be performed using LS-means due to the limited number of observations within some item-treatments. The degrees of freedom are different for tests on “item-directed behaviours” because this data are Lognormal distributed compared to Poisson distribution of data on “passive” and “other non-item related behaviours”.
a
0.4 b 4.1 a 3.9 b 1.5 a ± ± ± ± 1.7 38.9 52.8 6.5 29.4 ± 3.9 b 64.8 ± 3.8 a 5.7 ± 1.3 b Study 2. Horses in groups Item-directed behaviours Passive behaviours (Standing or lying) Other non-item related activities Social interactions
b
<0.0001 <0.0001 <0.0001 <0.0001 F3,92 = 11.3b F4,212 = 59.4 F4,212 = 63.8 F4,212 = 19.4 4.7 a 3.0 c 4.8 b 1.6 b ± ± ± ± 26.0 19.3 50.2 4.5 0.7 b 4.0 c 3.9 a 1.4 a ± ± ± ± 2.8 22.4 68.4 6.2 3.5 a 4.2 a 4.4 c 0.8 c ± ± ± ± 23.7 33.2 41.0 1.9
<0.05 <0.0001 <0.0001 F6,27 = 2.9b F7,104 = 38.9 F7,104 = 26.9 13.7 ± 4.8 35.0 ± 4.8 b 51.2 ± 4.5 c 6.3 ± 1.9 54.7 ± 6.0 a 38.9 ± 5.9 c 20.0 ± 5.7 22.4 ± 4.5 d 57.4 ± 4.9 b 0.1 ± 0.1 34.6 ± 6.3 b 65.2 ± 6.3 ab 2.1 ± 1.9 40.7 ± 5.9 b 57.0 ± 6.0 b 0.3 ± 0.2 30.9 ± 6.8 bc 68.7 ± 6.7 ab
P-Value F-Value Straw (STRA) Branches (BRAN) Ball with concentrates (CBALL) Peat (PEAT)
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0.4 ± 0.2 24.0 ± 6.7 cd 75.5 ± 6.8 a Study 1. Horses in individual paddocks Item-directed behavioursa Passive behaviours (Standing or lying) 52.5 ± 7.2 a Other non-item related activities 47.4 ± 7.2 c
3.1.2. Passive behaviours Time spent standing or lying ranged from 22 to 55% of total observations and this passive behaviour was more prevalent in CONT and BRAN treatment, than during STRA and CONE treatments (Table 4). Generally, the horses showed more passive behaviours after 4–5 h with the item than straight after the item were introduced, in all treatments except when given the BRAN item (Fig. 2b). A significant interaction effect between addi-
Scratching pole (POLE)
3.1.1. Item-directed behaviours The horses spent significantly more time (in average 13.2% vs. non-edible items: 0.9% of tot. obs.) performing item-directed behaviours when exposed to edible items like straw (STRA), the ball with concentrates (CBALL) and branches (BRAN) (Table 4). The other items, however, were rarely touched by the horses, but this was probably not related to horses being afraid of the items since no events of “Keeping distance to items” were seen. In the CBALL-treatment the horses spent most of the time either chewing concentrates that had fallen out of the ball (9.8 ± 4.0%) or sniffing the ground behind the ball (7.5 ± 2.7%). Horses seemed, however, to lose interest in the items over time since significantly more item-directed behaviours were observed straight after the new item was introduced, especially for the STRA and CBALL treatment (Fig. 2a). Individual horse had no significant effect on the item-directed behaviours and no interaction effect between item and time of observation was found (F3,27 = 1.2, P = 0.3).
Ball (BALL)
3.1. Study 1—horses kept individually
Control (CONT) Cone (CONE)
3. Results
Behaviours (mean ± SE % of tot. obs.)
additional item and observation time was included in the model statement, while horse (1–8) was specified as a random effect (Schabenberger, 2007). A Glimmix model of analysis of variance was used when testing the effect of enrichment items on group kept horses during study 2. Here we used additional item (CONT, STRA, CBALL, BRAN and POLE), group (1–6), observation time (day 1 or day 4) and the interaction between additional item and observation time as class variables. Group was specified as a random effect. Also the effects of enrichment items on social interactions during study 2 was analysed using a Glimmix model with additional item, group, observation time and the interaction between additional item and observation time as class variables. Group was specified as a random effect. The effects of enrichment items on number of aggressive and friendly social interactions were tested using separate datasets with a similar model. Correlations between item-directed and passive behaviours or passive behaviours and eating non-item related substrates were investigated using Spearman correlations. Differences between means were tested using LS-means with Tukey–Kramer adjustments for multiple comparisons. All model analysis was performed using the SAS® software.
Table 4 Behaviours related to enrichment items during study 1: horses in individual paddocks, and study 2: horses kept in group. Means within behaviour category that are indicated with unequal letters are significantly different (P < 0.05).
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Fig. 2. (a and b) The effect of observation time on (a) item-directed behaviours and (b) passive behaviours during study 1. Differences within treatment, between observation time are given as follows: *P < 0.05; ***P < 0.0001. Differences within observation time, between treatments are indicated by different letters (P < 0.05). ns = non-significant.
tional item and observation time was found (F7,104 = 4.9, P < 0.0001, Fig. 2b). The number of passive behaviours were, however, not reduced by an increase in number of item-directed behaviours (Fig. 3a), and only when given STRA (R = −0.62, P = 0.01) and CBALL (R = −0.52, P = 0.037) did the number of item-directed behaviours and passive behaviours correlate over observations. 3.1.3. Other non-item directed activities Other non-item related activities ranged from 47.4 to 75.5% of total observations and were mostly observed when horses were given CONE, BALL, PEAT, POLE and STRA items (Table 4). Horses were often observed eating small green leaves growing from the surface of the paddocks and when given the CONE item, more of this behaviour was observed than when given the BRAN item (Fig. 3b). This eating of non-item related substrates affected the number of passive behaviours in general (Fig. 3b) and horses given each of the items CONE (R = −0.91, P < 0.0001), Ball (R = −0.96, P < 0.0001), POLE (R = −0.80, P < 0.001) and BRAN (R = −0.83, P < 0.0001) showed significantly less passive behaviours when more non-item related eating was performed. 3.2. Study 2—horses kept in groups 3.2.1. Item-directed behaviours Horses kept in groups showed more item-directed behaviours when given edible items like STRA and CBALL
compared to POLE (Table 4), and this is similar to what we found in horses kept individually. Chewing the item was most common of the item-directed behaviours and horses chewed significantly more on STRA (23.2 ± 3.4%) than when given other edible items (CBALL: 10.3 ± 2.4%, BRAN: 2.7 ± 0.7% and POLE: 0.2 ± 0.1, F3,53 = 22.3, P < 0.001). In the CBALL-treatment, most item-directed behaviours were either chewing concentrates that had fallen out of the ball (9.8 ± 2.3%) or sniffing the ground behind the ball (6.9 ± 1.6%). We found no effect of group and no interaction effect between enrichment item and observation time, showing that contrary to our findings in individually kept horses, the group kept horses did not lose interest in the given items from day 1 to day 4. 3.2.2. Passive behaviours Most passive behaviours where recorded when horses were exposed to the POLE treatment and the least passive behaviours were recorded during the CBALL treatment (Table 4). The behaviour “standing, not watching the item” explained more than 75% of the passive behaviours in the POLE treatment, >95% in the STRA treatment and 100% in the CBALL treatment. In CONT and BRAN treatments, horses were standing 100% and >85% of the passive behaviours, respectively. The number of passive behaviours did not change from day 1 to day 4 in each experimental period
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Fig. 3. (a and b) Correlations (a) between item-directed behaviours and passive behaviours or (b) between passive behaviours and eating nonitem related substrates in horses kept singly during study 1.
