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Effects of group housing systems on behaviour and production performance in farmed juvenile mink (Mustela vison)
Applied Animal Behaviour Science 88 (2004) 89–100
Effects of group housing systems on behaviour and production performance in farmed juvenile mink (Mustela vison) V. Pedersen∗ , L.L. Jeppesen, N. Jeppesen Department of Animal Behaviour, Biological Institute, University of Copenhagen, Tagensvej 16, Copenhagen N DK-2200, Denmark Received 7 July 2003; received in revised form 22 March 2004; accepted 22 March 2004
Abstract Juvenile mink were kept in two different group housing systems and their behaviour and physiology compared to that of juvenile mink kept traditionally in pairs. One group housing system was made by adjoining three traditional cages (row system) and the other by stacking a slightly smaller cage on top of a traditional cage (stacked system). Frequent scan sampling observations on behaviour and choice of stay were performed during 3 months on a focal female mink in each system. The occurrence and severity of damages to the fur was registered as well as morbidity and mortality in each system. The data showed that the frequency of stereotypies, auto-grooming and play did not differ significantly between systems. But the stacked system deviated significantly from both the traditional and row system in a number of occasions. There was a higher frequency of surveillance (P < 0.01), exploration (P < 0.01) and agonistic behaviour (P < 0.05) and a lower frequency of sleeping (P < 0.05) and eating/drinking (P < 0.05) in the stacked system. Morbidity and mortality was significantly higher in both group housing systems (9–11%), compared to the traditional system (0%). Group housing of juvenile mink, as practised in this experiment, could not be recommended from a welfare point of view. If group housing of mink, despite these findings, gets widely adopted, it is crucial that further research continues in order to find the appropriate stocking density, no. of feeding places and nest boxes, and optimal group composition acquired to obtain a good and acceptable welfare level in all individuals in the group. © 2004 Elsevier B.V. All rights reserved. Keywords: Mink; Groups; Social aggression; Stereotypies; Morbidity and mortality
∗
Corresponding author. Tel.: +45-35-32-13-04; fax: +45-35-32-12-99. E-mail address: [email protected] (V. Pedersen). 0168-1591/$ – see front matter © 2004 Elsevier B.V. All rights reserved. doi:10.1016/j.applanim.2004.03.003
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1. Introduction In the wild, mink is considered a solitary and highly territorial species (Birks, 1986; Dunstone, 1993). At mating time the male and female spend time together for a brief period but during pregnancy the female is alone in her territory. After parturition, during lactation, and for a few weeks more the female is together with her kits. Then the kits disperse to establish their own territories when 12–15 weeks of age (Birks, 1986; Dunstone, 1993). This natural way of living has to some extent been mimicked by man when keeping mink on farms. The male and female breeding stock is kept solitarily for most of the year. During the mating period the female is introduced to a male twice or thrice in his home cage. When mating has succeeded, the female continues to be housed solitarily during pregnancy. After parturition and nursing the kits for 6–7 weeks, the female is re-housed solitarily again. The litter stays together for a couple of weeks more and is then split into male/female pairs and housed as such for the remainder of the year. The breeding stock is selected in October and re-housed individually, whereas the surplus is killed. Keeping the juveniles as pairs during their growing period has been demonstrated to be better for their welfare than solitary housing: compared to pair housed juveniles, solitarily housed juveniles emitted more distress calls (Hansen et al., 1997), performed more stereotypies later in life (Jeppesen et al., 1990), and were more fearful towards humans and con-specifics (Hansen et al., 1997). In addition, their sexual development was inhibited leading to non-mating males and more barren females (Hansen et al., 1997) and their growth was inhibited (Møller, 1991). Juvenile mink also preferred to lie together rather than physically apart (Hansen et al., 1997). These studies all point in the direction that being housed with another mink is a positive social enrichment for juvenile mink. Studies of extended group housing in Denmark was initiated by the fact that the Dutch government implemented an Action plan of fur farming in 1996 (de Jonge, 1996), introducing group or family housing as the only acceptable way of keeping farmed mink in the Netherlands. At the time of this decision, only a limited amount of scientific evidence concerning the welfare consequences for mink in groups existed, and this evidence did not support the hypothesis of an improved welfare in group housed mink: as early as 1989, it was found that mink establish a social hierarchy when kept in groups (Houbak, 1989, 1990). This hierarchy was most persistent in males (being the most aggressive) with females being submissive to all males. No hierarchy between females was observed. The females and submissive males showed physiologically signs of stress reflected in high levels of eosinophil leucocytes and plasma cortisol, most prevalent in October. It was also found that an intense resource competition took place. Hansen and Damgaard (1991) found that juvenile females kept in groups had a higher plasma cortisol level than females kept singly. They also had a higher frequency of bite damages and a higher enzyme activity (ASAT and CK) all reflecting that they suffered from social stress. In a later study, it was found that group housed mink showed higher levels of bite damages to the pelt than pair housed mink (Hansen et al., 1998). de Jonge and van Iwaarden (1995) suggested in a Dutch popular article that family housing, equal to no weaning, would be an economically sound way to produce mink. They reported that the mother stayed healthy and there was no fighting among the family housed mink. Referring to this family system, de Jonge (1996) later stated in a technical report that “the frequency of damaged pelt is a matter of concern” and
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he found significantly more pelt damages in group housed mink compared to pair housed mink. For social husbandry animals such as cattle and pigs, group housing as opposed to solitary housing has been demonstrated to increase welfare (Boissy and Le Neindre, 1997; Bøe and Færevik, 2003), though problems arisen from competition for resources are also reported (Bøe and Færevik, 2003; Andersen et al., 2000). The fox is considered a solitary species in the wild, but possesses capabilities to lead a social life dependent on ecological resources or constraints (Hersteinsson and Macdonald, 1982, von Schantz, 1984). Hovland and Bakken (2000) reviewed group housing literature of farmed foxes. They found both positive (lower stereotypy levels, better physical condition, higher activity) and negative (fear of humans, higher cortisol levels, reduced growth, increased aggression, fights) in group housed foxes, though aggression were mostly related to the silver fox (Vulpes vulpes). Hovland and Bakken (2000) concluded in their review, that “in relation to the question of whether the welfare of group housed foxes is better than in singly housed foxes the answer is far from clear-cut and the results must be assessed in relation to the methodology applied in the respective studies”. Capabilities to lead a social life has never been documented in the wild mink and its solitary way of life in the wild cannot be questioned (Birks, 1986; Dunstone, 1993). Forcing a social life upon such a species, resource competition and social aggression might become so intense that it overshadows the positive consequences of social housing and instead impairs welfare. But on the other hand, group housing of juveniles might introduce some improvements of the mink’s environment: since cages have to be larger, more dynamics are present due both to pathways between cages and to cage mates, more nest boxes might be present and later weaning might be a possibility. Therefore, the aim of the present study was to compare behaviour and physiological parameters in traditional pair housed juvenile mink with two alternative group housing systems. The study was expected to reveal both benefits and drawbacks of all systems, leading to a conclusion on whether or not group housing, as examined in this study, improved welfare of farmed mink.
