Welfare of farmed silver foxes (Vulpes vulpes) housed in sibling groups in large outdoor enclosures

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1 Welfare of farmed silver foxes (Vulpes vulpes) housed in sibling groups in large outdoor enclosures L. Ahola, M. Harri, J. Mononen, T. Pyykönen, and S. Kasanen Institute of Applied Biotechnology, University of Kuopio, P.O. Box 1627, FIN Kuopio, Finland ( Received 10 November 2000, accepted 15 May Ahola, L., Harri, M., Mononen, J., Pyykönen, T. and Kasanen, S Welfare of farmed silver foxes (Vulpes vulpes) housed in sibling groups in large outdoor enclosures. Can. J. Anim. Sci. 81: The aim of the present study was to evaluate the effects of housing farmed silver foxes in large outdoor enclosures with less abundant human contacts on some behavioural and physiological welfare parameters. Farmed silver fox cubs were housed either singly in traditional fox cages or in sibling groups in enclosures. Mass of adrenals, serum cortisol level after adrenocorticotrophic hormone (ACTH) administration and stress-induced hyperthermia, as well as 24-h activity measures and the number of bite scars, were used to draw conclusions on the welfare effects of housing farmed silver foxes in the two experimental housing systems. The housing system had significant effects neither on the serum cortisol level after ACTH administration nor on the mass of adrenals. This result shows that intra-group social tension and non-habituation to humans, both leading to increased long-term stress in foxes housed in large outdoor enclosures, can be partly overcome by, respectively, altering the group composition and keeping the cubs for a longer time in cage conditions with close human contact. However, a large number of bite scars and increased stress-induced hyperthermia (SIH) in the foxes housed in enclosures, indicating an acute stress response to the presence of humans, may not be overcome. Furthermore, the 24-h activity rhythm changed in the foxes housed in large enclosures resembling, especially in November, the nocturnal activity pattern of the wild red fox, indicating that the foxes in enclosures became at least to some extent feral. Key words: Activity rhythm, aggression, hypothalamic-pituitary-adrenal axis, human-animal relation, stress-induced hyperthermia, Vulpes vulpes Ahola, L., Harri, M., Mononen, J., Pyykönen, T. et Kasanen, S Bien-être des renards argentés (Vulpes vulpes) élevés en groupes dans de grands enclos extérieurs. Can. J. Anim. Sci. 81: L étude devait établir quels effets l élevage de renards argentés en semi-liberté, dans de vastes enclos en plein air, doublé de contacts moins for avec les humains, peut avoir sur certains paramètres comportementaux et physiologiques de l animal. Des renardeaux d élevage ont été gardés seuls dans des cages classiques ou en groupes dans un enclos. Pour évaluer les conséquences de chaque système expérimental, les auteurs se sont servis de la masse des surrénales, de la concentration de cortisol dans le sang après administration d ACTH et de l hyperthermie induite par le stress ainsi que du degré d activité circadien et du nombre de cicatrices attribuables à des morsures. Le type de logement n a aucune incidence sensible sur la concentration de cortisol dans le sang après administration d ACTH ni sur la masse des surrénales. Les résultats révèlent qu on peut atténuer partiellement le plus grand stress à long terme qu éprouvent les renards gardés en semi-liberté consécutivement à la tension sociale dans le groupe et au côtoiement des humains en modifiant la composition du groupe et en gardant les petits en cage plus longtemps, à proximité des humains, respectivement. Néanmoins, on pourrait ne pas surmonter le nombre accru de cicatrices venant des morsures ni la plus forte concentration de SIH résultant du stress plus intense causé par la présence des humains. Par ailleurs, le rythme circadien des renards élevés en semi-liberté subit une modification, de telle sorte qu il se rapproche du schéma d activité nocturne du renard roux à l état sauvage, en novembre surtout, signe que les animaux retournent au moins en partie à l état sauvage. Mots clés: Cycle d activité, agression, axe hypothalamo-hypophyso-surrénalien, relations animaux-humains, hyperthermie induite par le stress, Vulpes vulpes The European Convention (1998) stated in its recommendations concerning fur animals that, according to the natural behaviour of the red fox, farmed foxes should be provided with an opportunity to behave socially, i.e., housed in social groups. Although wild red foxes are often considered to be mainly solitary (Cavallini 1996) they can live in social groups (Macdonald 1983). However, group housing of foxes implies housing the two sexes together. In the wild, female foxes behave differently from male foxes when Deceased. 