Effect of space and floor material on the behaviour of farmed blue foxes

Effect of space and floor material on the behaviour of farmed blue foxes H. T. Korhonen 1, P. Niemelä 1, and L. Jauhiainen 2 1 Agricultural Research Centre of Finland, Animal Production Research, Fur Animals, FIN-69100 Kannus, Finland (e-mail: hannu.t.korhonen@mtt.fi); 2 Agricultural Research Centre of Finland, Data and Information Services, FIN- 31600 Jokioinen, Finland. Received 15 September 2000, accepted 16 February 2001. Korhonen, H. T., Niemelä, P. and Jauhiainen, L. 2001. Effect of space and floor material on the behaviour of farmed blue foxes. Can. J. Anim. Sci. 81: 189 197. Effects of space and floor material on the behaviour of blue foxes were evaluated in the following groups: (1) small wire-mesh cages (50 cm long 105 wide cm 70 cm high; W50); (2) medium wire-mesh cages (120 cm long 105 cm wide 70 cm high; W120); (3) wire-mesh floored pens (5 m long 3m wide 1.8 m high:w500); and (4) earthen floored pens (5 m long 3 m wide 1.8 m high; E500). Activity and locomotion were lowest in W50 foxes and tended to increase with increasing cage size. Floor material had only a slight effect on activity and stereotypies. Locomotion was higher in E500 than in W500 foxes. Locomotor stereotypy increased with increasing cage size, and was higher in W500 than in E500 foxes. Significant periodic changes were found in several behavioural variables. Activity was concentrated most and least frequently between 8 and 16 h and 0 and 8 h, respectively. The same tendency was found for sitting, standing, locomotion and activity. Digging was noted only in E500 foxes, averaging 15 min/24 h, and being most common between 16 and 24 h. Key words: Alopex lagopus, cage size, floor type, housing conditions, ethogram Korhonen, H. T., Niemelä, P. et Jauhiainen, L. 2001. Incidence de l espace et du type de sol sur le comportement du renard arctique d élevage. Can. J. Anim. Sci. 81: 189 197. Les auteurs ont évalué les effets de l espace et du type de sol sur le comportement du renard arctique. Les animaux étaient répartis de la façon suivante : (1) petites cages en treillis métallique (50cm de longueur 105 cm de largeur 70 cm de hauteur; W50); (2) cages de taille moyenne en treillis (120 cm de longueur 105 cm de largeur 70 cm de hauteur; W120); (3) enclos au sol recouvert de grillage (5 m de longueur 3 m de largeur 1,8 m de hauteur; W500); (4) enclos au sol de terre battue (5 m de longueur 3 m de largeur 1,8 m de hauteur; E500). Les animaux élevés dans les cages W50 étaient ceux les moins actifs et qui se déplaçaient le moins. Le degré d activité et la fréquence des déplacements ont tendance à augmenter avec les dimensions de l enclos. Le type de sol n a qu une légère incidence sur le degré d activité et les stéréotypes. Les renards se déplacent davantage dans les cages E500 que W500. Le stéréotype locomoteur s intensifie avec les dimensions de l enclos et est plus manifeste dans les enclos W500 que E500. L expérience révèle d importants changements périodiques au niveau de plusieurs variables du comportement. Les animaux sont les plus et les moins actifs, respectivement, entre 8 et 16 heures et entre 0 et 8 heures. On a relevé la même tendance pour les stations assise et debout, pour les déplacements et pour le degré d activité. Seuls les renards du quatrième groupe ont creusé le sol 15 minutes par jour, en moyenne, généralement entre 16 h et 24 h. Mots clés: Alopex lagopus, dimensions des cages, type de sol, conditions d élevage, éthogramme A concrete example of the recent interest in improving housing conditions of farm-raised foxes is contained in the recommendations of the European Council (European Convention 1999), which provide general instructions for acceptable housing management. The recommendations point out that the scientific evidence currently available is not sufficient for the elaboration of detailed instructions and, therefore, further research on alternative housing design should be encouraged. More information is still needed, for example, on appropriate floor materials. Traditionally, foxes have been raised on wire-mesh floors, which, are not the natural walking surface of this species in the wild. One can, therefore, expect that replacement of wire-mesh floors by earthen floors would be a better alternative. This assumption has not yet been substantiated, either by preference tests (Pedersen 1993; Skovgaard et al. 1995, 1998; Harri et al. 1999) or by long-term housing experiments (Pyykönen 189 et al.1997; Korhonen et al. 2000b). Earth has also been considered a suitable floor material for foxes because it permits species-specific behaviour like digging (European Convention 1999). The amount of appropriate housing space has also been a concern of recent legislation (European Convention 1999). Three main approaches have been used to evaluate the space requirements for foxes, namely, the physiological pathological production-related approach (Korhonen et al. 2000a,b; Ahola et al. 2000a), the behavioural approach (Korhonen et al. 1999a) and a combination of these two (Pedersen et al. 1995; Pedersen and Jeppesen 1998; Ahola et al. 2000b). Results have been inconclusive and more clarification is necessary, in particular concerning behaviour and welfare in extremely small cages and in spacious semi-natural pens. The purpose of the present study was to compare the behaviour of growing male blue foxes (Alopex lagopus) in

