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Rabbit preference for cages and pens with or without mirrors
Applied Animal Behaviour Science 116 (2009) 273–278
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Applied Animal Behaviour Science journal homepage: www.elsevier.com/locate/applanim
Rabbit preference for cages and pens with or without mirrors Antonella Dalle Zotte a,*, Zolta´n Princz b, Zsolt Matics c, Zsolt Gerencse´r b, Szilvia Metzger b, Zsolt Szendro˝ b a
Department of Animal Science, Padova University, Agripolis, Viale dell’Universita` 16, 35020 Legnaro (PD), Italy Faculty of Animal Science, Kaposva´r University, 7401 Kaposva´r, P.O. Box 16, Hungary c MTA - KE Research Group of Animal Breeding and Hygiene, Kaposva´r University, Hungary b
A R T I C L E I N F O
A B S T R A C T
Article history: Accepted 12 August 2008 Available online 23 September 2008
Five-week-old Pannon White rabbits were housed in a closed climatized rabbitry and randomly assigned to either pens (56 rabbits) having a basic area of 1 m2 with a stocking density of 16 and 12 rabbits/m2 or to 18 individual cages (0.24 m2/cage). The pens and the cages were divided into two halves and animals could move freely between the two halves through swing doors. The walls of one half of the pens and cages were completely covered with mirrors while the other half was covered with white plastic panels. A 24 h video recording was made twice a week using infrared cameras and the number of rabbits in each pen and cage was counted every 15 min. The duration of the trial was 6 weeks. The lighting period was 16L/8D. In each half of the cage or pen, a feeder and nipple drinkers were available and feed intake was measured separately. Throughout the entire rearing period, 72% of the individually caged rabbits showed a preference for the cage half enriched with mirrors (P < 0.001). This preference decreased slightly with increasing age. Preference toward the cage half provided with mirror walls was independent of the time of day; in other words, during the active period (23:00–05:00) corresponding to the dark part of the day, rabbits continued to prefer the mirrored half even if the vision of the reflected image was reduced. The presence of conspecifics at different stocking densities (12 vs. 16 rabbits/m2) did not reduce this interest in mirrors: averaging the ages, 66% of animals living at 16 rabbits/m2 stocking density and 63% of those living at 12 rabbits/m2 density were found in the half pen with mirrors (P < 0.001). Group-penned rabbits showed a marked preference toward mirrors during the active period (73–76% for 12 and 16 rabbits/ m2 stocking densities, respectively; P < 0.001). The results suggest that the presence of mirrors offers advantages perhaps related to comfort and welfare, and therefore might be used as environmental enrichment for fattening rabbits and advised for rabbits caged individually for long periods. ß 2008 Elsevier B.V. All rights reserved.
Keywords: Growing rabbits Preference test Mirrors Individually caged Group-penned
1. Introduction The current intensive rabbit breeding system for meat production holds small groups of animals in wire cages that might be considered barren environments. In Italy and Hungary, rabbits are most often caged in pairs for the best
* Corresponding author. Tel.: +39 0498272640. E-mail address: [email protected] (A. Dalle Zotte). 0168-1591/$ – see front matter ß 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.applanim.2008.08.011
expression of live performance, decreased ear lesions and other aggressive behaviour (Maertens and Van Herck, 2000; Princz et al., 2005; Princz et al., 2008b), lower mortality rates (Dal Bosco et al., 2002), and higher carcass yield (Dal Bosco et al., 2002; Dalle Zotte et al., 2008) compared to larger group-housed rabbits. On the other hand, rabbits kept as laboratory animals in social isolation can display physiological symptoms of stress, i.e. stereotypic behaviours such as cage chewing and bar biting which are relieved by the presence of conspecifics (Held
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et al., 1995; Chu et al., 2004). These stereotypic behaviours are much less frequent in pair-caged rabbits reared for meat production (Mirabito et al., 1999; Dal Bosco et al., 2002; Princz et al., 2008b). One of the main objections to caged rabbit housing is the barren environment. Several forms of enrichment have been studied (e.g., plastic platform, hiding box, gnawing stick) to alleviate this problem and specifically in regard to productive performance and the behaviour and welfare of growing rabbits (Maertens et al., 2004; Luzi et al., 2005; Princz et al., 2008a). Mirrors have also been shown to temporarily enrich the environment of some animals kept in partial isolation (conspecifics can be viewed by the isolated animal but social contact is not permitted) (Parrott et al., 1988; McAfee et al., 2002; Mills and Davenport, 2002). The effect of mirrors has been evaluated in several behavioural and welfare studies. Mirror self recognition (MSR) has been thoroughly studied in human and nonhuman primates. MSR was proven in chimpanzees (Gallup, 1970; Suarez and Gallup, 1981; Povinelli et al., 1997; Schilhab, 2004), bonobos (De Veer and Van den Bos, 1999), orangutans (Suarez and Gallup, 1981), dolphins (Delfour and Marten, 2001) and elephants (Plotnik et al., 2006). Birds have different