435 forming social bonds. Usually the social groups of the red fox consist of only one male fox and up to five females (Macdonald 1983). In general, male foxes are more loosely bonded to the social group they live in (Harris and White 1992). Therefore, it is not surprising that male cubs leave their natal group first (Harris and Trewhella 1988) and live a more solitary life. The consequence of not allowing the Abbreviations: ACTH, adrenocorticotrophic hormone; HPA, hypothalamic-pituitary-adrenal; SIH, stress-induced hyperthermia

2 436 CANADIAN JOURNAL OF ANIMAL SCIENCE male cubs to leave their mother s territory may lead to longterm stress reactions, as shown earlier by Ahola et al. (2000). Furthermore, the possibility for adequate species-specific locomotion in a larger area than the traditional cage is assumed to promote the welfare of farmed foxes (European Convention 1998). However, in our earlier study we found that the possibility to exercise in large enclosures (50 or 112 m 2 ) had no positive welfare effects, measured by the HPA-axis activity, in silver foxes (Ahola et al. 2000). On the other hand animals transferred into large enclosures had the possibility to avoid human contact, and thus may have experienced the presence of humans as aversive, which, in turn, may have reduced their welfare (Rushen et al. 1999). In the present study, we compared housing silver foxes either singly in a standard fox cage or in groups in outdoor enclosures; particular attention was paid to the effect on human-animal and animal-animal relations. In our earlier study, fox cubs transferred with their mother into enclosures after having lived in human proximity for 8 wk became fearful of people and showed a decreased welfare profile as a whole (Ahola et al. 2000). In the present study, we tried to ascertain whether a longer period of habituation to humans before the transfer would lead to less fearful animals. Furthermore, we tried to monitor the effect of the vixen in a social group on the welfare of her cubs by housing the cubs in sibling groups without their mother. Hypothalamic-pituitary-adrenal (HPA) axis activity, SIH, 24-h activity profiles and the number of animals with bite scars on their skin were used to draw conclusions about the welfare consequences of housing silver foxes in large enclosures as sibling groups. MATERIALS AND METHODS Animals and Housing Constructions An approval to conduct this study was granted by the Institutional Animal Care and Use Committee of the University of Kuopio (License No 99-68). Under this approval, the methods used for animal care were in accordance with the recommendations contained in the European Convention for the Protection of Animals Kept for Farming Purposes (European Convention 1998). All the cubs used were born in traditional fox cages ( cm, L W H) that were connected to a standard wooden nest box. The cubs were separated from their mother at the age of 8 wk and kept thereafter in sibling groups in a fox cage furnished with a plastic-covered wire mesh platform ( cm, L W, 27 cm from the cage ceiling). In mid-august, the litters were randomly divided into two experimental groups: the control group (group C) and the enclosure group (group E). The age of the cubs at that time was 110 ± 11 and 111 ± 11 d, respectively (between the groups: P > 0.1 ANOVA). In group C, one male and one female from 12 litters were housed singly in traditional fox cages furnished with a platform in an outdoor fur shed. In group E, six sibling groups from six litters, each consisting of two male and two female cubs, were transferred to the soil-floored outdoor enclosures. The sibling groups were standardised by removing any extra cubs from the family unit on the day of transfer. The soil-floored enclosures were fenced (2-m high) and roofed with wire mesh. Four enclosures measured m (W L) and two enclosures measured 5 10 m. In each enclosure, there were two nest boxes ( cm, L W H) and a resting shed. The resting shed consisted of a wooden floor ( cm, L W, 40 cm above ground level), a plastic-covered wire mesh resting platform ( cm, L W, 80 cm above ground level) and a slightly tilted