in general, but for two enrichment items the horses displayed more passive behaviours after 4 days (day 1 vs. day 4: STRA: 28.8 ± 4.6% vs. 37.5 ± 7.0%; POLE: 35.9 ± 5.8% vs. 41.7 ± 5.8%). Interestingly, the opposite occurred in CONT (day 1: 31.2 ± 5.8% vs. day 4: 27.5 ± 5.4%) and BRAN (day 1: 26.4 ± 6.7% vs. day 4: 18.5 ± 4.3%) treatments (interaction effect additional item vs. observation time: F4,212 = 10.9, P < 0.0001). Similarly to what we found in study 1, the number of passive behaviours was not reduced by an increase in number of item-directed behaviours (Fig. 4a). Here, the number of item-directed behaviours and passive behaviours correlated only for the STRA item (R = −0.36, P < 0.05). 3.2.3. Other non-item related activities For group-kept horses, the non-item related activities ranged from 41.0 to 68.4% of total observations and most of these behaviours were scored when given BRAN and during CONT (Table 4). The number of non-item related activities observed did not differ from day 1 to day 4 during the experimental period and no interaction between additional item and observation time was found. Approximately 80% of these non-item related activities were scored as ‘eating green leaves from the surface’, and the least eating of non-item related substrates was found in the STRA treatment (Fig. 4b). This eating of green leaves affected the number of passive behaviours in general (Fig. 4b), and horses given each of the items STRA (R = −0.56, P < 0.0001), BRAN (R = −0.71, P < 0.0001), CBALL (R = −0.37, P < 0.01) and POLE (R = −0.92, P < 0.0001) showed signifi-
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Fig. 4. (a and b) Correlations (a) between item-directed behaviours and passive behaviours or (b) between passive behaviours and eating nonitem related substrates in horses kept in groups during study 2.
cantly less passive behaviours when more non-item related eating was performed. 3.2.4. Social interactions Number of social interactions was highest in the POLE and BRAN treatments, somewhat lower in the CBALL and CONT treatments and the lowest in the STRA treatment (Table 4). Horses in the STRA treatment showed significantly less agonistic behaviour (F4,215 = 7.2, P < 0.0001; Fig. 5) and the highest number of friendly behaviours towards each other, but this measure did not differ sig-
Fig. 5. Agonistic and friendly behaviours in relation to enrichment items given. Bars with unequal letters differ significantly within colour (P < 0.05). (For interpretation of the references to color in this figure legend, the reader is referred to the web version of the article.)
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nificantly over treatments. The major contributor to the agonistic social behaviours was ‘displacements’ (CONT: 9.5 ± 4.6%; STRA: 42.8 ± 8.8%; CBALL: 18.7 ± 6.9%; POLE: 10.3 ± 5.4%; BRAN: 15.3 ± 6.6% of all social behaviours) while the other behaviours were rarely seen. 4. Discussion Both horses kept individually and in groups performed more item-directed behaviours when given access to edible items like straw (STRA) and a ball filled with concentrates (CBALL). There was, however, no overall relation between the numbers of item-directed behaviours and the number of passive behaviours observed, indicating that the enrichment items did not alone reduce the amount of passive behaviours during turnout periods. Horses kept individually paid more attention to non-edible items like the POLE compared to horses in groups. There might be a significant effect of social facilitation explaining the finding that group housed horses directed more of their attention towards the popular STRA and CBALL items, but less attention towards the other items compared to the horses kept individually. For the POLE item on the other hand, individually kept horses may have used the POLE for scratching parts of their body that they could not reach themselves, while horses kept in groups had the option of social grooming. Horses kept in individual paddocks displayed relative high frequencies of other non-item related behaviours, most of which was identified as eating green leaves. One of the primary motivations in horses is searching for and eating grass and earlier studies have documented horses spending 40–70% of their time in such activities (Arnold, 1984; Boyd et al., 1988). This is not different in domestic horses since horses in individual paddocks without any significant grass available, still spent up to 40% of their time searching for and nibbling grass from under the fence (Jørgensen and Bøe, 2007a). Our results from study 1 demonstrated that horses displayed more non-item directed eating behaviour when given access to the CONE item compared to when given the BRAN item. The explanation for this could be related to the horses ingesting or exploring the branches but it is also probably related to very subtle differences in the amount of green leaves in each paddock. The enrichment items were kept in the same paddocks, while the horses were rotated between paddocks during study 1. These differences were, however, not detectable by the human eye, and paddocks were evaluated to be very similar before the experiment took place. Looking at the same behaviour recorded in study 2 on horses kept in groups, there was still significantly more eating of non-item related substrates when horses were given BRAN compared to when given STRA items. This difference could, however, not be explained by differences in physical properties in the enclosures since the enrichment items were randomly rotated between horse groups and the effect of group was controlled for in the statistical model. Therefore it is probable that the horses spent time chewing and eating straw (STRA) when given access to this, decreasing the motivation for searching for and eating other substrates. Provision of roughage has also been shown to reduce feeding motivation and both risk and prevalence of stereotypic
behaviours in pigs (review: Tuyttens, 2005) and horses (e.g. McGreevy et al., 1995; Thorne et al., 2005). No horses with known stereotypic behaviour patterns were included in the present study and it would therefore be interesting if further experiments would investigate the effect of similar edible items on stereotypic behaviours during turnout periods. Horses were observed to use the POLE for scratching their body relatively seldom, but we found hairs both in the brush on top and on the rubber scratching mat fixed around the pole, indicating that it had been used outside observation periods. Cattle actually increased their total scratching behaviour by over 500% after they were given access to a mechanical brush and used it extensively to scratch in places where they could not reach themselves (DeVries et al., 2007). We hypothesized that horses in groups might spend less time in contact with additional items compared to horses kept individually, since the social environment in itself might be regarded as an enrichment that provides several stimuli and the possibility for play and social grooming. The results from our study do not provide very clear evidence to support this idea. Horses in groups did certainly show more item directed behaviour to the edible items STRA and CBALL but this can be explained by the mechanism of social facilitation (Rifa, 1990). Furthermore, horses kept individually displayed more item directed behaviours towards the POLE and BRAN items (Table 4) perhaps indicating that since they had nothing else to do, they spent some time investigating the items rather than standing passively. Individually kept horses seemed to lose interest in the enrichment items over the course of the day (4–5 h), but horses kept in groups showed a similar number of item-directed behaviours the first and the fourth day of each experimental period. Observations on individually kept horses might have been influenced by the horses’ daily activity budget, resulting in the afternoon observations coinciding with a quiet time of the day. Such effects were, however, not present in study 2 as both day 1 and day 4 observations were performed before noon. It is favourable that the horses did not seem to lose interest in the items over the course of 4 days, indicating some value as an ‘enrichment’ but it is important to have several items (or piles of feed), provided in large enough quantities in order to prevent competition when given in groups (Kruger and Flauger, 2008). Our results indicate that provision of straw (STRA) reduced the number of agonistic interactions in group kept horses. One of the most common arguments against keeping horses in groups is the fear of injuries from agonistic interactions. Straw has previously been shown to reduce the risk of pigs developing harmful behaviours (e.g. Van de Weerd et al., 2005), a result supporting our finding. Ad libitum access to other forms of roughage probably have similar positive effects, but one should consider the relative risk of impaction colic if horses are given low quality roughage (Cohen et al., 1999) combined with little ability to move (stabling) (Hillyer et al., 2002). Newberry (1995) stated that for an item to be considered an environmental enrichment it should improve the biological functioning of the animal. In the present