attitudes to mirrors. Fighting cocks show aggressive behaviour towards a mirror (Thompson, 1964). Mirror image has led to increased mirror pecking and wing flapping, which are typical aggressive behaviour in jungle crows (Kusayama et al., 2000). Pigeons showed induced attack against mirror (Cohen and Looney, 1973). In both cases, the mirror image represents an image of a conspecific. Contrary to these results, Java sparrows showed strong preference for a self-image in the mirror (Watanabe, 2002). Grey parrots engaged in mirror-image stimulation, mirror-mediated object discrimination, and mirror-mediated spatial location (Pepperger et al., 1995). Sometimes it is necessary to house animals individually; housing gregarious species as individuals might have a negative effect on welfare, however. This is why environmental enrichment is recommended. Mirrors have been provided routinely for caged pet birds. Sherwin (2004) investigated the potential of mirrors in improving the welfare of mice. Mirrors slightly reduced occupation levels in the cage with a mirror and considerably decreased the amount of feeding from the feeder next to the mirror. It seems that mice were fearful of the mirror (or perhaps they thought that the image represented a conspecific competing for the food). Stabled horses are usually allowed limited social contact, and this restriction can cause frustration. Weaving is a form of locomotor stereotypic behaviour. The provision of a mirror might mimic visual contact and therefore help reduce social isolation in the stable (Mills and Davenport, 2002; McAfee et al., 2002). Parrott et al. (1988) compared individually housed sheep in isolation pens in small huts with or without mirrors in them. Isolated sheep showed considerable interest in the mirror, and stress responses were lower in the group with the mirror. Later, Parrott (1990) established that the response to isolation can be partially reduced
when sheep are provided with a mirror, indicating that the sight of other sheep or their image may have stressreducing properties. Piller et al. (1999) examined whether exposure to a mirror reduces the stress of social isolation of heifers confined to single-animal weigh scales. Lower heart rates and decreased movement would seem to indicate that mirror exposure reduces stress more than side view placement. The objectives of this study were to examine how mirrors could influence the rabbits’ free choice towards the half of the cage or pen provided with mirrors on their walls rather than the other half of the cage or pen with plastic panels either when raised singly in total isolation or in groups. We also attempted to investigate rabbit preference towards the mirrored half by age, part of the day considered, and two stocking densities because all these factors are believed capable of modifying rabbit choice. 2. Materials and methods Seventy-four 5-week-old Pannon White rabbits – selected at random from both sexes and from different litters – were housed in a closed climatized rabbitry (room) in Kaposva´r University (Hungary). The lighting period was 16L/8D (lights on: 6:00–22:00) and the temperature of the rabbitry was kept constant at 18 8C. The rabbits were fed a commercial pelleted diet ad libitum and water was available on demand from nipple drinkers. Eighteen rabbits were caged individually (cage size: 0.24 m2) while 56 rabbits were housed in pens with a basic area of 1 m2 and a stocking density of 16 rabbits/m2 (2 pens) or 12 rabbits/m2 (2 pens). Each cage and pen was made of wire net with net floor and divided into two halves. The walls of one half of the cages and pens were covered with mirrors while those of the other half were covered with white plastic panels and placed alternatively in order to avoid disturbing position effects (Figs. 1 and 2). The panels were odourless with flat surface. Cages and pens were ventilated through their wire net parts (top and floor); bedding was not furnished. In each half of the cage and pen, a feeder and two nipple drinkers were available. Animals could move freely between the two halves of cage or pen through swing doors. The individually caged rabbits were totally isolated from conspecifics by these vertical mirrors and plastic panels. The duration of the trial was of 6 weeks (from 5 weeks – weaning – to 11 weeks of age), which corresponds to the standard fattening period of commercial rabbits reared for meat production. The feed intake of nine individual cages and all pens was measured weekly by weighing separately the two feeders on the mirror and plastic halves, and was expressed as a percentage of the total weekly intake in each half. A 24 h video recording using infrared cameras was made twice a week. On these recording days, no one entered the room and the animals were controlled through a large window covered with a light-isolating curtain. During non-recording days, rabbits were scarcely distracted by humans during environmental and animal controls and feeding that lasted only a few minutes each day, and mirrors or plastic panels reduced rabbit visibility even further. Using the recordings, the number of rabbits in each half of the cage and pen was counted with a frequency of 15 min. Only the 6–6 middle hours of light (from 11:00 to 17:00, corresponding to the most resting period) and dark (from 23:00 to 5:00, corresponding to the most active period) were taken into consideration.