190 CANADIAN JOURNAL OF ANIMAL SCIENCE extremely small shed cages, standard shed cages and larger outdoor pens. The starting point was that an extremely small cage apparently restricts the activity and behaviour of animals. The implications of space restriction are increased abnormal behaviours such as stereotypies or passiveness. Limited living space could also be assumed to increase agonistic interactions and social tension between cage mates. A larger pen served as an extensive housing condition, expected to give more opportunities for exercise and the expression of a wide repertoire of behaviours. The qualitative comparison included clarification of how floor material (wire-mesh vs. earth) affected behaviour in outdoor pens with the two floor types. The assumption was that earth, being the natural walking surface of foxes in the wild, should provide the best possibilities for locomotion and the expression of species-specific behaviour such as digging. The amount of abnormal behaviour would be expected to be lower on an earthen floor than on a wire-mesh floor. MATERIALS AND METHODS Animals and General Management The study was carried out at the Fur Farming Research Station at Kannus (63.54 N, 23.54 E) during July December 1998. The experimental animals were born in May. Until weaning, they were housed with their mothers and littermates in conventional wire-mesh floor cages measuring 120 cm long 105 cm wide 70 cm high. At weaning (8 wk), the foxes were divided into the following experimental groups: (1) small wire-mesh floored shed cages (50 cm long 105 cm wide 70 cm high; coded W50); (2) medium wire-mesh floored shed cages (120 cm long 105 cm wide 70 cm high; W120); (3) wire-mesh floored outdoor pens (5 m long 3 m wide 1.8 m high; W500); and, (4) earthen-floored outdoor pens (5 m long 3 m wide 1.8 m high; E500) (Fig. 1). The rationale for the various confinement conditions was as follows: W120 simulated the standard housing practices of farmed blue foxes; W50 provided restricted caging in a much smaller area than that recommended by law (European Convention 1999); and W500 and E500 provided extensive space outside the shed. Each test group comprised 20 blue fox male kits maintained in pairs. Thus, there were 10 of each cage type. One animal in each cage was white and the other one was blue, which made the identification of individuals possible. Four siblings (A) with their cage partners (B) formed a block (see statistical methods). Siblings were equally divided into each group so that one animal in each group was from a same litter. Experimental animals were fed by hand. Freshly-mixed fox feed was supplied twice a day during July September and once a day thereafter. The feed was mainly composed of slaughter-house offal, fish, fish offal and cereals, according to standard Finnish recommendations (Berg 1986). The daily feed ration was the same for each group, varying from 600 to 900 g animal 1 d 1. Any leftovers were divided among other members of the same test group. Water was continuously available from automatic watering devices. Animals were cared for under guidelines comparable to those laid out by the Canadian Council on Animal Care Fig. 1. Schematic diagram of the experimental set-up. W50: small wire-mesh floored shed cage (50 cm long 105 cm wide 70 cm high, W120: medium wire-mesh floored shed cage (120 cm long 105 cm wide 70 cm high), W500: wire-mesh floored outdoor pen (5 m long 3m wide 1.8 m high, and E500: earthen floored outdoor pen (5 m long 3 m wide 1.8 m high). Each test group comprised 20 blue fox male kits maintained in pairs. (1993). Furthermore, authors had legal permission from Finnish welfare/veterinary authorities to perform this experiment. Video Recordings The behaviour of experimental animals was recorded during five 24-h periods in each of August, September, October and November (480 h/animal totally). The video recording system comprised 16 black and white video cameras (Computar FC 55) equipped with wide-angle lenses, and four quad splitters (Computar QS-MX) enabling each simultaneous recording from four cameras onto a time-lapse video-recorder (Hitachi VT-L2500E) and four black and white monitors (Computar CEM-12). Half of the animals in each group were recorded during week 1 and the other half during week 2 in each month. Significant differences between weeks within a month were not found. Videograms were recorded at a frequency of 1.25 per second. During dark hours, each cage was lit with two dim red lights (Philips E27ES, 60 W). The ethogram was analysed from video tapes using the instantaneous sampling method (Martin and Bateson 1986) with a sampling interval of 2 min. In the case of stereotypies, however, continuous

KORHONEN ET AL. BEHAVIOUR OF FARMED BLUE FOXES 191 Table 1. Description of original behaviour categories Code Category Description 1 Sit Sitting on hind legs 2 Stand Standing on four legs 3 Run Running gait 4 Walk Ambulatory gait 5 Eat/drink Eating food, drinking/mouth at drinking nipple 6 Self-groom Licking, pulling at body/pelage 7 Defecate Defecating 8 Rest Lying down with eyes open or closed 9 Change position Changing position of the body at rest 10 Scratch Scratching something with forepads 11 Tail chase Repetitive chasing of tail 12 Slow-circle Circling around 13 Non-stop-cicrle Repetitive circling around 14 Slow-pace Pacing around 15 Non-stop-pace Repetitive pacing around 16 Slow-pace/N Pacing around with a neighbour 17 Non-stop-pace/N Repetitive pacing with a neighbour 18 Jump alone Repetitive jumping up, hind legs leave the floor 19 Social junp Repetitive jumping up with neighbour 20 Wall bounce Jumping at wall 21 Wall bounce/n Jumping at wall with neighbour 22 Coprophagy Eating own faeces 23 Tail bite Biting at tail 24 Bite Biting other part of the body 25 Agonistic bite Biting the other fox 26 Somersault Making somersaults 27 Lurk Lurking 28 Dig Digging with forepads 29 Cache food Burying food in earthen floor 30 Play Playing with faeces, hair etc. 31 Head rolling