sheet-iron roof ( cm, L W, cm above ground level). All animals were fed fresh fox feed twice a day until late September (i.e., until the cubs were approximately 21 wk old) and thereafter once a day. In group C, feed was delivered onto a feeding tray, while in group E feed was given on two plates placed on the floor of the resting shed. Water was available ad libitum for all animals. The health of the animals was checked daily. Measured Parameters In late September and in late November (cubs being approximately 21 and 29 wk old, respectively), 24-h activity of the cubs was observed. In group E, individually marked animals were directly observed from an observation tower (2.5 m above ground level) beside the enclosures. The animals were observed using scan sampling of the individuals in each enclosure as the sampling rule. The behaviour of the animals was recorded using instantaneous sampling with a 5-min sampling interval as the recording rule (Martin and Bateson 1993). The order of the animals being observed in each enclosure was the same from one observation to another. After observing the behaviour of the foxes in the first enclosure, observation was focused consecutively on the other enclosures. During 1 h, a total of 288 cub behaviour samples were obtained (i.e., 12 samples per individual per hour). In September, no extra lighting was used during the observations. In November, each enclosure was lit during the dark hours (16:00 08:00) with a dim florescent lamp (38 W) covered with a red plastic film. In group C, each fox was video-recorded for 24 h in September and in November. The video system consisted of six black and white video cameras (Ikegami CCD Model ICD 30 E) with wide-angle lenses (Cosmicar, 2.8 mm, 1:1.3 CS), a camera switcher (Computar CS8.1), a time-lapse video recorder (Hitachi VT-L2500E) and a black and white monitor (Philips 12TX3512). During the dark hours a dim red light (Osram, 25 W) for each two cages and a fluorescent lamp covered with red plastic film for each six cages was used in September and in November, respectively. The behaviour of the animals was analysed from video tapes using scan sampling with a 306-s sampling interval (i.e., each of the six cameras used recorded the behaviour of the animals in one cage for approximately 51-s, giving behavioural samples per animal per hour) (Martin and Bateson 1993). The behavioural categories for C and E cubs were: 1) active, i.e., moving, standing or sitting and 2) lying, i.e., lying awake or asleep. Because E cubs were not individually recognised in September during the dark hours

3 AHOLA ET AL. WELFARE OF FARMED SILVER FOXES HOUSED IN ENCLOSURES 437 (20:00 05:00) the activity was expressed as the mean value of four siblings in each enclosure (N = 6). Therefore, to be able to compare the results between the two groups and between the two time points, each family (group E) or its matched-paired group of four cubs in group C (matched by age and sex) was used as the data point. The time spent on active behaviours was analysed for the three 8-h periods of a day, i.e., early hours (00:00 0:800), working hours (08:00 16:00) and evening hours (16:00 00:00). Stress-induced hyperthermia was measured in late October (the age of the cubs being approximately 25 wk). Due to the diurnal variation in foxes deep body temperature with lowest temperatures between 07:00 and 16:00 (Moe and Bakken 1997), the SIH test was performed between 08:00 and 15:00. In group C, six neighbouring animals were successively caught in their home cages. The time needed to catch the animal (TIME) was recorded. TIME was determined as the time lapsed from the moment humans entered the shed for the first time to carry out the SIH test on the six animals, to the time the cub was captured in its cage. The rectal temperature (T re ) at the beginning of the test (T re0 ) was measured with a digital thermometer (Omron). Thereafter the fox was placed into a small wire mesh cage ( cm, L W H) situated inside the shed for 35 min and its T re was measured again (T re35 ) to obtain the maximum SIH (Moe and Bakken 1997). SIH was calculated as T re35 T re0. Except on the first day of the SIH test, only one set of six animals was tested during one day. On the first day, the two sets tested were situated in the shed some 13 m apart, and the animals in the set tested later were not disturbed by humans before the SIH test. In group E, TIME was determined as the time lapsed from the moment humans entered the enclosure for the