Fig. 1. Design of the cage.
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Table 1 Preference of individually caged growing rabbits for cages with or without mirrors depending on age (%) Age (weeks)
Mirrors b
Plastic panels a
S.E.
Prob.
5.5 6.5 7.5 8.5 9.5 10.5 S.E. Prob.
79.0 67.6 a 69.7 a 68.5 a 72.1b 72.0 b 0.66 <0.001
21.0 32.4 b 30.3b 31.5b 27.9 a 28.0 a 0.66 <0.001
2.37 1.43 1.43 1.43 1.43 1.43
<0.001 <0.001 <0.001 <0.001 <0.001 <0.001
5.5–10.5
71.5
28.5
0.66
<0.001
Means in a column with different superscripts (a and b) were significantly different (P < 0.05).
Fig. 2. Design of the pens.
2.1. Statistical analysis Preference data for the two half sections (mirror vs. plastic panel) in terms of percentages of rabbit occupancy and feed intake were analysed separately for individually caged and group-penned rabbits. Grouppenned rabbit data were also analysed separately for the two stocking densities (12 vs. 16/m2). The linear model of ANOVA adopted included the effect of the type of wall (mirror vs. plastic panels), age (5–11 weeks), part of the day (active vs. resting period), and their interaction. Variance analysis was performed using the GLM procedure of the SAS program (SAS Institute, 1990).
3. Results and discussion 3.1. Individually caged rabbits Throughout the entire rearing period, 72% of the individually caged rabbits showed a preference for the cage half enriched with mirrors, although this preference decreased significantly from 79.0% to 67.6% between ages of 5.5 and 6.5 weeks and increased to 72.0% up to the week 10.5 (Table 1). The results permit the hypothesis that isolated rabbits are attracted to reflected images of themselves, at least until 11 weeks of age, and that mirror images might serve them as ‘‘companions’’, as has already been adopted for other social farm animals, such as horses (Mills and Davenport, 2002; McAfee et al., 2002), sheep (Parrott et al., 1988) and cattle (Piller et al., 1999). Great apes (Gallup, 1970), dolphins (Reiss and Marino, 2001), chimpanzees (Suarez and Gallup, 1981), bonobos (Povinelli et al., 1997), orangutans (De Veer and Van den Bos, 1999), dolphins and other marine mammals (Delfour and Marten, 2001) have been proven capable of selfrecognition in mirrors. It is generally believed that
primates and dolphins have greater cognitive powers than rabbits, and therefore according to literature (Jones and Phillips, 2005), rabbits are unlikely to prove capable of selfrecognition. Rabbits might interpret the image in the mirror as a conspecific (familiar or unfamiliar), however. Jones and Phillips (2005), in fact, found that individually caged adult rabbits with or without the possibility to see a conspecific in the adjacent cage were initially attracted to the mirror and spent more time sniffing and scrabbling at it, apparently in an attempt to reach the image. Over a 1week period, this increased sniffing of vertical boundaries indicated the mirror as a more interesting stimulus to the rabbits than a conspecific, presumably because a relationship with the conspecific had been established and confirmed the rabbit’s expectations, whereas the image in the mirror failed to exhibit the expected behaviour. Jones and Phillips (2005) also observed that the presence of a mirror decreased the frequency of ‘‘looking out of the cage’’ behaviour, indicating that a mirror may make the cage a more stimulating environment. The preference of the individually housed rabbits for the cage half provided with mirror walls was independent of the time of day (Table 2). During the active period, 71.5% of the rabbits were found in the mirrored half, even if this active period corresponds to the dark phase. Most likely, the rabbits memorised the part of the cage that gave them the best social perception of presence of conspecifics, and they found it in the dark navigating primarily by smell helped by tactile signals (whiskers). The rabbits probably associated that section with the presence of conspecifics and recognized it by following odour marks. Moreover, given that the rabbit can see in the dark to some degree by the presence of tapetum lucidum – a remarkable example of
Table 2 Preference of individually caged growing rabbits for cages with or without mirrors depending on part of day (%) Part of the day (h)
Mirrors
Plastic panels
S.E.