2. Materials and methods 2.1. Subjects The study was carried out on 335 mink from 72 litters selected from a pool of 100 litters according to birth dates (26 April–5 May) and litter sizes (4–10). Pastel (brown) and Pearl (light beige) colour types were used and equally distributed across systems. In each litter a focal animal, i.e. a female mink kit of a different colour type, was added when 2 days old to 2 days old foster litters. The kits were weaned when 8 weeks old and distributed to three different cage systems, equalising birth dates and litter sizes between systems. 2.2. Cage systems The stocking density in the traditional and stacked system (see below) was chosen as the maximal number of mink allowed according to present Danish and EU recommendations
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TRADITIONAL
ROW
STACKED 60 cm
PF
PF
PF
PF
PF
90 cm PW
PW
NB
NB
30 cm
PW
NB
PW
NB
PF
PW
90 cm
NB
90 cm 90 cm
Fig. 1. Illustration of the three different cage systems: TRADITIONAL = 1-room cage system, view from above; ROW = made of three connected traditional cages, view from above; STACKED = made of one traditional cage with a smaller cage (in length) stacked on top, view from the side. NB = nest box, PW = pathway, PF = platform. Dimensions of the traditional 1 room cage is 30 cm wide, 45 cm in height, and 90 cm in length.
under the European Convention (1999). These recommendations allow two mink per 2550 cm2 . For every additional added mink, space allowance should increase by 850 cm2 . The traditional system (T) comprised 24 standard mink cages (30 cm × 90 cm × 45 cm, w × d × h). A sibling pair (one male and one female juvenile mink) was housed in each of these cages and each pair had access to one wooden nest box (see Fig. 1). The row system (R) comprised 24 three-compartment cages made by making two pathways in the walls between three standard cages. Here the litter (4–10 animals) had access to the three compartments and three nest boxes at all times. The stacked system (S) was made by placing a cage (30 cm × 60 cm × 45 cm) on top of a standard mink cage and making a pathway to the “upper-floor”. These cages (24) each contained two male and three female (one focal) juvenile mink (from one litter, excess mink removed randomly) having access to one nest box in the bottom compartment. The T- and R-cages were equipped with a wire mesh platform on the back wall of each compartment (Fig. 1). The S-cages were equipped with two platforms: one in the bottom and one in the upper compartment also mounted on the backside. All nest boxes were equipped with a thick layer of straw on the roof that was renewed at least once a week or when else required. The mink were fed ad lib (wet feed from a professional feed kitchen) and drinking water was available at all times through drinking nipples in each compartment (one in T-system, three in R-system and one in S-system). 2.3. Behavioural observations Instantaneous scan sampling observations (Martin and Bateson, 1993) were conducted during the months of September–November at approximately 4–6 months of age. The scan samplings were conducted in three periods of 12 days with a week pause in between.
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During one period each cage system was exposed to scan sampling for 4 days, starting with a different system each day at random. During a scan sampling each “focal” animal was observed every 10th minute for 1.5 h. During observation of one focal animal, the observer stood still for 30 s in front of the preceding cage in the row system and the third preceding cage in the traditional and stacked system in order always to keep a distance of 1 m during samplings. This method allowed habituation to the observer and kept the level of disturbance by human presence minimal in all three systems. The observer noted the behaviour of the mink after additional 20 s, i.e. at the 50th second (sample point, Martin and Bateson, 1993). The observer used the next 10 s to write down observations and walk slowly and quietly on to carry out the next observation. The focal mink was categorised as performing a certain behaviour if this behaviour (see ethogram, Table 1) was observed at the 50th second or during the preceding 20 s. With regard to stereotypies, the mink was also scored as showing a stereotypy if it obviously had been disturbed by the human observer in performing this behaviour at the start of the habituation period and did not resume the behaviour during the next 50 s. The observations were carried out for 1.5 h starting 2 h and ending 0.5 h prior to feeding time (feeding during 11.30 a.m. and 12.30 p.m.). One hour after feeding, the observations were resumed and carried on for 3 h in the afternoon. Each focal animal was scanned 27 times during one day (nine times in the morning and 18 in the afternoon). In all, 7776 scanning observations were made in the traditional and row-cage system (24 cages × 27 scan samplings × 4 days × 3 periods). Since one of the focal animals in the stacked system died during the experiment only 23 cages are contained in the analysis and therefore 7236 scanning observations were made for this system (23 cages × 27 scan samplings × 4 days × 3 periods). At the scan samplings the behaviour (see ethogram, Table 1) of the “focal” animal was registered. Definitions used in the ethogram (Table 1) were based on studies of Bildsøe et al. (1990, 1991), and Hansen (1993) and own pilot studies. Also the focal animal’s position in the cage was noted and ascribed to the following categories: nest box (whole body inside the nest box), nest box entrance (forelimbs, head and neck outside the nest box), cage (on wire mesh bottom), and platform. For the R-group it was also noted which compartment the focal animal occupied during an observation (left = 1, middle = 2, right = 3) and the same for the S-group (bottom = B, upper = U). In addition it was noted if the focal animal was alone (distance between her and another mink >10 cm) or together with one or more individuals (distance between her and another mink <10 cm). 2.4. Physiological observations All focal animals were observed visually (no restrain or capture) in the cage in the end of October. Prior to this observation the observer had performed the same visual inspection a couple of times in August and September to “train the eye”. At the collection of data it was noted if the focal animal suffered from (1) superficial damages to the fur or (2) severe damages with bare parts or wounds at the (1) tail or (2) rest of the body. Furthermore the occurrence of mink with severe skin lesions needing isolation and treatment and the mortality rate in each of the systems were noted from weaning and on.