first time to the time the cub was captured in the enclosure. The animals were caught successively from one enclosure at a time. After capturing the cub T re0 was measured and the cub was put alone into the small wire mesh cage situated inside the enclosure. T re35 was measured and SIH was calculated as in group C. At pelting time in January (the cubs being approximately 36 wk old), the foxes were caught and injected i.m. with ACTH (0.3 mg per animal synthetic ACTH 1-24, Synacthen Depot, Ciba). The foxes were placed alone into a smaller cage ( cm, L W H), and 2 h after the injection they were euthanised according to the methods recommended by the Standing Committee of the European Convention for the Protection of Animals Kept for Farming Purposes (European Convention 1998) by electrocution (Foxstop 1; Evikoje Ltd, Evijärvi, Finland) and blood samples were drawn with cardiac puncture. Serum cortisol level (mmol L 1 ), as a maximum response to ACTH administration (Fraser and Broom 1990; Rekilä et al. 1998; Ahola et al. 2000), was analysed by a competitive immunoassay technique (Coat-A-Count Cortisol Assay, Diagnostic Products Corporation, Los Angeles, CA). After pelting, both adrenals were removed, cleaned and weighed. Bite scars from the leather side of the fleshed skins were counted and localised in neck, throat, upper and lower back and belly or side areas. Statistical Analyses The Repeated Measures MANOVA was used to examine differences in activity level within and between the experimental groups. Independent-Samples T-test was used to test for differences between the groups and sexes in SIH and in the cortisol level after ACTH administration. Because no sex differences within experimental groups in the activity level (during the 8-h periods when the animals were individually recognised), in SIH and in the cortisol level after ACTH administration were found (for all P > 0.1), the results from both sexes were pooled. The adrenal mass correlated with the body mass of the animal (r = 0.638, P < 0.01 and r = 0.378, P = in group C and E, respectively, Pearson s correlation). Therefore, this value was adjusted for the effect of the body mass by using two-way ANCOVA with body size at the pelting time as a covariate. Differences in the incidence and in the number of bite scars in the skins between the experimental groups were examined using the Chi-square Test and the Mann-Whitney U-Test, respectively. All results are expressed as mean ± SE. RESULTS During the whole experiment, two female cubs were found dead in one enclosure (group E). One female died accidentally in mid-october, the other in mid-december because of an intestinal disorder. In group C, no cubs were found injured or dead. The effect of the housing system on the 24-h activity of the cubs was, in general, highly significant (group: P < 0.001) (Fig. 1). From September to November, a slight rise only (approximately 2% of time) in 24-h active time was observed (month: P = 0.072), and this rise was equal in both experimental groups (month group: P > 0.1). The effect of the time of day, i.e., the 8-h period, on activity was obvious in both groups (hours: P < 0.001) but this effect was different in the two groups (hours group: P < 0.001). While in group C the main activity occurred during the working hours (08:00 16:00), in group E the most active phase occurred during the evening (16:00 24:00). Furthermore, this difference in timing of the activity peaks between the experimental groups was even more pronounced in November than in September (month hours group: P < 0.001). TIME did not differ between groups C and E (P > 0.1) (Table 1), possibly because after the person had entered the enclosure to carry out the SIH test, most of the cubs housed in the enclosure fled into their nest boxes where they were easy to capture. No difference was found in T re0 between the two groups either (P > 0.1). Both T re 35 min after human exposure and restraint and the rise in T re during the test were significantly higher in group E than in group C (for both: P < 0.01). The serum cortisol level after ACTH administration was equal in both experimental groups (424 ± 13 and 430 ± 19 nmol L 1 in group C and E, respectively, P > 0.1). The adrenal mass differed neither between the experimental groups nor, after adjusting for the effect of the body