Prob.
23:00–05:00a 11:00–17:00b S.E. Prob.
71.5 71.5 0.66 0.958
28.5 28.5 0.66 0.958
0.93 0.88
<0.001 <0.001
a b
Active period. Resting period.
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Table 3 Feed intake proportion (%) of individually caged growing rabbits depending on wall type and age Age (weeks)
Mirrors
Plastic panels
S.E.
Prob.
5–6 6–7 7–8 8–9 9–10 10–11 S.E. Prob.
70.3 69.5 68.9 69.6 67.3 67.0 2.24 0.99
29.7 30.5 31.1 30.4 32.7 33.0 2.24 0.99
5.49 5.49 5.49 5.49 5.49 5.49
<0.001 <0.001 <0.001 <0.001 <0.001 <0.001
5–11
68.8
31.2
2.24
<0.001
Feed intake was recorded in nine cages.
neural cell and tissue specialization as an adaptation to a dim light environment – (Ollivier et al., 2004) and because the experimental room adopted was not completely dark, recognition was probably aided by the partial sight of reflected rabbits in the mirror (the dim light of the videocamera LED and the white coloured room walls might have been sufficient for the rabbits to perceive their reflection). Our findings are supported by the observation of Sherwin (2004) on mice: the same behaviour observed during the illuminated phase (avoidance of feeding from the feeder next to the mirror) was noticed during the dark phase as well. The feed intake proportion of the individually caged rabbits was significantly higher in the cage half with mirrors (69% of the total feed intake) regardless of the
rabbit’s age (Table 3), indicating that when the rabbits stayed in the mirrored half of the cage they also fed there. This feeding behaviour could represent a positive sign of welfare diametrically opposed to the negative effect that mirrors appeared to have on mouse feeding habits (Sherwin, 2004). The results of our study seem to show that mirrorimage stimulation could be a partial conspecific substitute for prepubertal individually housed rabbits, as observed by Parrott et al. (1988) in sheep. Further study could quantify how important mirrors are to individual- and group-reared young rabbits by using economic demand theory, e.g. attaching weights to the push door, as recently assessed by Seaman et al. (2008) in individually caged adult female rabbits, in order to test their motivation to reach a platform, social contact, or food. 3.2. Group-penned rabbits Rabbits housed in pens with different stocking densities (16 vs. 12 rabbits/m2) showed a clear preference for the part of the pen enriched with mirrors by all age groups considered (Table 4). Averaging the ages, 66% of the rabbits living at 16/m2 rabbit density and 63% of those living at 12 rabbit/m2 density were found on the side with mirrors (P < 0.001). Preference for the mirrored half was highest at 5.5 weeks of age (about 87%) but significantly decreased (P < 0.001) with age to 55.8 and 52.8% at 16 and 12 rabbit/ m2 density, respectively. This result was unexpected because the presence of conspecifics should have theoretically reduced interest in
Table 4 Preference of group-penned growing rabbits for pens with or without mirrors depending on age and stocking density (%) Age (weeks)
Stocking density 16 rabbits/m2
12 rabbits/m2
Mirrors
Plastic panels
S.E.
Prob.
Mirrors
Plastic panels
S.E.
Prob.
5.5 6.5 7.5 8.5 9.5 10.5 S.E. Prob.