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Table 1 Ethogram with the behavioural categories used in the scan sampling observations and their description Category
Description
Exploration
The animal walks around in the cage system, sniffing and investigating the surroundings. Manipulating straw (carrying and placing) is included in this category The animal eats or drinks This category includes ego-play and social play. The animal is playing with straw in different ways (distinct from manipulating straw), playing with its own tail or with another animal or body parts of another animal. Includes play-stalking, chasing, wrestling and is characterised by soft or no vocalisation. Most often the movements are soft and slow The animal is standing or lying while looking around directing its head and eyes towards noises, movements and (possibly) odours, and observer The animal is cleaning its fur with the teeth or tongue or scratching itself with hind legs
Eating/drinking Playing
Being alert Auto-grooming Social behaviour Agonistic
Allo-grooming Being groomed Neck-biting Being neck-bitten Sleep/rest Stereotyping Platform Nipple Tunnel Chase Vertical Horizontal Pacing
Mix Other
Any behaviour intended to frighten or damage another individual and behavioural attempts to avoid/escape this. Aggressive elements occur with loud vocalisations such as screaming, making the opponent flee/attack and scream. Includes side wards attacks, defensive threats and submissive elements that do not occur in play. Includes own escape behaviour to a threat or attack The animal is grooming another animal with mouth, tongue or teeth in a gently manner The animal is groomed by another (see above) The animal holds or drags another with a firm grip in the back of the neck The animal is held or dragged by another animal by a firm grip to its back of the neck The animal is lying quietly with eyes closed The animal is repeatedly jumping up and down from the platform The animal circle its head repeatedly around the drinking nipple The animal repeatedly jumps up, through and down the tunnel, making circles The animal is repeatedly circling, chasing its own tail The animal repeatedly jumps up and down on the spot or stand still on the hind legs while the head and upper body repeatedly move up and down The animal repeatedly jumps back and forth with the head forelimbs and upper body, while the hind legs stands still. Usually along the back of the cage The animal repeatedly runs back and forth along the length of the cage with a turn inside or outside the nest box and for some individuals with a body roll at the turning point Any mixture of the above characterised stereotypies Defecating, urinating, body rubbing (rubbing anal region or cheeks toward or along the wire mesh wall or floor), scratching on the nest box walls while outside or inside it
2.5. Statistical analysis Behavioural data from the scan samplings were pooled for all three periods prior to analysis with a Mann–Whitney U-test (Martin and Bateson, 1993; Statistical Analysis System, 1985; Siegel and Castellan, 1988). Since levels of stereotypies were low and no differences between systems were found, data were for each type of stereotypy (see ethogram) pooled into one category. A Spearmann rank correlation on numbers of animals in the
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litter in the row system and parameters observed did not reveal any significant correlations (−0.08 < r2 < 0.06, 0.16 < P < 0.68). Therefore litter size in the row system is not further commented. Physical data were tested with a pair-wise t-test or GLM procedure in SAS for un-balanced data. Nominal data were tested with a χ2 - or Fisher exact test in SAS.
3. Results 3.1. Behaviour The frequencies of observed behavioural elements during scan samplings are shown in Table 2. No significant differences were observed in any of the categories between the traditionally kept focal animals and the row-kept focal animals. But the S-system deviated significantly from both the T- and R-system in a number of cases by showing a higher frequency of surveillance (P < 0.01), exploration (P < 0.01) and social behaviour (P < 0.05) and a lower frequency of sleeping (P < 0.05) and ingestion (P < 0.05). The frequency of stereotypies, self-grooming and play did not differ significantly in any of the comparisons (Table 2). Analysing the category “social behaviour” more detailed (Table 3), it was found that agonistic elements occurred significantly more in the S-system than in both the T- and R-system (P < 0.01), whereas neck-biting and being neck-bitten were seldom seen in the S-system. The R-system was also found to show more agonistic behaviour than the T-system (P < 0.01) and this system received also more neck-biting than the T-system (P < 0.005). Grooming or being groomed did not differ significantly between systems. Fig. 2 shows how the focal animals were positioned in the cage during the scan samplings. In the T-system they were observed more frequently in the nest box and less frequently in Table 2 Percentage of different behavioural elements observed during scan samplings of focal female mink kept traditionally, in a row-cage system, or a stacked cage system Behavioural categories Exploration Eating/drinking Play Alert Sleep/rest Ego-groom Social behaviour Stereotypies Other Total
Traditional N = 24 % 11.9 a 4.5 a 3.8 2.5 a 72.1 a 3.0 0.9 a 1.1 0.3 100.0
Row N = 24 % 11.8 a 4.4 a 4.1 3.3 a 72.2 a 2.8 0.9 a 0.4 0.4 100.0
Stacked N = 23 % 14.7 b 3.4 b 4.5 4.5 b 67.3 b 3.3 1.4 b 0.6 0.2 100.0
Total scan samplings in the traditional and row system = 7776 and in the stacked system = 7236. Statistics performed with a Mann–Whitney U-test two-sample. Different letters (a, b) indicate significant differences below a 5% level.
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Table 3 Percentages of different social behaviours observed during scan sampling of focal female mink housed traditionally, in a row system, or stacked cage system Social behaviour Agonistic Allo-grooming Being groomed Neck gripping Neck gripped Total
Traditional N = 24 % 1.4 a 47.1 34.3 15.7 a 1.4 a 100.0
Row N = 24 % 23.2 b 37.7 7.2 18.8 a 13.0 b 100.0
Stacked N = 23 % 52.5 c 26.3 20.2 0.0 b 1.0 a 100.0
Total of social behaviours sampled in the traditional system = 70, in the row system = 69 and in the stacked system = 90. Statistics performed with a Mann–Whitney U-test two-sample. Different letters (a–c) indicate significant difference below a 5% level.
the nest box entrance compared to both the R- and S-system focal animals (P < 0.0001). The S-system used the nest box the least and also significantly less than the R-system (P < 0.01). But the S-system used the platforms more frequently in stead (data joined for upper and lower platform, P < 0.0001). In the S-system the focal female mink was observed more frequently in the bottom cage (wire mesh + platform, 21%) than in the upper cage (wire mesh + platform, 15%, P < 0.01). In the R-system the focal female mink was observed more frequently in the left cage compared to the middle cage (P < 0.001), and there was a tendency (P = 0.09) to her being observed more in the right side than in the middle cage as well. No other significant differences were found regarding this parameter. Focal animals in the R-system were less often alone than the focal animal in the T-system (19.1 and 23.9%, respectively, P < 0.005). A tendency in the same direction was found between the R- and S-system (19.1 and 21.5%, respectively, P = 0.097), whereas no difference between the T- and S-system was found regarding this parameter.