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experiment we have not measured the horses biological functioning directly, but we found differences in behaviour indicating that ad libitum access to forage have positive effects. Looking at it from another angle put forward by Appleby (1997), we could, however, say that providing ample amounts of forage does indeed facilitate the performance of adaptive behaviours, and is therefore an important environmental enrichment for horses. These studies were performed using privately owned horses living in different stables. Despite our best efforts to standardize groups and enclosures, some differences had to be accepted. We did, however, include this effect in the statistical analysis, but could not find indications for some groups reacting differently than others to our treatments. In conclusion, even when horses were given the most popular edible items (STRA and CBALL) the amount of passive behaviours was not reduced. More time spent eating green leaves growing from the paddock surface did, however, correlate with a reduction in passive behaviours both for individually and group kept horses. Our results therefore emphasize the importance of providing horses with grass pasture or good quality roughage during turnout. When horses are kept in groups, they are influenced by social facilitation that underlines the importance of providing edible items of enrichment in several locations. When this is done correctly, the provision of straw might even reduce the risk of aggressive interactions between horses kept in groups. Based on behavioural measures alone, the provision of toys or other non-edible items does not seem to be an obvious enrichment for horses, but no negative effects were discovered either. Acknowledgements This experiment was funded by the Research committee at the Norwegian Equine Centre. We would like to thank Guro Vasdal for valuable comments on earlier versions of this manuscript. We would also like to extend our gratitude to Hallkjell Jensen and all participating horses and stable owners. Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at doi:10. 1016/j.applanim.2010.11.004. References Appleby, M.C., 1997. Life in a variable world: behaviour, welfare and environmental design. Appl. Anim. Behav. Sci. 54, 1–19. Arnold, G.W., 1984. Comparison of the time budgets and circadian patterns of maintenance activities in sheep, cattle and horses grouped together. Appl. Anim. Behav. Sci. 13, 19–30. Bachmann, I., Stauffacher, M., 2002. Housing and exploitation of horses in Switzerland: a representative analysis of the status quo. Schweiz. Arch. Tierheilkd. 144, 331–347. Boyd, L.E., Carbonaro, D.A., Houpt, K.A., 1988. The 24-hour budget of Przewalski horses. Appl. Anim. Behav. Sci. 21, 5–17. Chaya, L., Cowan, E., McGuire, B., 2005. A note on the relationship between time spent in turnout and behaviour during turnout in horses (Equus caballus). Appl. Anim. Behav. Sci. 98, 155–160.
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Christensen, J.W., Ladewig, J., Søndergaard, E., Malmkvist, J., 2002. Effects of individual versus group stabling on social behaviour in domestic stallions. Appl. Anim. Behav. Sci. 75, 233–248. Cohen, N.D., Gibbs, P.G., Woods, A.M., 1999. Dietary and other management factors associated with colic in horses. J. Am. Vet. Med. Assoc. 215, 53–60. Cooper, J.J., McDonald, L., Mills, D.S., 2000. The effect of increasing visual horizons on stereotypic weaving: implications for the social housing of stabled horses. Appl. Anim. Behav. Sci. 69, 67–83. DeVries, T.J., Vankova, M., Veira, D.M., von Keyserlingk, M.A.G., 2007. Short communication: usage of mechanical brushes by lactating dairy cows. J. Dairy Sci. 90, 2241–2245. Dykgraaf, S., Fith, E.C., Rogers, C.W., Kawcak, C.E., 2008. Effects of exercise on chondrocyte viability and subchondral bone sclerosis in the distal third metacarpal and metatarsal bones of young horses. Vet. J. 178, 53–61. Grogan, E.H., McDonnell, S.M., 2005. Injuries and blemishes in a semi-feral herd of ponies. J. Equine Vet. Sci. 25, 26–30. Henderson, J.V., Waran, N.K., 2001. Reducing equine stereotypies using an Equiball (TM). Anim. Welfare 10, 73–80. Hillyer, M.H., Taylor, F.G.R., Proudman, C.J., Edwards, G.B., Smith, J.E., French, N.P., 2002. Case control study to identify risk factors for simple colonic obstruction and distension colic in horses. Eq. Vet. J. 34, 455–463. Jørgensen, G.H.M., Bøe, K.E., 2007a. A note on the effects of daily exercise and paddock size on the behaviour of domestic horses (Equus caballus). Appl. Anim. Behav. Sci. 107, 166–173. Jørgensen, G.H.M, Bøe, K.E., 2007. Individual paddocks versus social enclosure for horses. Horse behaviour and welfare, EAAP publication No. 122, 79–83. Jørgensen, G.H.M., Borsheim, L., Mejdell, C.M., Søndergaard, E., Bøe, K.E., 2009. Grouping horses according to gender—effects on aggression, spacing and injuries. Appl. Anim. Behav. Sci. 120, 94–99. Koolhaas, J.M., Korte, S.M., De Boer, S.F., Van Der Vegt, B.J., Van Reenen, C.G., Hopster, H., De Jong, I.C., Ruis, M.A.W., Blokhuis, H.J., 1999. Copings styles in animals: current status in behaviour and stress-physiology. Neurosci. Biobehav. Rev. 23, 925–935. Koolhaas, J.M., 2008. Coping style and immunity in animals: making sense of individual variation. Brain Behav. Immun. 22, 662–667. Kruger, K., Flauger, B., 2008. Social feeding decisions in horses (Equus caballus). Behav. Proc. 78, 76–83. Landbruks og matdepartementet, 2005. Forskrift om velferd for hest. FOR-2005-06-02-505, Forskrift om velferd for hest [Homepage of Lovdata.no] Available online: http://lovdata.no/for/sf/ld/xd-200506020505.html [09/01, 2005]. Luescher, U.A., McKeown, D.B., Halip, J., 1991. Reviewing the causes of obsessive-compulsive disorders in horses. Vet. Med. 86, 527–530. McGreevy, P.D., Cripps, P.J., French, N.P., Green, L.E., Nicol, C.J., 1995. Management factors associated with stereotypic and redirected behavior in the Thoroughbred horse. Equine Vet. J. 27, 86–91. Nagy, K., Bodó, G., Bárdos, G., Bánszky, N., Harnos, A., Kabai, P., 2009. The effect of a feeding stress-test on the heart rate variability of control and crib-biting horses (with or witout inhibition). Appl. Anim. Behav. Sci. 121, 140–147. Nagy, K., Bodó, G., Bárdos, G., Bánszky, N., Kabai, P., 2010. Differences in temperament traits between crib-biting and control horses. Appl. Anim. Behav. Sci. 122, 41–47. Newberry, R.C., 1995. Environmental enrichments: increasing the biological relevance of captive environments. Appl. Anim. Behav. Sci. 44, 229–243. Rifa, H., 1990. Social facilitation in the horse (Equus caballus). Appl. Anim. Behav. Sci. 25, 167–176. Rogers, C.W., Firth, E.C., Mcilwraith, C.W., Barneveld, A., Goodship, A.E., Kawcak, C.E., Smith, R.K.W., van Weeren, P.R., 2008. Evaluation of a new strategy to modulate skeletal development in racehorses by imposing track-based exercise during growth: the effects on 2- and 3-year-old racing careers. Eq. Vet. J. 40, 119–127. Schabenberger, O., 2007. Growing Up Fast: SAS® 9.2 Enhancements to the GLIMMIX Procedure. SAS Global Forum 2007, Internet resource, accessed online: 7 January 2009. http://www2.sas.com/proceedings/forum2007/177-2007.pdf. Søndergaard E., Clausen E., Christensen J.W., Schougaard, H., 2002. Opstaldning og hold af heste—Danske anbefalinger (Housing and management of horses—Danish recommendations). DJF report Husdyrbrug 39, 105 pp. Danish Agricultural Research Tjele, Denmark. Thorne, J.B., Goodwin, D., Kennedy, M.J., Davidson, H.P.B., Harris, P., 2005. Foraging enrichment for individually housed horses: practicality and effects on behaviour. Appl. Anim. Behav. Sci. 94, 149–164.