87.0 d 71.5 c 62.0 b 62.3 b 58.9 b 55.8 a 0.40 <0.001
13.0 a 28.5 b 38.0 c 37.7c 41.1c 44.2 d 0.40 <0.001
1.29 0.91 0.91 0.91 0.91 0.91
<0.001 <0.001 <0.001 <0.001 <0.001 <0.001
86.7d 70.7 c 59.3 b 58.9 b 50.5 a 52.8 a 0.43 <0.001
13.3 a 29.3b 40.7c 41.1c 49.5 d 47.2d 0.43 <0.001
1.38 0.97 0.97 0.97 1.00 0.97
<0.001 <0.001 <0.001 <0.001 1.000 0.004
5.5–10.5
66.2
33.8
0.40
<0.001
63.1
36.9
0.43
<0.001
Means in a column with different superscripts (a, b, c and d) were significantly different (P < 0.05).
Table 5 Preference of group-penned growing rabbits for pens with or without mirrors depending on part of day and stocking density (%) Part of day (h)
Stocking density 16 rabbits/m2
23:00–05:00a 11:00–17:00b S.E. Prob. a b
Active period. Resting period.
12 rabbits/m2
Mirrors
Plastic panels
S.E.
Prob.
Mirrors
Plastic panels
S.E.
Prob.
75.9 56.6 0.40 <0.001
24.1 43.4 0.40 <0.001
0.56 0.56
<0.001 <0.001
73.0 53.2 0.43 <0.001
27.0 46.8 0.43 <0.001
0.60 0.60
<0.001 <0.001
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Table 6 Feed intake proportion (%) of group-penned growing rabbits depending on wall type, age, and stocking density Age (weeks)
Stocking density 16 rabbits/m2
12 rabbits/m2
Mirrors
Plastic panels
S.E.
Prob.
Mirrors
Plastic panels
S.E.
Prob.
5–6 6–7 7–8 8–9 9–10 10–11 S.E. Prob.
70.3 57.6 57.5 60.2 55.2 57.6 1.36 0.134
29.7 42.4 42.5 39.8 44.8 42.4 1.36 0.134
3.33 3.33 3.33 3.33 3.33 3.33
<0.001 0.473 0.509 0.065 1.000 0.478
67.2 bc 62.4b 53.6 ab 54.8 ab 49.0 a 51.1ab 0.73 0.002
32.8 a 37.6 ab 46.4 bc 45.2 bc 51.0c 48.9bc 0.73 0.002
1.80 1.80 1.80 1.80 1.80 1.80
<0.001 <0.001 0.953 0.189 1.000 1.000
5–11
59.7
40.3
1.36
<0.001
56.4
43.6
0.74
<0.001
Means in a column with different superscripts (a, b and c) were significantly different (P < 0.05).
this form of enrichment. The highest preference for the mirrored part of the pen in most animals from 5.5 to 8.5 weeks of age confirms that young rabbits like to congregate and huddle together (Matics et al., 2004) and the perception of being present in greater number than in reality does not appear stressful for them. Contrary to the behaviour observed in individually caged rabbits, group-penned rabbits showed a greater preference for mirrors during the active (dark) period (P < 0.001), and although such preference remained statistically significant (P < 0.001; Table 5) during the resting (light) period (11:00–17:00), it was of lower magnitude. This appears to be in contrast with the behaviour observed in wild rabbits, which huddle together during the resting period but disperse around the rabbit hole to feed during the active period (Williams et al., 1995). The question arises whether rabbits in mirrored pens consider the reflected images only as other rabbits or whether they feel the cage is larger as well. As age increased, group-housed rabbits spent less time in the mirrored pen half. Matics et al. (2004) observed that although young rabbits like to huddle together in a little cage, after 6–7 weeks of age, more and more rabbits prefer to occupy larger cages that meet their need for more space. Our study indicated the opposite tendency: fewer and fewer rabbits preferred the seemingly larger mirrored half while more and more stayed in the pen without mirrors as age increased. This might mean either that the ‘‘enlarging effect’’ of mirrors has less effect on rabbit choice or that the apparently double group size generated by mirror reflections causes a feeling of crowding in older rabbits close to age of dispersal. In this study, all four sides of the cage and pen half were covered with mirrors, and the feeling of overcrowding generated by the multiple reflection probably began disturbing the older rabbits. It derives that mirrors on only one side of the cage and pen could be enough to provide some advantage to the welfare of reared rabbits. The average feed intake proportion of group-penned rabbits was to the favour of the half of the pen provided with mirrors in both 16 (59.7%) and 12 rabbits/m2 (56.4%) stocking densities (P < 0.001; Table 6). This preference for feeding in the mirrored half was statistically different in the first week of age in 16 rabbits/m2 stocking density and