Repetitive circling or twirling of head 32 Bite the cage Biting the cage 33 Lick the cage Licking the cage 34 Social groom Licking, grooming the other fox 35 Chase Chasing the other fox 36 Dominate Bodyposture high; tail up; head and ears upfront 37 Submissive Bodyposture low; ears back and tail pressed down 38 Tread Underfoot the other fox 39 Fight Intensive physical contact 40 Sniff Nose to air or sniffing with another fox analysing was performed whenever it was necessary. After the initial examination of video data, the behavioural elements shown in Tables 1 and 2 were extracted. The original behavioural categories were reorganised for later analyses according to Table 3. Statistical Methods The foxes were group-housed, two animals per cage, 10 cages per treatment, such that the experiment had 10 blocks of four cages. So, cage was used as the experimental unit in each analysis of variance. For each fox, there were repeated measurements at four different months. Typically, the repeated measurements are correlated. Correlation was taken into account in the statistical models. The covariance structure of the repeated measurements was chosen comparing all biologically sensible structures using Akaike s and Schwarz s Bayesian information criterion (Wolfinger 1996). The compound symmetry covariance structure proved useful except for total activity and inactivity. The analysis of each original and each reorganised behavioural element was based on the following statistical model: Y ijk = µ + B j + C i + δ ij + T k + (B T) jk + (C T) ik + ε ijk where Y is the mean of two foxes housed in one cage. µ is the intercept and C i is the fixed effect of the ith cage. B j and δ ij represent the normally distributed random effect associated with the jth block and the block group interaction (= variation between cages), respectively. This first part of the model is equivalent to the randomised complete block ANOVA. This ANOVA was used if the behavioural element occurs rarely and the effect of the month and the cage month interaction cannot be estimated with sufficient accuracy. T k and (C T) ik represent the fixed effect of the month and the cage month interaction. (B T) jk represents the normally distributed random effect of the block month interaction. ε ijk are correlated residual errors (Gumperetz and Brownie 1993). The statistical model for circadian change was identical to that in the previous model, when the period took the place of the month. The assumptions of the models were checked by graphical methods: box-plot for normality of errors and plots of residuals for constancy of error variance (Neter et al. 1996). Usually, the assumption of constancy of error variance was achieved with log or square-root transformation. In these cases, all presented estimates were transformed to the original scale. The 95% confidence interval for means was used to present the accuracy of means instead of the standard error of means due to transformation. The parameters of the models were estimated by the restricted maximum likelihood (REML) estimation method using the SAS system for Windows, release 6.12, and MIXED procedure. Because the numerous statistical tests made data extrapolation from the tables difficult, all P values greater than 0.08 were marked not significant (NS), thus enabling P values near the statistical significant value 0.05 to be taken into account. RESULTS Original Behaviour Elements Several significant differences were found in original behaviour elements between the experimental groups (Table 2). These were more common between cage sizes than between floor materials. Foxes ran and walked more on the earthen (E500) than on the wire-mesh floor (W500). Correspondingly, foxes rested least on the earthen floor. Running, walking and chasing increased whereas resting and sitting decreased with cage size. Play was more common on the earthen floor than on the wire-mesh floor. Cage size had no effect on the amount of playing. Self-grooming was significantly higher in penned (W500, E500) than in shed groups (W50, W120). Furthermore, self-grooming was lower in E500 than in W500 foxes. Scratching was most frequent in W500 foxes. Most fights occurred in W120 cages. Wall bouncing as well as biting and tail biting declined with cage size. Tread was the most common and pacing the least

192 CANADIAN JOURNAL OF ANIMAL SCIENCE Table 2. Estimated LSMEANS (min/24 h) for original behaviour elements Code Variable W50 W120 W500 E500 P z 1 P 2 P 3 P 4 1 Sit 23 164 116 122 <0.001 <0.001 <0.001 NS 2 Stand 20 19 34 45 <0.001 <0.001 <0.001 0.04 3 Run 0.1 0.2 3.0 4.7 y <0.001 <0.005 4 Walk 18 38 72 88 <0.001 <0.005 <0.001 0.02 5 Eat/drink 68 76 34 35 <0.001 <0.005 <0.001 NS 6 Self-groom 44 51 93 87 <0.001 <0.001 <0.001 NS 7 Defecate 5 8 5 6 <0.001 <0.001 0.01 NS 8 Rest 939 939 907 864 <0.005 <0.001 0.02 <0.005 9 Change position 7 8 9 6 <0.001 <0.001 <0.005 <0.001 10 Scratch 7 7 21 12 <0.001 0.03 11 Tail chase 0.6 0.7 0.4 0.5 NS NS 12 Slow-circle 16 21 10 10 <0.001 <0.001 <0.001 NS 13 Non-stop-circle 0.7 0.6 0.5 0.7 NS NS 14 Slow-pace 4 14 16 12 <0.001 <0.001 <0.001 NS 15 Non-stop-pace 0.5 2.7 2.3 2.2 <0.001 <0.005 <0.001 NS 16 Slow-pace/N 0 0.3 2.2 1.8 <0.001 NS 17 Non-stop-pace/N x 0 0.2 0.7 0.6 <0.001 NS 18 Jump alone 28 23 32 34 <0.001 <0.001 NS NS 19 Social jump 0.5 0.6 0.4 0.3 NS NS 20 Wall bounce 25 19 9 12 <0.001 <0.001 <0.001 NS 21 Wall bounce/n 0.5 0.6 0.4 0.3 NS NS 22 Coprophagy 2.0 2.3 5.0 12.4 <0.001 <0.001 <0.001 <0.001 23 Tail bite 0.3 0.2 0.1 0.1 <0.001 NS 24 Bite 4.6 2.3 2.0 2.4 0.01 <0.001 <0.001 NS 25 Agonistic bite 1.5 1.5 0.6 0.7 <0.001 NS 26 Somersault 0.1 0.1 0.1 0.1 NS NS 27 Lurk 0.2 0.4 0.9 0.9 <0.001 NS 28 Dig 0 0 0 15 <0.001 NS 29 Cache food 0 0 0 0.1 NS 30 Play 