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Contents lists available at ScienceDirect
Applied Animal Behaviour Science journal homepage: www.elsevier.com/locate/applanim
Effects of enrichment items on activity and social interactions in domestic horses (Equus caballus) Grete Helen Meisfjord Jørgensen ∗ , Silje Hanche-Olsen Liestøl, Knut Egil Bøe Norwegian University of Life Sciences, Department of Animal and Aquacultural Sciences, P.O. box 5003, 1432 Ås, Norway
a r t i c l e
i n f o
Article history: Accepted 2 November 2010 Available online 3 December 2010 Keywords: Horse Activity Behaviour Item Enrichment Social interactions
a b s t r a c t The aim of this study was to investigate the use of items intended to provide enrichment during turnout, both for individual and group kept horses in an attempt to reduce the amount of passive behaviours. The study was divided into two parts, where study 1 involved eight horses rotated through eight individual paddocks, each containing one of seven enrichment items and one paddock being kept without item, functioning as a control. The horses’ item-directed behaviours; passive behaviours or other non-item related activities were scored using instantaneous sampling, every minute for 1 h at the beginning and the end of the turnout period. Study 2 involved six horse groups (3–6 horses) and the same scoring methods and ethogram as in study 1. The four items that the horses interacted the most with during study 1 (straw STRA, ball filled with concentrates CBALL, branches BRAN and scratching pole POLE) are investigated in study 2. In addition, the amount of social interactions was recorded. Both horses kept individually (P < 0.05) and in groups (P < 0.0001) performed significantly more item-directed behaviours towards edible items like STRA and CBALL than other objects. There was, however, no overall relation between the numbers of item-directed behaviours and the number of passive behaviours observed, indicating that the enrichment items did not alone reduce the amount of passive behaviours during turnout periods. Such a reduction was, however, only apparent when horses spent more time eating green leaves growing on the paddock surface (R = −0.97 study 1, R = −0.67 study 2, P < 0.0001). Access to STRA in group kept horses also seemed to reduce the amount of agonistic behaviours (P < 0.0001). In conclusion, if grass is not available in paddocks, the provision of roughage reduces the amount of passive behaviours in singly kept horses and it also reduces the risk of agonistic interactions between horses kept in group. © 2010 Elsevier B.V. All rights reserved.
1. Introduction Turnout is generally regarded as positive for horses, as it gives opportunity for fresh air and voluntary exercise which is important for developing strong bones, joints and improving long term health in general (e.g. Dykgraaf et al., 2008; Rogers et al., 2008). However, experiments have shown that horses’ activities in such paddocks are rather
∗ Corresponding author. Tel.: +47 64 96 51 42; fax: +47 64 96 51 01. E-mail address: [email protected] (G.H.M. Jørgensen). 0168-1591/$ – see front matter © 2010 Elsevier B.V. All rights reserved. doi:10.1016/j.applanim.2010.11.004
limited and mostly linked to feed (Jørgensen and Bøe, 2007a). Longer periods of confinement increases the horses activity when turned out (Chaya et al., 2005), and when horses are actively exercised they become more passive during turnout (Jørgensen and Bøe, 2007a). Interestingly, horses display significantly more active behaviours when turned out in social groups compared to when kept individually (Jørgensen and Bøe, 2007b). Barren environments and social isolation have also been linked to many equine behavioural problems (Luescher et al., 1991; Waters et al., 2002) and stereotypies (e.g. weaving: Cooper et al., 2000). Despite this, the most common way of housing horses is
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still in individual tie-stalls or boxes inside barns (Bachmann and Stauffacher, 2002; Søndergaard et al., 2002). Welfare regulations in several countries demand that horses are given daily access to an outdoor paddock (e.g. Norway: Landbruks og matdepartementet, 2005), Denmark even recommends that young horses are kept in groups until they reach sexual maturity (Søndergaard et al., 2002). Even so, many horse owners prefer to keep their horses individually in paddocks during turnout, probably due to an unwarranted fear of injuries from social interactions (Grogan and McDonnell, 2005; Jørgensen et al., 2009). Several studies have linked low reactivity and passive behaviours to a passive coping strategy and apathy that is probably related to high rather than low stress sensitivity (Koolhaas et al., 1999; review: Koolhaas, 2008; Nagy et al., 2009). In horses this means that passive horses might be prone to developing stereotypic behaviours like crib-biting (Nagy et al., 2010). In an attempt to reduce boredom, apathy and the risk of developing stereotypic behaviours, different objects, toys or feedstuffs are now commercially available. Only a few of these have been scientifically tested and only individually stabled horses where then used (Winskill et al., 1996; Henderson and Waran, 2001). A study on horses’ use of the “Edinburgh Foodball” revealed a reduction in concentrate ingestion, movement, nosing of bedding material and standing compared to control observations (Winskill et al., 1996). A significant reduction in time spent performing stereotypic behaviours was also found when testing the same feeding device on stabled horses displaying some form of stereotypic behaviour (Henderson and Waran, 2001). Newberry (1995) defined environmental enrichment as: “an improvement in the biological functioning of captive animals resulting from modifications to their environment”. There is, however, no standard criteria for assessing whether access to an object or item functions as enrichment for the animal in question. Studies on environmental enrichments for other domestic animals emphasize that such enrichments should stimulate foraging and exploratory behaviour (e.g. pigs: Van de Weerd et al., 2003) and further studies on pigs report a higher degree of manipulation of edible items like straw compared to other commercial objects like a “Bite Rite” chewing toy (Van de Weerd et al., 2005, 2006). Environmental enrichments could be divided into four sub-categories: foraging opportunities, structural complexity, sensory stimulation/novelty, and social companionship (Newberry, 1995). In addition to provision of forage, the complexity of diets are important (Thorne et al., 2005) and objects could be provided that enable animals to groom or scratch in places they cannot reach themselves, as shown by the use of mechanical brushes for cattle (DeVries et al., 2007). The aim of this experiment was to investigate the use of enrichment items during turnout, both for singly and group kept horses. We hypothesized that horses would react differently to edible items compared to other nonedible items. From this we predicted that:
- Horses would show more item-directed behaviours towards edible items.