in the first 2 weeks of age in 12 rabbits/m2 stocking density. This behaviour might be due to the constantly diminishing space available caused by rabbit growth around the feeder in the mirrored half, and this could have encouraged some of the rabbits to feed at the other feeder. 3.3. Conclusion This study has brought us to several conclusions. The application of mirrors in one half of the cage or pen affected rabbit preference. Both isolated and grouped-living rabbits preferred to stay and eat in the cage/pen half covered with mirrors. Although this high preference towards the mirrored half did not change with age in isolated-living rabbits, it decreased significantly with age in grouppenned rabbits, probably due to the less and less livingspace in the mirrored half as the rabbits grew. Both isolated and group-penned rabbits significantly preferred the mirrored half also during the dark phase, and this could have depended on the fact that the rabbit positively associated the area with the presence of conspecifics and recognized it by their senses. Further research is needed to evaluate rabbit behaviour and investigate the reasons behind their preference for mirrored walls in greater depth. The results suggest that the presence of mirrors offers some advantages, perhaps related to comfort and welfare, and that they could be used as environmental enrichment for fattening rabbits and advised for rabbits caged individually for long periods, such as those reared as laboratory or exhibition animals. Acknowledgements Research supported by the Italian-Hungarian Intergovernmental (Ministry of Foreign Affairs) Science and Technology cooperation programme (OMFB-00607/2005). The authors wish to thank Dr. Barbara Contiero of the Department of Animal Science (University of Padova, Italy) for helping with statistical analysis, Prof. Bruno Cozzi of the Department of Experimental Veterinary Science (University of Padova, Italy) for valuable discussion while the manuscript was in preparation, and two anonymous referees for comment on the manuscript.
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Ollivier, F.J., Samuelson, D.A., Brooks, D.E., Lewis, P.A., Kallherg, M.E., Koma´romy, A.M., 2004. Comparative morphology of the tapetum lucidum (among selected species). Vet. Ophthalmol. 7 (1), 11–22. Parrott, R.F., 1990. Social Stress in Domestic Animals. Kluwer Academic Publishers, Dordrecht, Netherlands, pp. 212–226. Parrott, R.F., Houpt, K.A., Misson, B.H., 1988. Modification of the responses of sheep to isolation stress by the use of mirror panels. Appl. Anim. Behav. Sci. 19 (3–4), 331–338. Pepperger, I.M., Garcia, S.E., Jackson, E.C., Marconi, S., 1995. Mirror use by African Grey parrot (Psittacus erithacus). J. Comp. Phycho. 109 (2), 182–195. Piller, C.A.K., Stookey, J.M., Watts, J.M., 1999. Effect of mirror-image exposure on heart rate and movement of isolated heifers. Appl. Anim. Behav. Sci. 63, 93–102. Plotnik, J.M., de Waal, F.B.M., Reiss, D., 2006. Self-recognition in an Asian elephant. PNAS 103 (45), 17053–17057., www.phas.org/cgi/doi/ 10.1073/pnas0608062103. Povinelli, D.J., Gallup, G.G., Eddy, T.J., Biershwale, D.T., Engstrom, M.C., Perilloux, H.K., Toxopeus, I.D., 1997. Chimpanzees recognize themselves in mirrors. Anim. Behav. 53, 1083–1088. Princz, Z., Dalle Zotte, A., Metzger, Sz., Radnai, I., Biro´-Ne´meth, E., Orova, Z., Szendro˝ , Zs., 2008a. Response of fattening rabbits reared under different housing conditions. 1. Live performance and health status. Livest. Sci., doi:10.1016/j.livsci.2008.05.018. Princz, Z., Dalle Zotte, A., Radnai, I., Biro´-Ne´meth, E., Matics, Zs., Gerencse´r, Zs., Nagy, I., Szendro˝ , Zs., 2008b. Behaviour of growing rabbits under various housing conditions. Appl. Anim. Behav. Sci. 111, 342–356. Princz, Z., Szendro˝ , Zs., Dalle Zotte, A., Radnai, I., Biro´ Ne´meth, E., Metzger, Sz., Gyovai, M., Orova, Z., 2005. Effect of different housing on productive traits and on some behaviour patterns of growing rabbits. In: Proceedings of the 17th Hung. Conf. Rabbit Prod., Kaposva´r, pp. 95–102. Reiss, D., Marino, L., 2001. Mirror self-recognition in the bottlenose dolphin: a case of cognitive convergence. Proceedings of the National Academy of Science of the United States of America 98, 5937–5942. SAS Institute, 1990. SAS/STAT User’s Guide, Version 6, 4th ed. SAS Institute Inc., Cary, NC, USA, ISBN: 1-55544-376-1. Schilhab, T.S.S., 2004. What mirror self-recognition in nonhumans can tell us about aspects of self. Biol. Philos. 