Fig. 2. The choice of stay of focal female mink during scan sampling observations: on the wire mesh bottom, the platform, or in the nest box or the nest box entrance. The mink were kept either in a traditional cage system (TRA), in a row-cage system made by three connected traditional cages (ROW) or in a stacked cage system made by a traditional cage with a smaller cage placed on the top (STA).
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Table 4 Percentage of individuals with superficial or severe damages to the tail, damages at the hind part of the body or the fore part or neck region at a visual inspection of mink in October kept in three different systems from August Quality of damages
Traditional N = 48 %
Row N = 167 %
Stacked N = 120 %
Tail total Superficial Severe Hind parts Fore parts/neck Total with damages Removed/dead October Removed/dead November Total removed/dead
29 a 17 a 12 a 4 17 50 0 0 0a
42 b 20 a 23 b 4 9 55 4 7 11 b
50 b 3b 47 c 3 8 61 6 3 9b
Statistics performed with a χ2 -test, corrected for contingency. Different letters indicate significant differences below 5% level between systems in a paired comparison.
3.2. Physical observations During the visual inspection of fur damages in October, the R- and S-system scored the highest proportion of individuals with some kind of damages to the tail in comparison with the T-system (P < 0.05, Table 4). The S-system also had a significantly higher proportion of individuals with severe damages to the tail compared to both the T- and R-systems (P < 0.001). The R-system also showed significant more individuals with severe damages to the tail in comparison with the T-system (P < 0.001). On the rest of the body (hind part, fore part and neck), damages were limited in all systems and no other significant differences were found between systems. In October, 4 out of 167 animals in the R-system and 6 out of 120 animals in the S-system had either been removed due to severe damages or had been killed by cage mates (see Table 4). From October to November (4 weeks) an additional number of animals were removed or died in these two systems ending with a total of 11% in the R-system and 9% in the S-system.
4. Discussion Overall, the results indicate that group housing is not an obvious alternative to the traditional pair housing when welfare of the mink is the concern. Supposedly positive behaviours like activity levels, social play, and grooming were not increased in the group housing systems. These results are in concordance with other studies in which no significant differences in levels of play (de Jonge, 1996; Hansen et al., 1997), or grooming behaviour (de Jonge, 1996) were found between group and pair housed mink. In the present study, levels of stereotypies were low in all systems and not affected by the cage system. Juvenile mink would show low levels of stereotypies in the months of August–November with an increasing frequency during the winter months December–February (Hansen, 1993; Jeppesen et al., 1990). Regarding group housing studies no effect of housing system and stereotypy levels was found by de Jonge (1996), whereas Hansen et al. (1997) found increased stereotypy
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levels in singly kept mink and no differences between pair housed and family housed mink in stereotypy levels. Jeppesen et al. (1990) found the highest stereotypy levels in singly and group housed mink (three females), compared to pair housed mink. In the present study, group housing decreased the frequency of eating in the stacked system, decreased the use of the nest box in the row and stacked systems, increased agonistic behaviours in the row and stacked systems, and increased the incidence of pelt damages and bite marks on the leather side in the row and stacked systems compared to the traditional system. Increased agonistic behaviours were also found in family kept mink compared to pair housed mink in the study of Hansen et al. (1997). Pelt damages and bite marks on the leather side were also found to be higher in group housed mink compared to pair housed mink in the studies of Houbak and Hansen (1996), Hansen et al. (1998), de Jonge (1996), and Mononen et al. (2000). In that respect, it seems that welfare was reduced in the group housing systems, probably due to resource competition with a lot of fighting (inflicting pain) and deprivation from food and nest box as a consequence. The stocking density chosen in this study was the maximum allowed according to Council of Europe Recommendations (1999). Surely a reduction of stocking density might reveal another picture in both alternative systems. The stacked housing system had most problems. Here a more intense resource competition seems to have taken place since feeding and use of the nest box were observed less frequently and fighting and damages to the pelt were observed most frequently here. The presence of only one nest box and one feeding place to five individuals seemed to be too restrictive and addition of nest boxes and feeding places might reduce agonistic encounters. The row housing system did not deviate from traditional pair housing in most behaviours, but some social stress and competition was observed with levels (aggression, fur damages, tail damages, bite marks) intermediate to levels of the traditional housing and stacked housing systems. In the study of Mononen et al. (2000), it was concluded that growth of kits in family groups was not affected, and they found no differences between family and pair housed kits regarding serum cortisol levels, either. The mink might possess a flexibility as regards social organisation as suggested by Hansen and Damgaard (1991) also seen in the light that mink, in the present study, were observed to be alone only in 19.1–23.9% of the scan samplings. It might be possible to find a way to house mink in groups with more positive consequences than observed in the present study. However, including the mother in group housing is not a good idea (Pedersen and Jeppesen, 2001). Maybe the social flexibility of the mink is limited to just one or two partners, due to its solitary nature. And it seems somewhat a paradox, that we, with so much eagerness, try to group house a species that basically is solitary. For the sake of the mink’s welfare it might be more fruitful to focus on environmental enrichment and perhaps stocking density in the future.
5. Conclusion The two different group housing systems examined in the present study are not defendable from a welfare point of view. Severe fighting occurred with fatal consequences in up to 11% of the cases. Especially the stacked system showed that there was competition for
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resources such as a nest box and food. If group housing of mink gets widely adopted, despite these findings and the minks solitary nature, it is crucial that further research continues in order to find the appropriate stocking density, the optimal no. of feeding places and nest boxes, and optimal group composition for the sake of the welfare of each individual mink.