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- Horses would display less passive behaviours when given edible items. We also hypothesized that horses in groups would react differently to items of “enrichment” than individually kept horses, and predicted that: - Horses in groups would pay less attention to items than horses kept individually. 2. Materials and methods Two different studies were performed. The first and preliminary study aimed to discover which items individually kept horses would interact with, while in study 2 the four most popular items from the preliminary study were tested in six different groups of horses. 2.1. Study 1—horses kept individually Experiments were done during October and November 2008 in the south-eastern parts of Norway. A large stable located in Akershus County with singly kept horses was recruited by direct contact initiated by the researchers. 2.1.1. Experimental design A total of eight horses were individually turned out into eight paddocks and given access to one of the enrichment items for 1 day (7 h), before being randomly rotated to another paddock with another item the next day, functioning as their own control. This was repeated for 8 days until all horses have had access to all paddocks, functioning as their own control. The enrichment items used were divided into two categories; edible items: peat soil (PEAT), straw (STRA), a pile of branches (BRAN), a ball filled with concentrates (CBALL) or objects: a cone (CONE), a ball (BALL), a scratching pole (POLE), while the last paddock was barren, without enrichment items for control (CONT). 2.1.2. Animals and feeding Eight riding horses (7 warmblood horses and 1 sport pony, 4 mares and 4 geldings), aged 6–18 years old (mean age 11 years) were randomly selected from the population of 25 privately owned horses at the stable. Both before and during the experiment, all horses were regularly ridden in disciplines like dressage, jumping or trekking 1–2 h per day and were kept individually in standard sized boxes (3 m × 3 m) inside an insulated building during night (15:00–08:00). Every day after morning feeding, horses were turned out into the paddocks for 7 h (8:00–15:00). The horses were fed an individually adjusted diet of hay (4 times/day) and concentrate feed (2 times/day). Two of these hay meals were administered while the horses were outside in the paddocks, between observation periods. All horses were wearing blankets and halters during turnout and no horses displayed any form of stereotypic behaviours. 2.1.3. Paddocks The paddocks measured in average >10 m × >20 m (range 231–465 m2 ), and no physical contact was possi-
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Fig. 1. Experimental periods (horizontal arrows) and observation times (vertical arrows). Control observations are shown in yellow arrows. The order of items was random, this is only an example. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of the article.)
ble between horses. The ground consisted of mainly clay and topsoil, but despite the fact that all paddocks were in daily use, some very small plants (mainly common horsetail, Equisetum arvense) could be found. 2.1.4. Treatment items A detailed description of the seven enrichment items can be found in Table 1, and we chose to divide the items into two categories according to if they were edible or not. The items were placed in the middle of each paddock, allowing horses to approach them from all directions. The PEAT and POLE were permanent items in their designated paddocks, while all other items were given just before observations started each day and removed at the end of the last observational period. One day of observations for the POLE item was lost due to it being broken. 2.1.5. Behavioural observations The horses’ behaviour and contact with the items were scored instantaneously every minute for 1 h (morning: 10:00 to 11:00) at the beginning of the turnout period and 1 h at the end of the turnout period (afternoon: 14:00 to 15:00) each day. A total of 19 mutually exclusive behaviours were recorded, and these were later organized into the 3 categories according to item or non-item directed behaviours (Table 2). Weather, temperature and surface conditions were recorded at the start of every observation period. 2.2. Study 2—horses kept in groups
turned out into the experimental enclosures for 3 days in order to get acclimatized to the new social situations. Then the horse groups were exposed to one of four enrichment items at a time in their enclosure; STRA, CBALL, BRAN and POLE, in a randomized order and each experimental period lasted 4 days (Fig. 1). A fifth experimental period at the end of the experiment served as control (CONT) with no additional item. 2.2.2. Animals and feeding In groups 1, 2, 5 and 6 the horses were singly stabled indoors during night and turned out in groups, 6–7 h per day, while groups 3 and 4 were kept outdoors in their paddock 24 h a day. All horses within each group were familiar with each other and had been together for at least 3 weeks prior to the study. Groups 1 and 2 consisted of only geldings whereas groups 3–6 contained both mares and geldings. No stallions were used in the study, and groups consisted of mostly adult horses (mean age 11.3 years) ranging from 2 to 29 years old. Horse breeds varied from Norwegian Døla horses (∼500 kg) to Icelandic horses (∼300 kg), and they were used and exercised as normal during the experimental period, but only after the observations and turnout time were completed. Most of the horses wore halters and blankets during turnout, depending on the weather. Groups 3 and 4 had permanent access to shelter and were fed (3 times/day) from hayracks mounted on the shelter wall; while the rest of the groups were fed meals of hay on the ground (one meal was given during turnout while morning and evening meals were given inside the stable). Feed rations consisted mostly of several kilograms of hay per horse and concentrates were given only to supplement the energy from the roughage. All horses were able to feed at the same time, and had ad libitum access to water.
A total of 13 stable owners contacted the researchers and wished to participate in our study, after we had advertised through a popular Norwegian horse webpage (www.hest.no). Three of these stables were selected on the following criteria: (1) have privately owned horses that were kept in groups of three individuals or more, for at least 6 h daily and (2) stable located less than 1 h drive from the Norwegian University of Life Science. On each of the three farms, two groups of horses were selected at random.
2.2.3. Experimental enclosures The mean enclosure space was 1577 m2 /horse ranging from 262 to 5833 m2 /horse and the surface mainly consisted of topsoil and clay that became somewhat muddy after heavy rains.
2.2.1. Experimental design During the experiment, in November; the number of horses in the original groups was reduced so that each of the six groups now consisted of three or four horses, except for group number four that had six horses. Horse groups were
2.2.4. Behavioural observations The behaviour of the horses was recorded live by an observer the first (day 1) and last day (day 4) of each experimental period for 1 h (between 08:00 and 12:00) using instantaneous sampling every minute. One 1-h baseline
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Table 1 Description of the enrichment items used. Additional item
Description
Brand
Size
CONE
Red, soft plastic, marked with Gaffa tape in two horizontal stripes around the body of the cone to make a different appearance.
Hööks Hestesport
31 cm tall, standing on a 19 cm × 19 cm plate
BALL
Hard plastic ball with two small holes of 1.5 cm in diameter.
Canac activity ball
25 cm in diameter
POLE
A wooden fencing pole 8.0 cm in diameter, 1.40 m tall was driven well into the ground. A rubber scratching mat was fixed around the upper parts of the pole and a short haired, stiff brush was fixed on top of the pole with the bristle facing up.
Scratching mat from Hööks Hestesport (30 cm x 50 cm)
1.10 m tall
PEAT
40 l were placed in a pile directly on the ground.
Herbia
5.0 l added each day
STRA
Straw of barley placed directly on the ground.
BRAN
The branches were between 1.0 and 3.5 cm in diameter at the point where they were cut, measuring 1.0–2.0 m long.
Norway spruce (Picea abies) Birch (Betula) Sallow (Salix caprea)
2 branches of Spruce and 3 branches of Birch and Sallow. Fresh each day
CBALL
Same as BALL, but filled with 0.5 kg standard concentrate feed for horses.