0.8 0.6 0.9 1.5 NS 0.04 31 Head rolling 0.1 0.1 0 0 32 Bite the cage 4.0 4.0 4.7 5.8 0.01 NS NS 33 Lick the cage 0 0 0.5 0.5 <0.001 NS 34 Social groom 3.1 4.5 2.7 2.8 NS NS 35 Chase 0.1 0.4 0.8 1.3 <0.001 NS 36 Dominate 0.7 0.7 0.3 0.4 <0.001 NS 37 Submissive 1.6 2.1 2.2 3.3 NS 0.06 38 Tread 0.8 0.3 0.2 0.2 <0.001 NS 39 Fight 17 26 15 15 <0.001 <0.001 <0.001 NS 40 Sniff 1.6 2.2 9.0 8.2 <0.001 NS z P 1, effect of month group; P 2, effect of month; P 3, effect of cage size (W50 vs W120 vs W500); P 4, effect of floor material (W500 vs E500). y indicates that behaviour was too rare for statistical analyses. x N = with neighbour. Table 3. Reorganised behaviour categories. Original behaviours shown in Table 1 were grouped into new elements as shown here Variable Description Activity All-1,2,8 Locomotion 3,4,9,10,11,12,13,14,15,16, 17,18,19,20,21,26,28, 29,30,31,35,39 Locomotor stereotypy 10,11,13,15,17,18,19, 32 Oral Activity 5,6,22,25,34 Oral Stereotypy 23,24,32 Total stereotypy Locomotor stereotypy + oral stereotypy Non-stereotypic activity Activity-total stereotypy Jumping 18,19,20,21 Alimentary 5,7,22,29 Socialising within cage 25, 34, 36,37,38,39,40 Socialising between cages 16,17,19,21,40 Total socialising Socializing within cage + between cages Agonistic behaviour 25,36,37,38,39 common in the smallest cage (W50). Sniffing was more common among penned than among shed foxes. The time spent on eating/drinking was greater among foxes in sheds (W50, W120) than among those in pens (W500, E500). Coprophagy was most common on the earthen floor. Digging activity varied daily, being on average 15 min/24 h in the earthen pen. Only 5 out of 20 studied foxes dug on each study day. Two foxes did not dig at all on 5 out of 20 study days. In addition, four foxes did not dig on 4 out of 20 study days. Digging activity peaked in August (21.6 min/24 h). Thereafter, the following declining tendency was found: 14.8 min/24 h in September, 15.2 min/24 h in October and 8.9 min/24 h in November. Reorganised Behaviour Elements Main and Interaction Effects of Group and Month Table 4 provides a detailed summary of the main and interaction effects between reorganised behaviour elements. The

KORHONEN ET AL. BEHAVIOUR OF FARMED BLUE FOXES 193 Table 4. Estimated LSMEANS (min/24 h)for reorganised behaviour elements. 95% confidence intervals for LSMEANS are given in parentheses Variable W50 W120 W500 E500 P z 1 P 2 P 3 P 4 Activity 249 312 381 402 <0.001 NS <0.001 NS 232, 267 291, 336 356, 409 375, 432 Locomotion 109 157 201 224 <0.001 <0.001 <0.001 NS 92, 126 137, 178 179, 225 200, 249 Locomotor stereotypy 10 13 26 16 <0.001 <0.001 <0.001 <0.001 9, 12 11, 15 22, 32 14, 20 Oral activity 122 137 152 149 <0.001 <0.001 <0.001 NS 117, 136 127, 150 144, 167 142, 165 Oral stereotypy 6.6 4.6 5.8 7.4 <0.001 0.02 0.04 0.08 5.4, 8.0 3.8, 5.7 4.8, 7.0 6.1, 9.0 Total stereotypy 17 18 33 24 <0.001 <0.001 <0.005 <0.001 15, 20 15, 21 28, 39 21, 29 Non-stereotypic activity 229 293 346 377 <0.001 0.05 <0.001 0.03 214, 246 274, 314 324, 371 352, 403 Jumping 27 21 13 15 <0.001 <0.001 <0.001 NS 21, 36 16, 28 10, 16 12, 20 Alimentary 75 87 42 54 <0.001 <0.001 <0.001 <0.001 69, 81 79, 94 39, 46 49, 58 Socialising within cage 26 37 24 25 <0.005 <0.001 <0.001 NS 21, 31 31, 43 20, 30 21, 31 Socialising between cages 1 2 12 10 <0.005 <0.001 <0.001 NS 0, 1 1, 2 10, 14 9, 12 Total socialising 27 39 38 37 <0.01 <0.001 <0.001 NS 22, 32 43, 45 33, 44 31, 42 Agonistic 1.6 2.1 2.2 3.3 y NS 0.06 1.2, 2.2 1.6, 2.9 1.6, 3.0 2.5, 4.5 z P 1, effect of month group; P 2, effect of month; P 3, effect of cage size (W50 vs W120 vs W500); P 4, effect of floor material (W500 vs E500). indicates that behaviour was too rare for statistical analyses. effect of month group was statistically significant in most behavioural variables. This implies that the difference between groups varied somewhat from month to month. However, this interaction was biologically unimportant in most variables, because the preference of cage types followed the same pattern each month. Activity and locomotion were lowest in W50 foxes and tended to increase with increasing cage size. Floor material affected activity only in November when it was higher in the E500 than in the W500 group. Locomotion was higher in E500 than in W500 foxes each month. Locomotor stereotypy increased with increasing cage size. The amount of locomotor stereotypy was lower (P < 0.04) in the W50 than in the W120 group. In each month, locomotor stereotypy was higher in W500 than in E500 foxes. Differences in oral stereotypy between groups varied from month to month. Floor material affected incidences of oral stereotypy only in November, being higher in W500 foxes. Total stereotypy levels increased with increasing cage size except in November, when it was lowest for W120 foxes. Total stereotypy levels were affected by floor material. They were higher in the wire-mesh than in the earthen pen. This effect, however, weakened with advancing time and, in November, floor material had became nonsignificant. Jumping was more common under shed than under pen conditions. Furthermore, jumping tended to decrease with increasing cage size. Floor material did not substantially affect the amount of jumping. Alimentary behaviour was significantly lower in penned than in shed groups. In August, alimentary behaviour was higher in E500 than in W500 foxes. Thereafter the group difference declined with time, having totally vanished by November. Socialising within the cage was most common in W120 foxes except in November, when no differences were found. In contrast to cage size, floor material had no effect at all on socialising within the cage. Socialising between cages was significantly lower in the