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Mononen, J., Kasanen, S., Harjunpää, S., Harri, M., Pyykönen, T., Ahola, L., 2000. A family housing experiment in mink. Scientifur 24 (4), 114–117. Pedersen, V., Jeppesen, L.L., 2001. Effects of family housing on behaviour plasma cortisol and performance in adult female mink (Mustela vison). Acta Agric. Scand. Sect. A: Animal Science 51, 77–88. Siegel, S., Castellan Jr., N.J., 1988. Nonparametric Statistics for the Behavioural Sciences, 2nd ed. McGraw-Hill. Statistical Analysis System, 1985. SAS Users Guide, Basics and Statistics, Version 5th ed. SAS Institute Inc., Cary, NC. von Schantz, T., 1984. Carnivore social behaviour-does it need patches. Nature 307, 388–390.
Effects of group housing systems on behaviour and production performance in farmed juvenile mink (Mustela vison) V. Pedersen∗ , L.L. Jeppesen, N. Jeppesen Department of Animal Behaviour, Biological Institute, University of Copenhagen, Tagensvej 16, Copenhagen N DK-2200, Denmark Received 7 July 2003; received in revised form 22 March 2004; accepted 22 March 2004
Abstract Juvenile mink were kept in two different group housing systems and their behaviour and physiology compared to that of juvenile mink kept traditionally in pairs. One group housing system was made by adjoining three traditional cages (row system) and the other by stacking a slightly smaller cage on top of a traditional cage (stacked system). Frequent scan sampling observations on behaviour and choice of stay were performed during 3 months on a focal female mink in each system. The occurrence and severity of damages to the fur was registered as well as morbidity and mortality in each system. The data showed that the frequency of stereotypies, auto-grooming and play did not differ significantly between systems. But the stacked system deviated significantly from both the traditional and row system in a number of occasions. There was a higher frequency of surveillance (P < 0.01), exploration (P < 0.01) and agonistic behaviour (P < 0.05) and a lower frequency of sleeping (P < 0.05) and eating/drinking (P < 0.05) in the stacked system. Morbidity and mortality was significantly higher in both group housing systems (9–11%), compared to the traditional system (0%). Group housing of juvenile mink, as practised in this experiment, could not be recommended from a welfare point of view. If group housing of mink, despite these findings, gets widely adopted, it is crucial that further research continues in order to find the appropriate stocking density, no. of feeding places and nest boxes, and optimal group composition acquired to obtain a good and acceptable welfare level in all individuals in the group. © 2004 Elsevier B.V. All rights reserved. Keywords: Mink; Groups; Social aggression; Stereotypies; Morbidity and mortality
∗
Corresponding author. Tel.: +45-35-32-13-04; fax: +45-35-32-12-99. E-mail address: [email protected] (V. Pedersen). 0168-1591/$ – see front matter © 2004 Elsevier B.V. All rights reserved. doi:10.1016/j.applanim.2004.03.003
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1. Introduction In the wild, mink is considered a solitary and highly territorial species (Birks, 1986; Dunstone, 1993). At mating time the male and female spend time together for a brief period but during pregnancy the female is alone in her territory. After parturition, during lactation, and for a few weeks more the female is together with her kits. Then the kits disperse to establish their own territories when 12–15 weeks of age (Birks, 1986; Dunstone, 1993). This natural way of living has to some extent been mimicked by man when keeping mink on farms. The male and female breeding stock is kept solitarily for most of the year. During the mating period the female is introduced to a male twice or thrice in his home cage. When mating has succeeded, the female continues to be housed solitarily during pregnancy. After parturition and nursing the kits for 6–7 weeks, the female is re-housed solitarily again. The litter stays together for a couple of weeks more and is then split into male/female pairs and housed as such for the remainder of the year. The breeding stock is selected in October and re-housed individually, whereas the surplus is killed. Keeping the juveniles as pairs during their growing period has been demonstrated to be better for their welfare than solitary housing: compared to pair housed juveniles, solitarily housed juveniles emitted more distress calls (Hansen et al., 1997), performed more stereotypies later in life (Jeppesen et al., 1990), and were more fearful towards humans and con-specifics (Hansen et al., 1997). In addition, their sexual development was inhibited leading to non-mating males and more barren females (Hansen et al., 1997) and their growth was inhibited (Møller, 1991). Juvenile mink also preferred to lie together rather than physically apart (Hansen et al., 1997). These studies all point in the direction that being housed with another mink is a positive social enrichment for juvenile mink. Studies of extended group housing in Denmark was initiated by the fact that the Dutch government implemented an Action plan of fur farming in 1996 (de Jonge, 1996), introducing group or family housing as the only acceptable way of keeping farmed mink in the Netherlands. At the time of this decision, only a limited amount of scientific evidence concerning the welfare consequences for mink in groups existed, and this evidence did not support the hypothesis of an improved welfare in group housed mink: as early as 1989, it was found that mink establish a social hierarchy when kept in groups (Houbak, 1989, 1990). This hierarchy was most persistent in males (being the most aggressive) with females being submissive to all males. No hierarchy between females was observed. The females and submissive males showed physiologically signs of stress reflected in high levels of eosinophil leucocytes and plasma cortisol, most prevalent in October. It was also found that an intense resource competition took place. Hansen and Damgaard (1991) found that juvenile females kept in groups had a higher plasma cortisol level than females kept singly. They also had a higher frequency of bite damages and a higher enzyme activity (ASAT and CK) all reflecting that they suffered from social stress. In a later study, it was found that group housed mink showed higher levels of bite damages to the pelt than pair housed mink (Hansen et al., 1998). de Jonge and van Iwaarden (1995) suggested in a Dutch popular article that family housing, equal to no weaning, would be an economically sound way to produce mink. They reported that the mother stayed healthy and there was no fighting among the family housed mink. Referring to this family system, de Jonge (1996) later stated in a technical report that “the frequency of damaged pelt is a matter of concern” and
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he found significantly more pelt damages in group housed mink compared to pair housed mink. For social husbandry animals such as cattle and pigs, group housing as opposed to solitary housing has been demonstrated to increase welfare (Boissy and Le Neindre, 1997; Bøe and Færevik, 2003), though problems arisen from competition for resources are also reported (Bøe and Færevik, 2003; Andersen et al., 2000). The fox is considered a solitary species in the wild, but possesses capabilities to lead a social life dependent on ecological resources or constraints (Hersteinsson and Macdonald, 1982, von Schantz, 1984). Hovland and Bakken (2000) reviewed group housing literature of farmed foxes. They found both positive (lower stereotypy levels, better physical condition, higher activity) and negative (fear of humans, higher cortisol levels, reduced growth, increased aggression, fights) in group housed foxes, though aggression were mostly related to the silver fox (Vulpes vulpes). Hovland and Bakken (2000) concluded in their review, that “in relation to the question of whether the welfare of group housed foxes is better than in singly housed foxes the answer is far from clear-cut and the results must be assessed in relation to the methodology applied in the respective studies”. Capabilities to lead a social life has never been documented in the wild mink and its solitary way of life in the wild cannot be questioned (Birks, 1986; Dunstone, 1993). Forcing a social life upon such a species, resource competition and social aggression might become so intense that it overshadows the positive consequences of social housing and instead impairs welfare. But on the other hand, group housing of juveniles might introduce some improvements of the mink’s environment: since cages have to be larger, more dynamics are present due both to pathways between cages and to cage mates, more nest boxes might be present and later weaning might be a possibility. Therefore, the aim of the present study was to compare behaviour and physiological parameters in traditional pair housed juvenile mink with two alternative group housing systems. The study was expected to reveal both benefits and drawbacks of all systems, leading to a conclusion on whether or not group housing, as examined in this study, improved welfare of farmed mink.