Canac activity ball
25 cm in diameter
Objects
Edible items
2.0 kg fresh each day
Picture
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Table 2 Ethogram of behaviours scored both during study 1 and 2. Categories and underlying behaviours
Description
Item directed behaviours Watching the item The horse is standing with eyes fixed on the item. Walking towards the The horse is moving towards the item, with item eyes fixed on the item. Sniffing the item The horse is standing with head very close to the item and is sniffing or blowing air (identified by the characteristic sound). Examining the item The horse is standing with muzzle in physical with muzzle contact with the item, but not chewing on it or making sniffing/blowing sounds. Chewing on the item The horse is standing close to the item and is chewing on it, parts of the item inside the mouth. Chewing The horse is not chewing on the item itself concentrates from (CBALL) but is eating concentrates that has CBALL fallen out of the CBALL. Pushing the item The horse is using its head or muzzle to push with muzzle/head the item so that it visibly moves. Touching the item The horse is in physical contact with the item with front legs with its front leg (often a scraping, pushing or digging motion). Rubbing body against The horse is rubbing parts of the body (head, POLE neck, chest, sides or rump) against the scratching pole. Keeping a distance to The horse is standing as far away from the the item item as possible, keeps eyes and ears fixed towards the item while head and tail are raised. Horse seems frightened. Passive behaviours Standing, not watching the item Lying
The horse is standing relaxed without directing any attention towards the item. The horse is lying on the ground.
Other non-item related activities Sniffing the ground The horse is standing or moving around with its muzzle in contact or very close to the ground. Eating The horse is eating/grazing or chewing on other things than the item. Drinking The horse stands with its muzzle in the water bucket. Rolling The horse lies on the ground and is rolling from side to side, rubbing its back and sides against the ground. Moving The horse is walking or running around in the paddock, not paying attention to the item. Eliminative The horse is urinating or defecating. behaviour Self grooming The horse is using its teeth, hoofs, legs or muzzle to scratch itself in other parts of the body. Other The horse is showing other behaviours not described in the ethogram (for example stereotypes).
observation was performed before, and one after groups were introduced to all enrichment items was pooled in order to provide control measures of horses’ activity and social behaviours (Fig. 1). We used the same ethogram as in study 1 (Table 2), but also added a category for any social interaction if this was seen during the scan. In addition, every event of social interactions was recorded continuously in a separate dataset using a modified ethogram from Christensen et al. (2002) (Table 3).
Table 3 Ethogram of social interactions (adjusted from Christensen et al., 2002). Behaviours
Description
Agonistic behaviours Displacement Approach of one horse causes another to move away (at least 3 m) so that distance is maintained or increased, without overt aggression (also termed retreat/avoidance, depending on whether receiver or sender is noted). Chase One horse chases another (trotting or galloping) with ears laid back. Mouth clapping Submissive behaviour. Opening and closing mouth with lips retracted. Typically, the head and neck are extended, and the ears oriented back or laterally (also termed snapping). Threat to bite Bite intention movement with ears back and neck extended, with no actual contact. Threat to kick Kick intention movement, performed by swinging rump or backing up, AND waving or stamping hind leg towards another horse, without making contact. Backing The horse backs towards another horse with ears laid back. Physical contact may or may not be obtained. Bite Opening and rapid closing of the jaws with actual contact to another horse’s body. The ears are back and lips retracted. Kick One or both hind legs lift off the ground and rapidly extend backwards towards another horse, with apparent intent to make contact. Push Pressing of the head, neck, shoulder, chest, or body against another horse, causing it to move one or more legs to regain balance. Friendly behaviours Head rest A horse rests its head on the rump or back of another horse. May involve a gentle rubbing of the head against the body of the other horse. Play Play directed at another individual, which may or may not reciprocate; includes low intensity play movements such as nipping, grasping, and pulling mane or tail. Play fight High intensity play, which is reciprocated by one or more partners; includes vigorous play movements such as rearing, boxing, circling, kneeling, and chasing. Social grooming Reciprocal coat care in which the partners stand beside one another, usually head-to-shoulder or head-to-tail, grooming each other’s neck, mane, rump, or tail by gently nipping, nuzzling, or rubbing.
The actor and receiver of these social interactions were noted, in order to detect individuals being mobbed or mobbing other group members. Because of few recordings, the actor social interactions were later pooled into agonistic behaviours and friendly behaviours. 2.3. Statistical analysis The distribution of each response variable was tested using goodness of fit analysis in JMP® 7.0 statistical software. The effect of different enrichment items on the behaviour of individual horses during study 1 was analysed using the Glimmix procedure with the following class variables: additional item (CONT, PEAT, STRA, CONE, BALL, CBALL, POLE or BRAN) and observation time (morning or afternoon in 1 day turnout period). The interaction between
Exact tests of differences between means could not be performed using LS-means due to the limited number of observations within some item-treatments. The degrees of freedom are different for tests on “item-directed behaviours” because this data are Lognormal distributed compared to Poisson distribution of data on “passive” and “other non-item related behaviours”.
a
0.4 b 4.1 a 3.9 b 1.5 a ± ± ± ± 1.7 38.9 52.8 6.5 29.4 ± 3.9 b 64.8 ± 3.8 a 5.7 ± 1.3 b Study 2. Horses in groups Item-directed behaviours Passive behaviours (Standing or lying) Other non-item related activities Social interactions
b
<0.0001 <0.0001 <0.0001 <0.0001 F3,92 = 11.3b F4,212 = 59.4 F4,212 = 63.8 F4,212 = 19.4 4.7 a 3.0 c 4.8 b 1.6 b ± ± ± ± 26.0 19.3 50.2 4.5 0.7 b 4.0 c 3.9 a 1.4 a ± ± ± ± 2.8 22.4 68.4 6.2 3.5 a 4.2 a 4.4 c 0.8 c ± ± ± ± 23.7 33.2 41.0 1.9
<0.05 <0.0001 <0.0001 F6,27 = 2.9b F7,104 = 38.9 F7,104 = 26.9 13.7 ± 4.8 35.0 ± 4.8 b 51.2 ± 4.5 c 6.3 ± 1.9 54.7 ± 6.0 a 38.9 ± 5.9 c 20.0 ± 5.7 22.4 ± 4.5 d 57.4 ± 4.9 b 0.1 ± 0.1 34.6 ± 6.3 b 65.2 ± 6.3 ab 2.1 ± 1.9 40.7 ± 5.9 b 57.0 ± 6.0 b 0.3 ± 0.2 30.9 ± 6.8 bc 68.7 ± 6.7 ab
P-Value F-Value Straw (STRA) Branches (BRAN) Ball with concentrates (CBALL) Peat (PEAT)
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0.4 ± 0.2 24.0 ± 6.7 cd 75.5 ± 6.8 a Study 1. Horses in individual paddocks Item-directed behavioursa Passive behaviours (Standing or lying) 52.5 ± 7.2 a Other non-item related activities 47.4 ± 7.2 c
3.1.2. Passive behaviours Time spent standing or lying ranged from 22 to 55% of total observations and this passive behaviour was more prevalent in CONT and BRAN treatment, than during STRA and CONE treatments (Table 4). Generally, the horses showed more passive behaviours after 4–5 h with the item than straight after the item were introduced, in all treatments except when given the BRAN item (Fig. 2b). A significant interaction effect between addi-
Scratching pole (POLE)
3.1.1. Item-directed behaviours The horses spent significantly more time (in average 13.2% vs. non-edible items: 0.9% of tot. obs.) performing item-directed behaviours when exposed to edible items like straw (STRA), the ball with concentrates (CBALL) and branches (BRAN) (Table 4). The other items, however, were rarely touched by the horses, but this was probably not related to horses being afraid of the items since no events of “Keeping distance to items” were seen. In the CBALL-treatment the horses spent most of the time either chewing concentrates that had fallen out of the ball (9.8 ± 4.0%) or sniffing the ground behind the ball (7.5 ± 2.7%). Horses seemed, however, to lose interest in the items over time since significantly more item-directed behaviours were observed straight after the new item was introduced, especially for the STRA and CBALL treatment (Fig. 2a). Individual horse had no significant effect on the item-directed behaviours and no interaction effect between item and time of observation was found (F3,27 = 1.2, P = 0.3).