shed than in the penned groups. Incidences of agonistic behaviour were not affected by cage size. Agonistic behaviour tended to be higher in E500 than in W500 foxes. Circadian Effect The 24 h of the day were divided into three circadian time intervals (0 8 vs. 8 16 vs. 16 24 h) to evaluate circadian periodic changes. The period 8 16 h represents working hours, 16 24 h evening and 0 8 h night. Significant periodic changes were found for all behavioural variables except socialising between cages (Table 5). The effect of time group analysis revealed that circadian periodic differences in all housing groups followed the same pattern for locomotor stereotypy, oral stereotypy, total stereotypy and agonistic behaviour. Activity was concentrated most and least frequently between 8 and 16 and 0 and 8 h, respectively. The same tendency was found for sitting, standing and locomotion. Locomotor stereotypy and oral stereotypy were at their lowest between 0 and 8 h in each group. Oral activity occurred least frequently between 0 and 8 h. Significant circadian differences were found in digging activity (P < 0.001). Digging occurred least frequently between 8 and 16 h (3.9 min/8 h). Between 0 and 8, and 16 and 24 h it amounted to 5.1 and 6.6 min/8 h, respectively. Scratching

194 CANADIAN JOURNAL OF ANIMAL SCIENCE Table 5. Estimated LSMEANS (min/8h) for circadian changes in reorganised behaviour elements. Variable 0 8 8 16 16 24 P z 1 P 2 Activity 89 128 119 <0.005 <0.001 82, 96 119, 136 111, 128 Locomotion 47 67 57 <0.005 <0.001 42, 52 62, 73 52, 63 Locomotor stereotypy 4.9 5.8 6.4 NS <0.005 4.2, 5.7 5.0, 6.7 5.5, 7.3 Oral activity 36 52 53 <0.001 <0.001 34, 41 50, 57 50, 58 Oral stereotypy 1.9 2.5 2.7 NS <0.001 1.6, 2.2 2.2, 2.8 2.4, 3.0 Total stereotypy 6.7 8.1 8.9 NS <0.001 5.8, 7.7 7.1, 9.3 7.7, 10.2 Non-stereotypic activity 82 119 110 <0.005 <0.001 76, 89 111, 127 103, 118 Jumping 6.0 9.4 5.0 <0.005 <0.001 4.9, 7.2 8.0, 10.8 3.9, 6.0 Alimentary 12 26 26 <0.001 <0.001 11, 14 24, 30 23, 29 Socialising within cage 9 9 12 <0.01 <0.001 8, 10 8, 11 11, 14 Socialising between cages 1.2 1.3 1.2 <0.01 NS 1.0, 1.4 1.1, 1.5 1.0, 1.4 Total socialising 11 12 15 <0.005 <0.001 9, 12 10, 13 13, 16 Agonistic 0.6 0.9 0.8 NS 0.03 0.4, 0.8 0.7, 1.2 0.6, 1.0 z P 1, effect of time group; P 2, effect of time. was most common between 16 and 24 h. Socialising within the cage was most common between 16 and 24 h. No circadian periodic changes were noted in socialising between cages. Agonistic and alimentary behaviours were least frequent between 0 and 8 h. DISCUSSION One of the potential first steps in evaluating animal behaviour in a certain environment is to develop an ethogram, i.e., a largely complete catalogue of an animal s behavioural repertoire (Banks 1982; Mench and Mason 1997). The next step is to establish a baseline against which to compare it. An animal s behaviour in the wild is often considered a reasonable reference (Dawkins 1989; Mench and Mason 1997). The logic behind such a comparison seems to lie in the assumption that a healthy wild animal is likely to have adequate welfare. Thus, if a captive animal behaves in a similar way, it is plausible that its welfare is comparable (Veasey et al. 1996). This approach has its limitations, however, particularly because of the shortage of data on behaviour in the wild. Also, in the case of blue foxes, only a few previous ethograms are available. Frafjord (1986) presented 33 different behaviours for blue foxes living in the wild (i.e., the Arctic fox) whereas the catalogue of Kronholm (1994) included 28 behaviours described in seminatural ground floor enclosures. In the present study, 40 different behaviours were classified. In terms of behaviour categories, it appears that the behavioural repertoire of farm-raised blue fox is fairly wide-ranging. Quite another matter is to what extent the behaviour actually resembles that observed in the wild or under extended semi-natural conditions and to what extent one can draw conclusions regarding welfare from that resemblance. Comparisons between different ethogram studies should be done cautiously, for example, because they have been conducted at different times of the year and on different group sizes and sex combinations. Furthermore, Frafjord s study was purely descriptive, and that of Kronholm was also mostly descriptive, which makes comparisons between them and the present study difficult. Nevertheless, at least one major difference was found, namely, in food caching. Frafjord mentioned that Artic foxes were very adept at this behaviour, which they performed frequently. In the present study, little food caching was documented and then only in E500 foxes. Some food caching was also observed in the study of Kronholm (1994). The obvious explanation for the high rate of food caching in the wild is that it is necessary for survival under Arctic conditions because food availability varies dramatically year round. Under captive conditions, in contrast, food is regularly but not very excessively available all the time. If the wild cannot be used as a reliable benchmark against which to measure behavioural deviations, an alternative might be to compare ethograms referring to different captive conditions (Friend and Dellmeier 1988). Such a comparison is often technically easier and thus able to provide more accurate, unbiased data than when trying to compare behaviour between wild and captivity. In the present study, ethograms were compared between four different housing conditions. Each of 40 different behaviour categories described, except digging the ground, were noted in each housing option. As Table 2 shows, several more-or-less significant differences existed between the options studied.