19, 111–124. Seaman, S.C., Waran, N.K., Mason, G., D’Eath, R.B., 2008. Animal economics: assessing the motivation of female laboratory rabbits to reach a platform, social contact and food. Anim. Behav. 75, 31–42. Sherwin, C.M., 2004. Mirrors as potential environmental enrichment for individually housed laboratory mice. Appl. Anim. Behav. Sci. 87, 95–103. Suarez, S.D., Gallup, G.G., 1981. Self-recognition in chimpanzees and orangutans, but not gorillas. J. Hum. Evol. 10 (2), 175–188. Thompson, T.I., 1964. Visual reinforcement in fighting cocks. J. Exp. Anal. Behav. 7, 45–49. Watanabe, S., 2002. Preference for mirror images and video image in Java sparrows (Padda oryzivora). Behav. Process. 60, 35–39. Williams, C.K., Parer, I., Coman, B.J., Burley, J., Braysher, M.L., 1995. Managing Vertebrae Pets: Rabbits. Bureau of Resource Science/CSIRO Division of Wildlife and Ecology, Canberra, p. 245.
Contents lists available at ScienceDirect
Applied Animal Behaviour Science journal homepage: www.elsevier.com/locate/applanim
Rabbit preference for cages and pens with or without mirrors Antonella Dalle Zotte a,*, Zolta´n Princz b, Zsolt Matics c, Zsolt Gerencse´r b, Szilvia Metzger b, Zsolt Szendro˝ b a
Department of Animal Science, Padova University, Agripolis, Viale dell’Universita` 16, 35020 Legnaro (PD), Italy Faculty of Animal Science, Kaposva´r University, 7401 Kaposva´r, P.O. Box 16, Hungary c MTA - KE Research Group of Animal Breeding and Hygiene, Kaposva´r University, Hungary b
A R T I C L E I N F O
A B S T R A C T
Article history: Accepted 12 August 2008 Available online 23 September 2008
Five-week-old Pannon White rabbits were housed in a closed climatized rabbitry and randomly assigned to either pens (56 rabbits) having a basic area of 1 m2 with a stocking density of 16 and 12 rabbits/m2 or to 18 individual cages (0.24 m2/cage). The pens and the cages were divided into two halves and animals could move freely between the two halves through swing doors. The walls of one half of the pens and cages were completely covered with mirrors while the other half was covered with white plastic panels. A 24 h video recording was made twice a week using infrared cameras and the number of rabbits in each pen and cage was counted every 15 min. The duration of the trial was 6 weeks. The lighting period was 16L/8D. In each half of the cage or pen, a feeder and nipple drinkers were available and feed intake was measured separately. Throughout the entire rearing period, 72% of the individually caged rabbits showed a preference for the cage half enriched with mirrors (P < 0.001). This preference decreased slightly with increasing age. Preference toward the cage half provided with mirror walls was independent of the time of day; in other words, during the active period (23:00–05:00) corresponding to the dark part of the day, rabbits continued to prefer the mirrored half even if the vision of the reflected image was reduced. The presence of conspecifics at different stocking densities (12 vs. 16 rabbits/m2) did not reduce this interest in mirrors: averaging the ages, 66% of animals living at 16 rabbits/m2 stocking density and 63% of those living at 12 rabbits/m2 density were found in the half pen with mirrors (P < 0.001). Group-penned rabbits showed a marked preference toward mirrors during the active period (73–76% for 12 and 16 rabbits/ m2 stocking densities, respectively; P < 0.001). The results suggest that the presence of mirrors offers advantages perhaps related to comfort and welfare, and therefore might be used as environmental enrichment for fattening rabbits and advised for rabbits caged individually for long periods. ß 2008 Elsevier B.V. All rights reserved.