2. Materials and methods 2.1. Subjects The study was carried out on 335 mink from 72 litters selected from a pool of 100 litters according to birth dates (26 April–5 May) and litter sizes (4–10). Pastel (brown) and Pearl (light beige) colour types were used and equally distributed across systems. In each litter a focal animal, i.e. a female mink kit of a different colour type, was added when 2 days old to 2 days old foster litters. The kits were weaned when 8 weeks old and distributed to three different cage systems, equalising birth dates and litter sizes between systems. 2.2. Cage systems The stocking density in the traditional and stacked system (see below) was chosen as the maximal number of mink allowed according to present Danish and EU recommendations
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TRADITIONAL
ROW
STACKED 60 cm
PF
PF
PF
PF
PF
90 cm PW
PW
NB
NB
30 cm
PW
NB
PW
NB
PF
PW
90 cm
NB
90 cm 90 cm
Fig. 1. Illustration of the three different cage systems: TRADITIONAL = 1-room cage system, view from above; ROW = made of three connected traditional cages, view from above; STACKED = made of one traditional cage with a smaller cage (in length) stacked on top, view from the side. NB = nest box, PW = pathway, PF = platform. Dimensions of the traditional 1 room cage is 30 cm wide, 45 cm in height, and 90 cm in length.
under the European Convention (1999). These recommendations allow two mink per 2550 cm2 . For every additional added mink, space allowance should increase by 850 cm2 . The traditional system (T) comprised 24 standard mink cages (30 cm × 90 cm × 45 cm, w × d × h). A sibling pair (one male and one female juvenile mink) was housed in each of these cages and each pair had access to one wooden nest box (see Fig. 1). The row system (R) comprised 24 three-compartment cages made by making two pathways in the walls between three standard cages. Here the litter (4–10 animals) had access to the three compartments and three nest boxes at all times. The stacked system (S) was made by placing a cage (30 cm × 60 cm × 45 cm) on top of a standard mink cage and making a pathway to the “upper-floor”. These cages (24) each contained two male and three female (one focal) juvenile mink (from one litter, excess mink removed randomly) having access to one nest box in the bottom compartment. The T- and R-cages were equipped with a wire mesh platform on the back wall of each compartment (Fig. 1). The S-cages were equipped with two platforms: one in the bottom and one in the upper compartment also mounted on the backside. All nest boxes were equipped with a thick layer of straw on the roof that was renewed at least once a week or when else required. The mink were fed ad lib (wet feed from a professional feed kitchen) and drinking water was available at all times through drinking nipples in each compartment (one in T-system, three in R-system and one in S-system). 2.3. Behavioural observations Instantaneous scan sampling observations (Martin and Bateson, 1993) were conducted during the months of September–November at approximately 4–6 months of age. The scan samplings were conducted in three periods of 12 days with a week pause in between.
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During one period each cage system was exposed to scan sampling for 4 days, starting with a different system each day at random. During a scan sampling each “focal” animal was observed every 10th minute for 1.5 h. During observation of one focal animal, the observer stood still for 30 s in front of the preceding cage in the row system and the third preceding cage in the traditional and stacked system in order always to keep a distance of 1 m during samplings. This method allowed habituation to the observer and kept the level of disturbance by human presence minimal in all three systems. The observer noted the behaviour of the mink after additional 20 s, i.e. at the 50th second (sample point, Martin and Bateson, 1993). The observer used the next 10 s to write down observations and walk slowly and quietly on to carry out the next observation. The focal mink was categorised as performing a certain behaviour if this behaviour (see ethogram, Table 1) was observed at the 50th second or during the preceding 20 s. With regard to stereotypies, the mink was also scored as showing a stereotypy if it obviously had been disturbed by the human observer in performing this behaviour at the start of the habituation period and did not resume the behaviour during the next 50 s. The observations were carried out for 1.5 h starting 2 h and ending 0.5 h prior to feeding time (feeding during 11.30 a.m. and 12.30 p.m.). One hour after feeding, the observations were resumed and carried on for 3 h in the afternoon. Each focal animal was scanned 27 times during one day (nine times in the morning and 18 in the afternoon). In all, 7776 scanning observations were made in the traditional and row-cage system (24 cages × 27 scan samplings × 4 days × 3 periods). Since one of the focal animals in the stacked system died during the experiment only 23 cages are contained in the analysis and therefore 7236 scanning observations were made for this system (23 cages × 27 scan samplings × 4 days × 3 periods). At the scan samplings the behaviour (see ethogram, Table 1) of the “focal” animal was registered. Definitions used in the ethogram (Table 1) were based on studies of Bildsøe et al. (1990, 1991), and Hansen (1993) and own pilot studies. Also the focal animal’s position in the cage was noted and ascribed to the following categories: nest box (whole body inside the nest box), nest box entrance (forelimbs, head and neck outside the nest box), cage (on wire mesh bottom), and platform. For the R-group it was also noted which compartment the focal animal occupied during an observation (left = 1, middle = 2, right = 3) and the same for the S-group (bottom = B, upper = U). In addition it was noted if the focal animal was alone (distance between her and another mink >10 cm) or together with one or more individuals (distance between her and another mink <10 cm). 2.4. Physiological observations All focal animals were observed visually (no restrain or capture) in the cage in the end of October. Prior to this observation the observer had performed the same visual inspection a couple of times in August and September to “train the eye”. At the collection of data it was noted if the focal animal suffered from (1) superficial damages to the fur or (2) severe damages with bare parts or wounds at the (1) tail or (2) rest of the body. Furthermore the occurrence of mink with severe skin lesions needing isolation and treatment and the mortality rate in each of the systems were noted from weaning and on.