KORHONEN ET AL. BEHAVIOUR OF FARMED BLUE FOXES 195 Although statistically significant, the differences in duration were often rather small. Thus, interpretation of the biological meaning of these results is not necessarily unambiguous. One of the most distinct differences was documented in the amount of walking and running. These occurred more frequently in large (W500, E500) than in smaller cages (W50,W120). In addition, foxes on the earthen floor pen (E500) walked and ran more than did those on the wiremesh floor (W500). It appears that both space quantity and floor material affect the ability and/or willingness of farmed foxes to walk and run. The key factors providing insight into how animals cope in a certain environment are often behavioural disorders. Particularly when kept in considerable restricted housing environments, animals tend to behave in a manner that appears contextually inappropriate or otherwise beyond the natural repertoire (Fraser and Broom 1997). The most striking behavioural symptoms are possibly stereotypies that are repetitive actions with a fixed form and orientation and serving no obvious function (Ödberg 1978; Redbo 1992). Stereotypies are interesting in terms of animal welfare because they are abnormal in the sense that they do not occur in the wild. However, the interpretation of stereotyped behaviour is not always straightforward. There are two previous studies available on stereotypies in farmed blue foxes. Wikman et al. (1998) analysed the behaviour of 3- to 5-moold animals in cages measuring 115 cm long 105 cm wide 70 cm high. They found that the total amount of time spent on stereotypies averaged 26 min/24 h. In another study, Korhonen et al. (2000b) compared incidences of stereotypies between three wire-mesh cages, 80 cm, 120 cm and 240 cm in length. The mean time used for stereotypies in different cage sizes ranged from 12 to 16 min/24 h. The amount of total stereotypy found in the present study is fairly close to that of the previous studies. All three studies support the conclusion that stereotypies do not occur very frequently in blue foxes. Clear evidence can be found from the present data that cage size affected the type of activity. The amount of locomotion in W50 foxes was about half of that in W500 and E500 foxes. Instead of locomotion, W50 foxes sat for about twice as long as did W500 or E500 foxes. The extremely small cage markedly restricted horizontal movements, forcing W50 foxes to jump vertically significantly more frequently than penned foxes. The amount of locomotor stereotypy in minutes was lowest and highest in W50 and W500 foxes, respectively. The result was the same when calculated as a proportion of locomotion (9.2% vs. 12.9 %). The corresponding proportions for functional activity were 4.0% and 6.8%, respectively. All these comparisons reveal that, surprisingly, stereotypy was lowest in the extremely small cage. There are two explanations for this: (1) the observed difference is real or (2) the low amount of locomotor stereotypy in W50 foxes is due to fact that cage size was too small for even stereotypic activity and led to a certain passiveness. Because the amount of locomotion in W50 foxes was low, it is tempting to conclude that the latter explanation is more plausible than the former one. On the other hand, one can assume that if cage size is too small for locomotor stereotypy, the animal will, instead, develop more stationary stereotypies. The amount of head rolling, however, did not substantially differ between the housing options studied. Another behaviour that can be considered here as a stationary stereotypy, i.e., tail biting, was highest in the smallest cage and decreased with increasing cage size. This stereotypy occurred seldom, however, in all options. Comparisons of floor materials also leads to ambiguous conclusions. No significant differences were noted in locomotor activity between W500 and E 500 foxes but the amount of locomotor stereotypy was significantly lower on the earthen (E500) than on the wire-mesh (W500) floor. Oral activity was of the same order of magnitude in both groups but oral stereotypy, on the other hand, was higher in E500 foxes. Thus, it appears that the earthen floor reduces locomotor stereotypy but increases oral stereotypy. One problem in interpreting this result, and also some others, is that although statistically significant, the difference in minutes was not very large, and thus estimation of its practical meaning is difficult. According to the European Convention (1999), the housing conditions of farmed foxes should provide an opportunity for social behaviour. The present results reveal that the amount of social behaviour within the cage was of the same order of magnitude in W50 as in W500 and E500 cages. In W120 it was the highest. It appears that even the smallest cages do not restrict within-cage social behaviour. However, between-cage social behaviour in W50 and W120 foxes was very low compared with that in penned foxes. It is difficult to see the actual mechanism whereby small cage size restricts social behaviour between cages. The low amount of social behaviour between cages might, however, be a sign of a certain passiveness towards their surroundings among W50 and W120 foxes. An alternative explanation is that due to the large distance between foxes, those in pens made an active effort to seek neighbouring contacts. In small cages this is not needed because of the permanent