4 438 CANADIAN JOURNAL OF ANIMAL SCIENCE Fig. 1. Daily active time (% mean ± SE) in silver fox cubs housed singly in cages (open bars) and in sibling groups in outdoor enclosures (solid bars) during early hours (00:00 08:00), working hours (08:00 16:00) and evening hours (16:00 00:00). N = 6 four-animal sets in both groups. Table 1. Time (s) needed to catch the animal from its home cage/enclosure (TIME), rectal temperature ( C) immediately (T re0 ) and 35 min after capture (T re35 ), and increase in rectal temperature ( C) (T re35 T re0, T re ) in silver fox cubs housed singly in cages and in sibling groups in outdoor enclosures. Results are presented as mean ± SE Cages Enclosures N = 24 N = 23 P TIME (s) 357 ± ± 45 >0.1 T re0, ( C) 39.7 ± ± 0.1 >0.1 T re35 ( C) 39.8 ± ± 0.1 <0.01 T re ( C) 0.1 ± ± 0.2 <0.01 mass, between sexes (541 ± 31, 471 ± 19, 532 ± 17 and 471 ± 23 mg in C males, C females, E males and E females, respectively, P > 0.1). Sex difference in the number of animals with bite scars or in the number of bite scars in their skin was found neither in group C (P > 0.1) nor in group E (P > 0.1). The percentage of animals with bite scars was higher in group E than in group C (68.2 and 16.7%, respectively, P < 0.001). Furthermore, the number of bite scars per animal was higher in group E than in group C (6 ± 2 and 0 ± 0, respectively, P < 0.001). In group C, bite scars were observed on the neck (one bite scar), throat (one) and shoulders (five) of the foxes. In group E, the cubs had bite scars on the neck (17), throat (14), lower back (47), upper back (46) and sides (five). DISCUSSION In nature, many mammalian species are male biased in their dispersal behaviour (Greenwood 1980). This is the case in the wild fox; males are typically the ones to disperse first and further (Harris and Trewhella 1988) while females may stay in their natal territory with their mother, e.g., as helpers (Macdonald 1983). One ultimate hypothesis explaining this male-biased natal dispersion is inbreeding avoidance (Pusey 1987; but see Moore and Ali 1984). Based on this hypothesis, and on the observation that the male foxes are not as closely bonded to the social group as the females (Harris and White 1992), it could be argued that male cubs might experience stress if they are prevented from leaving their natal territory. Our earlier study showed that male silver fox cubs housed with their mother and sisters experienced more stress, as measured with HPA-axis activity, than cubs housed singly in traditional cages (Ahola et al. 2000). In the present study, no differences in the HPAaxis activity, i.e., in the cortisol level after ACTH administration (Fraser and Broom 1990; Broom and Johnson 1993; Terlouw et al. 1997) and in the adrenal mass (Gómez et al. 1996), were found between the cubs housed singly in cages and in sibling groups in enclosures. Therefore, it could be argued that the existence of females, especially older, dominant ones, or the looser family ties of males, in general, might be the social factors reducing the welfare of grouphoused male cubs. The more pronounced and positive effects of the littermates on the cubs welfare is further supported by the obviously tighter bonds between the littermates than between the mother and her cubs, because at least in some canids, the proportion of mother-offspring interactions is far less than the proportion of interactions within littermates (Scott 1967). Increased activity of the HPA-axis in farm animals may reflect a long-term stress reaction as a result of aversive human-animal relations (Hemsworth 1997; Rushen et al. 1999). In our earlier study, we concluded that inadequate human-animal relations resulted in a higher cortisol level after ACTH administration and in heavier adrenals in foxes housed in large enclosures than in foxes housed in traditional cage conditions (Ahola et al. 2000). In the present study no such effects were found. The reason for this might be a longer stay in farm cages with abundant human contacts prior to transfer to enclosures in the present study (approximately 16 wk) in comparison to our earlier study (8 wk). In silver foxes, the sensitive period of primary socialization begins when the cubs are approximately 3 wk old and lasts until the age of 6 wk (Belyaev et al. 1985). However, when foxes were selected for domestic behaviour the period was prolonged to the age of more than 9 wk. Under normal farming practice, breeding animals are selected for their tameness rather than for wildness and, therefore, it could be argued that the period of primary socialization would be longer in farmed silver foxes than in unselected populations.