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Table 1 Ethogram with the behavioural categories used in the scan sampling observations and their description Category
Description
Exploration
The animal walks around in the cage system, sniffing and investigating the surroundings. Manipulating straw (carrying and placing) is included in this category The animal eats or drinks This category includes ego-play and social play. The animal is playing with straw in different ways (distinct from manipulating straw), playing with its own tail or with another animal or body parts of another animal. Includes play-stalking, chasing, wrestling and is characterised by soft or no vocalisation. Most often the movements are soft and slow The animal is standing or lying while looking around directing its head and eyes towards noises, movements and (possibly) odours, and observer The animal is cleaning its fur with the teeth or tongue or scratching itself with hind legs
Eating/drinking Playing
Being alert Auto-grooming Social behaviour Agonistic
Allo-grooming Being groomed Neck-biting Being neck-bitten Sleep/rest Stereotyping Platform Nipple Tunnel Chase Vertical Horizontal Pacing
Mix Other
Any behaviour intended to frighten or damage another individual and behavioural attempts to avoid/escape this. Aggressive elements occur with loud vocalisations such as screaming, making the opponent flee/attack and scream. Includes side wards attacks, defensive threats and submissive elements that do not occur in play. Includes own escape behaviour to a threat or attack The animal is grooming another animal with mouth, tongue or teeth in a gently manner The animal is groomed by another (see above) The animal holds or drags another with a firm grip in the back of the neck The animal is held or dragged by another animal by a firm grip to its back of the neck The animal is lying quietly with eyes closed The animal is repeatedly jumping up and down from the platform The animal circle its head repeatedly around the drinking nipple The animal repeatedly jumps up, through and down the tunnel, making circles The animal is repeatedly circling, chasing its own tail The animal repeatedly jumps up and down on the spot or stand still on the hind legs while the head and upper body repeatedly move up and down The animal repeatedly jumps back and forth with the head forelimbs and upper body, while the hind legs stands still. Usually along the back of the cage The animal repeatedly runs back and forth along the length of the cage with a turn inside or outside the nest box and for some individuals with a body roll at the turning point Any mixture of the above characterised stereotypies Defecating, urinating, body rubbing (rubbing anal region or cheeks toward or along the wire mesh wall or floor), scratching on the nest box walls while outside or inside it
2.5. Statistical analysis Behavioural data from the scan samplings were pooled for all three periods prior to analysis with a Mann–Whitney U-test (Martin and Bateson, 1993; Statistical Analysis System, 1985; Siegel and Castellan, 1988). Since levels of stereotypies were low and no differences between systems were found, data were for each type of stereotypy (see ethogram) pooled into one category. A Spearmann rank correlation on numbers of animals in the
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litter in the row system and parameters observed did not reveal any significant correlations (−0.08 < r2 < 0.06, 0.16 < P < 0.68). Therefore litter size in the row system is not further commented. Physical data were tested with a pair-wise t-test or GLM procedure in SAS for un-balanced data. Nominal data were tested with a χ2 - or Fisher exact test in SAS.
3. Results 3.1. Behaviour The frequencies of observed behavioural elements during scan samplings are shown in Table 2. No significant differences were observed in any of the categories between the traditionally kept focal animals and the row-kept focal animals. But the S-system deviated significantly from both the T- and R-system in a number of cases by showing a higher frequency of surveillance (P < 0.01), exploration (P < 0.01) and social behaviour (P < 0.05) and a lower frequency of sleeping (P < 0.05) and ingestion (P < 0.05). The frequency of stereotypies, self-grooming and play did not differ significantly in any of the comparisons (Table 2). Analysing the category “social behaviour” more detailed (Table 3), it was found that agonistic elements occurred significantly more in the S-system than in both the T- and R-system (P < 0.01), whereas neck-biting and being neck-bitten were seldom seen in the S-system. The R-system was also found to show more agonistic behaviour than the T-system (P < 0.01) and this system received also more neck-biting than the T-system (P < 0.005). Grooming or being groomed did not differ significantly between systems. Fig. 2 shows how the focal animals were positioned in the cage during the scan samplings. In the T-system they were observed more frequently in the nest box and less frequently in Table 2 Percentage of different behavioural elements observed during scan samplings of focal female mink kept traditionally, in a row-cage system, or a stacked cage system Behavioural categories Exploration Eating/drinking Play Alert Sleep/rest Ego-groom Social behaviour Stereotypies Other Total
Traditional N = 24 % 11.9 a 4.5 a 3.8 2.5 a 72.1 a 3.0 0.9 a 1.1 0.3 100.0
Row N = 24 % 11.8 a 4.4 a 4.1 3.3 a 72.2 a 2.8 0.9 a 0.4 0.4 100.0
Stacked N = 23 % 14.7 b 3.4 b 4.5 4.5 b 67.3 b 3.3 1.4 b 0.6 0.2 100.0
Total scan samplings in the traditional and row system = 7776 and in the stacked system = 7236. Statistics performed with a Mann–Whitney U-test two-sample. Different letters (a, b) indicate significant differences below a 5% level.
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Table 3 Percentages of different social behaviours observed during scan sampling of focal female mink housed traditionally, in a row system, or stacked cage system Social behaviour Agonistic Allo-grooming Being groomed Neck gripping Neck gripped Total
Traditional N = 24 % 1.4 a 47.1 34.3 15.7 a 1.4 a 100.0
Row N = 24 % 23.2 b 37.7 7.2 18.8 a 13.0 b 100.0
Stacked N = 23 % 52.5 c 26.3 20.2 0.0 b 1.0 a 100.0
Total of social behaviours sampled in the traditional system = 70, in the row system = 69 and in the stacked system = 90. Statistics performed with a Mann–Whitney U-test two-sample. Different letters (a–c) indicate significant difference below a 5% level.
the nest box entrance compared to both the R- and S-system focal animals (P < 0.0001). The S-system used the nest box the least and also significantly less than the R-system (P < 0.01). But the S-system used the platforms more frequently in stead (data joined for upper and lower platform, P < 0.0001). In the S-system the focal female mink was observed more frequently in the bottom cage (wire mesh + platform, 21%) than in the upper cage (wire mesh + platform, 15%, P < 0.01). In the R-system the focal female mink was observed more frequently in the left cage compared to the middle cage (P < 0.001), and there was a tendency (P = 0.09) to her being observed more in the right side than in the middle cage as well. No other significant differences were found regarding this parameter. Focal animals in the R-system were less often alone than the focal animal in the T-system (19.1 and 23.9%, respectively, P < 0.005). A tendency in the same direction was found between the R- and S-system (19.1 and 21.5%, respectively, P = 0.097), whereas no difference between the T- and S-system was found regarding this parameter.