close proximity of neighbours. A larger space also means a larger territory, patrolling and defending of which also requires considerable amount of social contacts with neighbours. Evaluation of fur properties (Korhonen et al. 1999b, 2000b) has revealed that the fur of penned foxes (W500, E500) was significantly dirtier than that of shed cage foxes (W50,W120). This was attributed to the fact that penned conditions exposed the animals to outdoor conditions (rain, sunshine, wind, floor effect, etc.) more than shed cage conditions did. Present video recordings additionally reveal that the amount of self-grooming was much greater in penned foxes than in shed cage foxes, which may be explained by the dirtier fur of the penned foxes. Farmed blue foxes are typically most active between 8 and 16 h (Korhonen and Niemelä 1998). This was also the case in the present study. Furthermore, previous studies have shown that digging (Korhonen et al. 1999a) and object chewing (Korhonen and Niemelä 2000) occur least often during 8 16 h, i.e., when the personnel are working on the farm. The obvious explanation for this activity pattern is that human activity during working hours provides adequate external stimuli that can eliminate other stimulus-seeking

196 CANADIAN JOURNAL OF ANIMAL SCIENCE activities. During the remaining time, no personnel or any out-of-cage activities are conducted on the farm, and, therefore, the foxes appear to seek additional stimulus by digging or object interaction. In the present study, digging also occurred mostly outside working hours, suggesting that foxes seek extra stimulus or satisfy a recreational need by digging. The need to dig can be assessed from the present data in two ways. The amount of time spent digging provides us with a general overview of the situation. The foxes were found to dig 15 min per day, which is actually not very much. In addition, one can assume that if a certain behaviour, such as digging, is important for foxes, it should occur rather regularly. In the present study, however, the foxes did not dig every day and the time they spent digging varied within and between months. These figures do not provide sufficient evidence to demonstrate that digging is a crucial need for farmed blue foxes. Some previous data support the conclusion that farmed foxes are not very motivated to dig (Korhonen et al. 1999b,c). Further studies are needed to prove or disprove this assumption. According to Fraser (1992), a simple comparison of animal behaviour in different environments may identify interesting differences, but such an approach does not by itself allow us to conclude which of the differences are positive, negative or neutral in terms of welfare. Additional recent data are also available on the welfare-related physiological and behavioural responses of present foxes (Korhonen et al. 2000a). Such indicators as cortisol levels, ACTH response and size of adrenals showed that foxes in any of the four housing option did not suffer from long-term stress (Korhonen et al. 2000a). The amount of time spent performing stereotypies in the present study supports this conclusion. Bone strength was lowest in the W50 foxes and greatest in the E500 foxes. This coincides with the observation that foxes moved least in W50 cages and, correspondingly, most in E500 pens. Heart weight was also greatest in penned foxes (Korhonen et al. 2000a), obviously due to their greater locomotor activity. Feet were least bent in E500 foxes, indicating that locomotion may be easier on an earthen floor than a wire-mesh floor. It seems that at least the smallest cage size (W50) may compromise the welfare of foxes. CONCLUSIONS The behaviour repertoire of farmed blue foxes seems to be fairly wide-ranging because 40 different behaviours were classified. Several significant differences in behaviour between different housing conditions were noted, but the biological meaning of these differences was not necessarily unambiguous. The amount of space, in particular, appears to have a marked effect on the activity of animals. The amount of stereotypic behaviour was low in general. The results of this study and of a companion physiological study suggest that the standard cage environment (W120) does not substantially compromise the welfare of foxes born under farm conditions. The smallest cage size (W50), on the other hand, may compromise welfare; because of a restricted ability to move, foxes have smaller hearts, the weakest tibia and the most bent posture of feet. ACKNOWLEDGEMENTS This study was financially supported by the Ministry of Agriculture and Forestry. Great thanks to Mrs. Anne Iso- Niemi, Mrs. Tiina Huuki and Mrs. Aila Niemonen for analysing the video tapes and to Mr. Pekka Siirilä for computer assistance. Thanks are also due to Mr. Pekka Eskeli, Mr. Jaakko Huuki, Mr. Pekka Toikkanen, Mr. Aimo Joki- Huuki and Mr. Eero Uunila who cared for the animals. Ahola, L., Harri, M., Kasanen, S., Mononen, J. and Pyykönen, T. 2000a. Effects of group housing in an enlarged cage system on growth, bite wounds and adrenal cortex function in farmed blue foxes (Alopex lagopus). Anim. Welf. 9: 403 412. Ahola, L., Harri, M., Kasanen, S., Mononen, J. and Pyykönen, T. 2000b. Effect of family housing of farmed silver foxes (Vulpes vulpes) in outdoor enclosures on some behavioural and physiological parameters. Can. J. Anim. Sci. 80: 427 434. Banks, E. M. 1982. Behavioural research to answer questions about animal welfare. J. Anim. Sci. 54: 434 446. Berg, H. 1986. Rehutietoutta turkiseläinkasvattajille. Turkiseläintutkimuksia 23. Suomen Turkiseläinten Kasvattajain liitto ry. Vaasa. 