Ball (BALL)
3.1. Study 1—horses kept individually
Control (CONT) Cone (CONE)
3. Results
Behaviours (mean ± SE % of tot. obs.)
additional item and observation time was included in the model statement, while horse (1–8) was specified as a random effect (Schabenberger, 2007). A Glimmix model of analysis of variance was used when testing the effect of enrichment items on group kept horses during study 2. Here we used additional item (CONT, STRA, CBALL, BRAN and POLE), group (1–6), observation time (day 1 or day 4) and the interaction between additional item and observation time as class variables. Group was specified as a random effect. Also the effects of enrichment items on social interactions during study 2 was analysed using a Glimmix model with additional item, group, observation time and the interaction between additional item and observation time as class variables. Group was specified as a random effect. The effects of enrichment items on number of aggressive and friendly social interactions were tested using separate datasets with a similar model. Correlations between item-directed and passive behaviours or passive behaviours and eating non-item related substrates were investigated using Spearman correlations. Differences between means were tested using LS-means with Tukey–Kramer adjustments for multiple comparisons. All model analysis was performed using the SAS® software.
Table 4 Behaviours related to enrichment items during study 1: horses in individual paddocks, and study 2: horses kept in group. Means within behaviour category that are indicated with unequal letters are significantly different (P < 0.05).
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Fig. 2. (a and b) The effect of observation time on (a) item-directed behaviours and (b) passive behaviours during study 1. Differences within treatment, between observation time are given as follows: *P < 0.05; ***P < 0.0001. Differences within observation time, between treatments are indicated by different letters (P < 0.05). ns = non-significant.
tional item and observation time was found (F7,104 = 4.9, P < 0.0001, Fig. 2b). The number of passive behaviours were, however, not reduced by an increase in number of item-directed behaviours (Fig. 3a), and only when given STRA (R = −0.62, P = 0.01) and CBALL (R = −0.52, P = 0.037) did the number of item-directed behaviours and passive behaviours correlate over observations. 3.1.3. Other non-item directed activities Other non-item related activities ranged from 47.4 to 75.5% of total observations and were mostly observed when horses were given CONE, BALL, PEAT, POLE and STRA items (Table 4). Horses were often observed eating small green leaves growing from the surface of the paddocks and when given the CONE item, more of this behaviour was observed than when given the BRAN item (Fig. 3b). This eating of non-item related substrates affected the number of passive behaviours in general (Fig. 3b) and horses given each of the items CONE (R = −0.91, P < 0.0001), Ball (R = −0.96, P < 0.0001), POLE (R = −0.80, P < 0.001) and BRAN (R = −0.83, P < 0.0001) showed significantly less passive behaviours when more non-item related eating was performed. 3.2. Study 2—horses kept in groups 3.2.1. Item-directed behaviours Horses kept in groups showed more item-directed behaviours when given edible items like STRA and CBALL
compared to POLE (Table 4), and this is similar to what we found in horses kept individually. Chewing the item was most common of the item-directed behaviours and horses chewed significantly more on STRA (23.2 ± 3.4%) than when given other edible items (CBALL: 10.3 ± 2.4%, BRAN: 2.7 ± 0.7% and POLE: 0.2 ± 0.1, F3,53 = 22.3, P < 0.001). In the CBALL-treatment, most item-directed behaviours were either chewing concentrates that had fallen out of the ball (9.8 ± 2.3%) or sniffing the ground behind the ball (6.9 ± 1.6%). We found no effect of group and no interaction effect between enrichment item and observation time, showing that contrary to our findings in individually kept horses, the group kept horses did not lose interest in the given items from day 1 to day 4. 3.2.2. Passive behaviours Most passive behaviours where recorded when horses were exposed to the POLE treatment and the least passive behaviours were recorded during the CBALL treatment (Table 4). The behaviour “standing, not watching the item” explained more than 75% of the passive behaviours in the POLE treatment, >95% in the STRA treatment and 100% in the CBALL treatment. In CONT and BRAN treatments, horses were standing 100% and >85% of the passive behaviours, respectively. The number of passive behaviours did not change from day 1 to day 4 in each experimental period
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Fig. 3. (a and b) Correlations (a) between item-directed behaviours and passive behaviours or (b) between passive behaviours and eating nonitem related substrates in horses kept singly during study 1.
in general, but for two enrichment items the horses displayed more passive behaviours after 4 days (day 1 vs. day 4: STRA: 28.8 ± 4.6% vs. 37.5 ± 7.0%; POLE: 35.9 ± 5.8% vs. 41.7 ± 5.8%). Interestingly, the opposite occurred in CONT (day 1: 31.2 ± 5.8% vs. day 4: 27.5 ± 5.4%) and BRAN (day 1: 26.4 ± 6.7% vs. day 4: 18.5 ± 4.3%) treatments (interaction effect additional item vs. observation time: F4,212 = 10.9, P < 0.0001). Similarly to what we found in study 1, the number of passive behaviours was not reduced by an increase in number of item-directed behaviours (Fig. 4a). Here, the number of item-directed behaviours and passive behaviours correlated only for the STRA item (R = −0.36, P < 0.05). 3.2.3. Other non-item related activities For group-kept horses, the non-item related activities ranged from 41.0 to 68.4% of total observations and most of these behaviours were scored when given BRAN and during CONT (Table 4). The number of non-item related activities observed did not differ from day 1 to day 4 during the experimental period and no interaction between additional item and observation time was found. Approximately 80% of these non-item related activities were scored as ‘eating green leaves from the surface’, and the least eating of non-item related substrates was found in the STRA treatment (Fig. 4b). This eating of green leaves affected the number of passive behaviours in general (Fig. 4b), and horses given each of the items STRA (R = −0.56, P < 0.0001), BRAN (R = −0.71, P < 0.0001), CBALL (R = −0.37, P < 0.01) and POLE (R = −0.92, P < 0.0001) showed signifi-
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Fig. 4. (a and b) Correlations (a) between item-directed behaviours and passive behaviours or (b) between passive behaviours and eating nonitem related substrates in horses kept in groups during study 2.
cantly less passive behaviours when more non-item related eating was performed. 3.2.4. Social interactions Number of social interactions was highest in the POLE and BRAN treatments, somewhat lower in the CBALL and CONT treatments and the lowest in the STRA treatment (Table 4). Horses in the STRA treatment showed significantly less agonistic behaviour (F4,215 = 7.2, P < 0.0001; Fig. 5) and the highest number of friendly behaviours towards each other, but this measure did not differ sig-
Fig. 5. Agonistic and friendly behaviours in relation to enrichment items given. Bars with unequal letters differ significantly within colour (P < 0.05). (For interpretation of the references to color in this figure legend, the reader is referred to the web version of the article.)