5 AHOLA ET AL. WELFARE OF FARMED SILVER FOXES HOUSED IN ENCLOSURES 439 It seems obvious that the later transfer and the longer time spent in cage conditions with more abundant human contacts during the period of socialization resulted in more habituation to people. The positive effect (e.g., decreased fear response to people) of human contact during the period of socialization on later behaviour of the animals has earlier been detected in silver foxes handled early in their lives (Pedersen and Jeppesen 1990). However, the flight response during the SIH test (i.e., most of the cubs in the enclosures fled into their nest boxes immediately after human had entered the enclosure) as well as the increased SIH, indicating a strong acute fear reaction to the presence of human (Moe and Bakken 1997), was observed in the enclosures. Therefore, the foxes in outdoor enclosures were not under long-term stress, but experienced short-term stress at the times when humans were near to them. Thus, despite their initial high degree of habituation to human presence, the foxes became at least in some way feral (Daniels and Bekoff 1989) during their later stay in enclosures. The feralization process is often considered as the reverse of domestication, requiring genetic changes in population level (Price 1999) and thus being impossible to happen during one generation. However, it has also been suggested that feralization may include an ontogenetic process enabling an animal to become feral, determined by behavioural criteria, during its lifetime if it is never socialized to or is desocialized from humans (Daniels and Bekoff 1989). The present results show that when given the possibility to avoid human contact the foxes became desocialized from humans. One measure of their desocialization is the daily activity rhythm, which differs from that of people working on the farm, and also from that of foxes living in cages with abundant human contacts (Rekilä et al. 1998). The total time spent on active behaviours was higher in E than in C foxes throughout the experiment, but this increase was not equally distributed over the 24-h day or centred in working hours as in the C foxes. The main active phase in E foxes occurred during the evening, especially in November, resembling more the nocturnal activity pattern of the wild red fox (Harris and Lloyd 1991) and supporting our earlier results (Ahola et al. 2000). The larger space allocation for the foxes housed in sibling groups did not prevent the outbreak of bite wounds; E foxes had significantly more bite wounds on their skins than C foxes. The fact that singly housed foxes had bite wounds as well shows that some of these wounds may be either selfinflicted or already developed before weaning. During the first 5 wk, fox cubs form a stable dominance hierarchy through fighting aggressively and after this the level of aggression between the cubs declines (Henry 1986). In C cubs, most of the few bite wounds were found on the shoulder area, i.e., the area where the aggressive acts are especially directed during fights (Fox 1969). In E cubs, the number of bite wounds was also high in the lower and upper back. The location of the bite wounds suggests that the wounds were inflicted during aggressive acts rather than during play behaviour or during other social interactions (Fox 1969). The number of wounds was significantly higher in E foxes than in C foxes, indicating that aggressive acts occur after dominance hierarchy has been established for the first time. Further enlargement of the space is unlikely to prevent the incidence of bites because even under natural conditions with unlimited space available aggressive acts are common and up to 7% of red foxes may die in fights with conspecifics (Harris and Smith 1987). In conclusion, the intra-group social tension and nonhabituation to humans, both leading to increased long-term stress in foxes housed in large enclosures (Ahola et al. 2000), can be partly overcome by, respectively, altering the group composition (e.g., by excluding the vixen from the group) and keeping the cubs for a longer period in cage conditions within close vicinity to humans. However, aggressiveness between the group members and an acute stress response to the presence of human may not be prevented. The feralisation process, as defined by Daniels and Bekoff (1989), did not have any long-term stress effects as judged by cortisol response to ACTH administration and the adrenal mass. The lack of a long-term stress reaction following the feralisation process may, in fact, be beneficial if an individual is able to become feral in its lifetime, e.g., in a situation where is has been abandoned or has escaped from human care and, therefore, must cope with living conditions in the wild. However, foxes going through a feralisation process, yet being under human care, may experience the close proximity to humans as an aversive, frightening situation, and thus have impaired welfare (Rushen et al. 1999). Furthermore, because production animals are kept by people, fear of human can cause handling problems and increased incidence of injuries in both animals and humans. ACKNOWLEDGEMENTS This study was supported by the Research Council for the Environment and Natural Resources of the Academy of Finland, by the Ministry of Agriculture and Forestry, Finland and by the Finnish Fur Breeders Association (FFBA) through a joint project between FFBA and the Finnish Society for the Protection of Animals. We are grateful to Mrs. Maija Miskala for her skilful assistance during the field experiments. Ahola, L., Harri, M., Kasanen, S., Mononen, J. and Pyykönen, T Effect of family housing of farmed silver foxes (Vulpes vulpes) in outdoor enclosures on some behavioural and physiological parameters. Can. J. Anim. Sci. 80: Belyaev, D. K., Plyusnina, I. Z. and Trut, L. N Domestication in the silver fox (Vulpes fulvus Desm): Changes in physiological boundaries of the sensitive period of primary socialization. Appl. Anim. Behav. Sci. 13: Broom, D. and Johnson, K. G Stress and animal welfare. 1st ed. Chapman & Hall, London, UK. 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