99 p. Canadian Council on Animal Care. 1993. Guide to the care and use of experimental animals. 2nd ed. Vol. 1. CCAC, Ottawa, ON. Dawkins, M. S. 1989. Time budget in red junglefowl as a baseline for the assessment of welfare in domestic fowl. Appl. Anim. Behav. Sci. 24: 77 80. European Convention. 1999. Standing Committee of the European Convention for the Protection of Animals Kept for Farming Purposes (T-AP). Recommendation Concerning Fur Animals. The Standing Committee. 37th meeting, Strassbourg 22 25 June 1999. 23 pp. Frafjord, K. 1986. Etogram over fjellrevens atferd i hiområdet. Medd. Nor. Viltforsk. 15: 1 52. [English summary: An ethogram of the arctic fox behaviour in the denning area.] Fraser, A. F. 1992. The behaviour of the horse. CAB International, Wallingford, UK. pp. 226 263. Fraser, A. F. and Broom, D. M. 1997. Farm animal behaviour. 3rd ed. CAB Intrernational, Wallingford, Oxon, UK. 437 pp. Friend, T. H. and Dellmeier, G. R. 1988. Common practices and problems related to artificially rearing calves: an ethological approach. Appl. Anim. Behav. Sci. 20: 47 62. Gumperetz, M. L. and Brownie, C. 1993. Repeated measures in randomized block and split-splot experiments. Can. J. For. Res. 23: 625 639. Harri, M., Mononen, J. and Sepponen, J. 1999. Preferences of farmed silver foxes (Vulpes vulpes) for four different floor types. Can. J. Anim. Sci. 79: 1 5. Korhonen, H. and Niemelä, P. 1998. Seasonal and circadian changes in activity rates of adult farm blue foxes. Agric. Food Sci. Finl. 7: 21 29. Korhonen, H. and Niemelä, P. 2000. Enrichment value of wooden blocks for farmed blue foxes (Alopex lagopus). Anim. Welf. 9: 177 191. Korhonen, H., Jauhiainen, L. and Niemelä, P. 1999a. Effect of enlarged cage space and access to earthen floor on locomotor and digging activity in blue foxes. Agric. Food Sci. Finl. 8: 253 263. Korhonen, H., Niemelä, P. and Jauhiainen, L. 1999b. Effect of space allowance and floor material on fur properties in blue foxes. NJF seminar nr. 308, Reykjavik, Iceland, 21 24 October 1999. 8 pp. Korhonen, H., Wikman I. and Niemelä, P. 1999c. Digging activity and motivation in penned blue foxes. Proceedings of the 33rd International Congress of the International Society for Applied Ethology, 17 21 August 1999, Lillehammer, Norway. pp. 173.

KORHONEN ET AL. BEHAVIOUR OF FARMED BLUE FOXES 197 Korhonen, H., Jauhiainen, L., Niemelä, P., Harri, M. and Sauna-aho, R. 2000a. Physiological and behavioural responses in blue foxes: comparisons between space quantity and floor material. Anim. Sci. (in press). Korhonen, H., Niemelä, P., Jauhiainen, L. and Tupasela, T. 2000b. Effects of space allowance and earthen floor on welfarerelated physiological and behavioural responses in blue foxes. Physiol. Behav. 69: 571 580. Kronholm, A. 1994. Sexual differences in parental investment and behaviour during weaning in arctic foxes, Alopex lagopus, in a semi-natural environment. Specialarbete 20. Swedish University of Agricultural Sciences, Faculty of Veterinary Medicine, Department of Animal Hygiene. 41 pp. Martin, P. and Bateson, P. 1986. Measuring behaviour: an introductory guide. Cambridge University Press, London, UK. 200 pp. Mench, J. A. and Mason, G. I. 1997. Behaviour. Chapter 9, pages 127 141 in M. C. Appleby and B. O. Hughes, eds. Animal welfare. CAB International, Wallingford, Oxon, UK. Neter, J., Kutner, M., Nachtsheim, C. and Wasserman, W. 1996. Applied linear statistical models. 4th ed. Irwin, Chicago, IL.1310 pp. Ödberg, F. O. 1978. Abnormal behaviours: Stereotypies. Pages 475 480 in Proceedings from the 1st World Congress on Ethology Applied to Zootechnics, at Madrid. Pedersen, V. 1993. Evaluation of the welfare of farmed foxes based on behavioural and physiological measurements. NJF seminar no. 239, 23 26 September 1993, Oslo, Norway. Pedersen, V., Jeppesen, L. L. and Skovgaard, K. 1995. Effekten af forskellige indhusningssystemer på solv- och blåraevens adfaerd, fysiologi, reproduktion og skinkvalitet. NJF seminarium 4 6 October 1995, Göteborg, Sweden. 6 pp. Pedersen, V. and Jeppesen, L. L. 1998. Different cage sizes and effects on behaviour and physiology in farmed silver and blue foxes. Scientifur 22:13 22. Pyykönen, T., Ahola, L., Jalkanen, L. and Harri, M. 1997. Behaviour of silver foxes (Vulpes vulpes) in ground floor enclosures. NJF-seminarium nr. 280, Helsingfors, Finland, 6 8 October 1997. pp. 125 131. Redbo, I. 1992. Stereotypies in dairy cattle. Ph.D. Thesis. Swedish University of Agricultural Science, Uppsala, Sweden. 49 pp. Skovgaard, K., Pedersen, V. and Jeppesen, L. L. 1995. Praeference for forskellige bundtyper hos blåraeve. NJF seminar, 4 6 October 1995, Gothenbourg, Sweden. Skovgaard, K., Pedersen, C. and Jeppesen, L. L. 1998. The preference different types of floor in silver foxes (Vulpes vulpes) and blue foxes (Alopex lagopus). Scientifur 22: 99 106. Veasey, J. S., Waran, N. K. and Young, R. J. 1996. On comparing the behaviour of zoo housed animals with wild conspecifics as a welfare indicator. Anim. Welf. 5: 13 24. Wikman, I., Mononen, J., Rekilä, T. and Harri, M. 1998. Stereotypies hos unga farmrävar. NJF-seminar nr. 295. Bergen, Norge, 7 9 September 1998. 6 pp. Wolfinger, R. 1996. Heterogeneous variance-covariance structures for repeated measures. J. Agric. Biol. Environ. Statistics 1: 205 230.