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nificantly over treatments. The major contributor to the agonistic social behaviours was ‘displacements’ (CONT: 9.5 ± 4.6%; STRA: 42.8 ± 8.8%; CBALL: 18.7 ± 6.9%; POLE: 10.3 ± 5.4%; BRAN: 15.3 ± 6.6% of all social behaviours) while the other behaviours were rarely seen. 4. Discussion Both horses kept individually and in groups performed more item-directed behaviours when given access to edible items like straw (STRA) and a ball filled with concentrates (CBALL). There was, however, no overall relation between the numbers of item-directed behaviours and the number of passive behaviours observed, indicating that the enrichment items did not alone reduce the amount of passive behaviours during turnout periods. Horses kept individually paid more attention to non-edible items like the POLE compared to horses in groups. There might be a significant effect of social facilitation explaining the finding that group housed horses directed more of their attention towards the popular STRA and CBALL items, but less attention towards the other items compared to the horses kept individually. For the POLE item on the other hand, individually kept horses may have used the POLE for scratching parts of their body that they could not reach themselves, while horses kept in groups had the option of social grooming. Horses kept in individual paddocks displayed relative high frequencies of other non-item related behaviours, most of which was identified as eating green leaves. One of the primary motivations in horses is searching for and eating grass and earlier studies have documented horses spending 40–70% of their time in such activities (Arnold, 1984; Boyd et al., 1988). This is not different in domestic horses since horses in individual paddocks without any significant grass available, still spent up to 40% of their time searching for and nibbling grass from under the fence (Jørgensen and Bøe, 2007a). Our results from study 1 demonstrated that horses displayed more non-item directed eating behaviour when given access to the CONE item compared to when given the BRAN item. The explanation for this could be related to the horses ingesting or exploring the branches but it is also probably related to very subtle differences in the amount of green leaves in each paddock. The enrichment items were kept in the same paddocks, while the horses were rotated between paddocks during study 1. These differences were, however, not detectable by the human eye, and paddocks were evaluated to be very similar before the experiment took place. Looking at the same behaviour recorded in study 2 on horses kept in groups, there was still significantly more eating of non-item related substrates when horses were given BRAN compared to when given STRA items. This difference could, however, not be explained by differences in physical properties in the enclosures since the enrichment items were randomly rotated between horse groups and the effect of group was controlled for in the statistical model. Therefore it is probable that the horses spent time chewing and eating straw (STRA) when given access to this, decreasing the motivation for searching for and eating other substrates. Provision of roughage has also been shown to reduce feeding motivation and both risk and prevalence of stereotypic
behaviours in pigs (review: Tuyttens, 2005) and horses (e.g. McGreevy et al., 1995; Thorne et al., 2005). No horses with known stereotypic behaviour patterns were included in the present study and it would therefore be interesting if further experiments would investigate the effect of similar edible items on stereotypic behaviours during turnout periods. Horses were observed to use the POLE for scratching their body relatively seldom, but we found hairs both in the brush on top and on the rubber scratching mat fixed around the pole, indicating that it had been used outside observation periods. Cattle actually increased their total scratching behaviour by over 500% after they were given access to a mechanical brush and used it extensively to scratch in places where they could not reach themselves (DeVries et al., 2007). We hypothesized that horses in groups might spend less time in contact with additional items compared to horses kept individually, since the social environment in itself might be regarded as an enrichment that provides several stimuli and the possibility for play and social grooming. The results from our study do not provide very clear evidence to support this idea. Horses in groups did certainly show more item directed behaviour to the edible items STRA and CBALL but this can be explained by the mechanism of social facilitation (Rifa, 1990). Furthermore, horses kept individually displayed more item directed behaviours towards the POLE and BRAN items (Table 4) perhaps indicating that since they had nothing else to do, they spent some time investigating the items rather than standing passively. Individually kept horses seemed to lose interest in the enrichment items over the course of the day (4–5 h), but horses kept in groups showed a similar number of item-directed behaviours the first and the fourth day of each experimental period. Observations on individually kept horses might have been influenced by the horses’ daily activity budget, resulting in the afternoon observations coinciding with a quiet time of the day. Such effects were, however, not present in study 2 as both day 1 and day 4 observations were performed before noon. It is favourable that the horses did not seem to lose interest in the items over the course of 4 days, indicating some value as an ‘enrichment’ but it is important to have several items (or piles of feed), provided in large enough quantities in order to prevent competition when given in groups (Kruger and Flauger, 2008). Our results indicate that provision of straw (STRA) reduced the number of agonistic interactions in group kept horses. One of the most common arguments against keeping horses in groups is the fear of injuries from agonistic interactions. Straw has previously been shown to reduce the risk of pigs developing harmful behaviours (e.g. Van de Weerd et al., 2005), a result supporting our finding. Ad libitum access to other forms of roughage probably have similar positive effects, but one should consider the relative risk of impaction colic if horses are given low quality roughage (Cohen et al., 1999) combined with little ability to move (stabling) (Hillyer et al., 2002). Newberry (1995) stated that for an item to be considered an environmental enrichment it should improve the biological functioning of the animal. In the present
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experiment we have not measured the horses biological functioning directly, but we found differences in behaviour indicating that ad libitum access to forage have positive effects. Looking at it from another angle put forward by Appleby (1997), we could, however, say that providing ample amounts of forage does indeed facilitate the performance of adaptive behaviours, and is therefore an important environmental enrichment for horses. These studies were performed using privately owned horses living in different stables. Despite our best efforts to standardize groups and enclosures, some differences had to be accepted. We did, however, include this effect in the statistical analysis, but could not find indications for some groups reacting differently than others to our treatments. In conclusion, even when horses were given the most popular edible items (STRA and CBALL) the amount of passive behaviours was not reduced. More time spent eating green leaves growing from the paddock surface did, however, correlate with a reduction in passive behaviours both for individually and group kept horses. Our results therefore emphasize the importance of providing horses with grass pasture or good quality roughage during turnout. When horses are kept in groups, they are influenced by social facilitation that underlines the importance of providing edible items of enrichment in several locations. When this is done correctly, the provision of straw might even reduce the risk of aggressive interactions between horses kept in groups. Based on behavioural measures alone, the provision of toys or other non-edible items does not seem to be an obvious enrichment for horses, but no negative effects were discovered either. Acknowledgements This experiment was funded by the Research committee at the Norwegian Equine Centre. We would like to thank Guro Vasdal for valuable comments on earlier versions of this manuscript. We would also like to extend our gratitude to Hallkjell Jensen and all participating horses and stable owners. Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at doi:10. 1016/j.applanim.2010.11.004. References Appleby, M.C., 1997. Life in a variable world: behaviour, welfare and environmental design. Appl. Anim. Behav. Sci. 54, 1–19. Arnold, G.W., 1984. Comparison of the time budgets and circadian patterns of maintenance activities in sheep, cattle and horses grouped together. Appl. Anim. Behav. Sci. 13, 19–30. Bachmann, I., Stauffacher, M., 2002. Housing and exploitation of horses in Switzerland: a representative analysis of the status quo. Schweiz. Arch. Tierheilkd. 144, 331–347. Boyd, L.E., Carbonaro, D.A., Houpt, K.A., 1988. The 24-hour budget of Przewalski horses. Appl. Anim. Behav. Sci. 21, 5–17. Chaya, L., Cowan, E., McGuire, B., 2005. A note on the relationship between time spent in turnout and behaviour during turnout in horses (Equus caballus). Appl. Anim. Behav. Sci. 98, 155–160.
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