Fig. 2. The choice of stay of focal female mink during scan sampling observations: on the wire mesh bottom, the platform, or in the nest box or the nest box entrance. The mink were kept either in a traditional cage system (TRA), in a row-cage system made by three connected traditional cages (ROW) or in a stacked cage system made by a traditional cage with a smaller cage placed on the top (STA).
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Table 4 Percentage of individuals with superficial or severe damages to the tail, damages at the hind part of the body or the fore part or neck region at a visual inspection of mink in October kept in three different systems from August Quality of damages
Traditional N = 48 %
Row N = 167 %
Stacked N = 120 %
Tail total Superficial Severe Hind parts Fore parts/neck Total with damages Removed/dead October Removed/dead November Total removed/dead
29 a 17 a 12 a 4 17 50 0 0 0a
42 b 20 a 23 b 4 9 55 4 7 11 b
50 b 3b 47 c 3 8 61 6 3 9b
Statistics performed with a χ2 -test, corrected for contingency. Different letters indicate significant differences below 5% level between systems in a paired comparison.
3.2. Physical observations During the visual inspection of fur damages in October, the R- and S-system scored the highest proportion of individuals with some kind of damages to the tail in comparison with the T-system (P < 0.05, Table 4). The S-system also had a significantly higher proportion of individuals with severe damages to the tail compared to both the T- and R-systems (P < 0.001). The R-system also showed significant more individuals with severe damages to the tail in comparison with the T-system (P < 0.001). On the rest of the body (hind part, fore part and neck), damages were limited in all systems and no other significant differences were found between systems. In October, 4 out of 167 animals in the R-system and 6 out of 120 animals in the S-system had either been removed due to severe damages or had been killed by cage mates (see Table 4). From October to November (4 weeks) an additional number of animals were removed or died in these two systems ending with a total of 11% in the R-system and 9% in the S-system.
4. Discussion Overall, the results indicate that group housing is not an obvious alternative to the traditional pair housing when welfare of the mink is the concern. Supposedly positive behaviours like activity levels, social play, and grooming were not increased in the group housing systems. These results are in concordance with other studies in which no significant differences in levels of play (de Jonge, 1996; Hansen et al., 1997), or grooming behaviour (de Jonge, 1996) were found between group and pair housed mink. In the present study, levels of stereotypies were low in all systems and not affected by the cage system. Juvenile mink would show low levels of stereotypies in the months of August–November with an increasing frequency during the winter months December–February (Hansen, 1993; Jeppesen et al., 1990). Regarding group housing studies no effect of housing system and stereotypy levels was found by de Jonge (1996), whereas Hansen et al. (1997) found increased stereotypy
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levels in singly kept mink and no differences between pair housed and family housed mink in stereotypy levels. Jeppesen et al. (1990) found the highest stereotypy levels in singly and group housed mink (three females), compared to pair housed mink. In the present study, group housing decreased the frequency of eating in the stacked system, decreased the use of the nest box in the row and stacked systems, increased agonistic behaviours in the row and stacked systems, and increased the incidence of pelt damages and bite marks on the leather side in the row and stacked systems compared to the traditional system. Increased agonistic behaviours were also found in family kept mink compared to pair housed mink in the study of Hansen et al. (1997). Pelt damages and bite marks on the leather side were also found to be higher in group housed mink compared to pair housed mink in the studies of Houbak and Hansen (1996), Hansen et al. (1998), de Jonge (1996), and Mononen et al. (2000). In that respect, it seems that welfare was reduced in the group housing systems, probably due to resource competition with a lot of fighting (inflicting pain) and deprivation from food and nest box as a consequence. The stocking density chosen in this study was the maximum allowed according to Council of Europe Recommendations (1999). Surely a reduction of stocking density might reveal another picture in both alternative systems. The stacked housing system had most problems. Here a more intense resource competition seems to have taken place since feeding and use of the nest box were observed less frequently and fighting and damages to the pelt were observed most frequently here. The presence of only one nest box and one feeding place to five individuals seemed to be too restrictive and addition of nest boxes and feeding places might reduce agonistic encounters. The row housing system did not deviate from traditional pair housing in most behaviours, but some social stress and competition was observed with levels (aggression, fur damages, tail damages, bite marks) intermediate to levels of the traditional housing and stacked housing systems. In the study of Mononen et al. (2000), it was concluded that growth of kits in family groups was not affected, and they found no differences between family and pair housed kits regarding serum cortisol levels, either. The mink might possess a flexibility as regards social organisation as suggested by Hansen and Damgaard (1991) also seen in the light that mink, in the present study, were observed to be alone only in 19.1–23.9% of the scan samplings. It might be possible to find a way to house mink in groups with more positive consequences than observed in the present study. However, including the mother in group housing is not a good idea (Pedersen and Jeppesen, 2001). Maybe the social flexibility of the mink is limited to just one or two partners, due to its solitary nature. And it seems somewhat a paradox, that we, with so much eagerness, try to group house a species that basically is solitary. For the sake of the mink’s welfare it might be more fruitful to focus on environmental enrichment and perhaps stocking density in the future.
5. Conclusion The two different group housing systems examined in the present study are not defendable from a welfare point of view. Severe fighting occurred with fatal consequences in up to 11% of the cases. Especially the stacked system showed that there was competition for
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resources such as a nest box and food. If group housing of mink gets widely adopted, despite these findings and the minks solitary nature, it is crucial that further research continues in order to find the appropriate stocking density, the optimal no. of feeding places and nest boxes, and optimal group composition for the sake of the welfare of each individual mink.
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