Keywords: Growing rabbits Preference test Mirrors Individually caged Group-penned
1. Introduction The current intensive rabbit breeding system for meat production holds small groups of animals in wire cages that might be considered barren environments. In Italy and Hungary, rabbits are most often caged in pairs for the best
* Corresponding author. Tel.: +39 0498272640. E-mail address: [email protected] (A. Dalle Zotte). 0168-1591/$ – see front matter ß 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.applanim.2008.08.011
expression of live performance, decreased ear lesions and other aggressive behaviour (Maertens and Van Herck, 2000; Princz et al., 2005; Princz et al., 2008b), lower mortality rates (Dal Bosco et al., 2002), and higher carcass yield (Dal Bosco et al., 2002; Dalle Zotte et al., 2008) compared to larger group-housed rabbits. On the other hand, rabbits kept as laboratory animals in social isolation can display physiological symptoms of stress, i.e. stereotypic behaviours such as cage chewing and bar biting which are relieved by the presence of conspecifics (Held
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et al., 1995; Chu et al., 2004). These stereotypic behaviours are much less frequent in pair-caged rabbits reared for meat production (Mirabito et al., 1999; Dal Bosco et al., 2002; Princz et al., 2008b). One of the main objections to caged rabbit housing is the barren environment. Several forms of enrichment have been studied (e.g., plastic platform, hiding box, gnawing stick) to alleviate this problem and specifically in regard to productive performance and the behaviour and welfare of growing rabbits (Maertens et al., 2004; Luzi et al., 2005; Princz et al., 2008a). Mirrors have also been shown to temporarily enrich the environment of some animals kept in partial isolation (conspecifics can be viewed by the isolated animal but social contact is not permitted) (Parrott et al., 1988; McAfee et al., 2002; Mills and Davenport, 2002). The effect of mirrors has been evaluated in several behavioural and welfare studies. Mirror self recognition (MSR) has been thoroughly studied in human and nonhuman primates. MSR was proven in chimpanzees (Gallup, 1970; Suarez and Gallup, 1981; Povinelli et al., 1997; Schilhab, 2004), bonobos (De Veer and Van den Bos, 1999), orangutans (Suarez and Gallup, 1981), dolphins (Delfour and Marten, 2001) and elephants (Plotnik et al., 2006). Birds have different attitudes to mirrors. Fighting cocks show aggressive behaviour towards a mirror (Thompson, 1964). Mirror image has led to increased mirror pecking and wing flapping, which are typical aggressive behaviour in jungle crows (Kusayama et al., 2000). Pigeons showed induced attack against mirror (Cohen and Looney, 1973). In both cases, the mirror image represents an image of a conspecific. Contrary to these results, Java sparrows showed strong preference for a self-image in the mirror (Watanabe, 2002). Grey parrots engaged in mirror-image stimulation, mirror-mediated object discrimination, and mirror-mediated spatial location (Pepperger et al., 1995). Sometimes it is necessary to house animals individually; housing gregarious species as individuals might have a negative effect on welfare, however. This is why environmental enrichment is recommended. Mirrors have been provided routinely for caged pet birds. Sherwin (2004) investigated the potential of mirrors in improving the welfare of mice. Mirrors slightly reduced occupation levels in the cage with a mirror and considerably decreased the amount of feeding from the feeder next to the mirror. It seems that mice were fearful of the mirror (or perhaps they thought that the image represented a conspecific competing for the food). Stabled horses are usually allowed limited social contact, and this restriction can cause frustration. Weaving is a form of locomotor stereotypic behaviour. The provision of a mirror might mimic visual contact and therefore help reduce social isolation in the stable (Mills and Davenport, 2002; McAfee et al., 2002). Parrott et al. (1988) compared individually housed sheep in isolation pens in small huts with or without mirrors in them. Isolated sheep showed considerable interest in the mirror, and stress responses were lower in the group with the mirror. Later, Parrott (1990) established that the response to isolation can be partially reduced
when sheep are provided with a mirror, indicating that the sight of other sheep or their image may have stressreducing properties. Piller et al. (1999) examined whether exposure to a mirror reduces the stress of social isolation of heifers confined to single-animal weigh scales. Lower heart rates and decreased movement would seem to indicate that mirror exposure reduces stress more than side view placement. The objectives of this study were to examine how mirrors could influence the rabbits’ free choice towards the half of the cage or pen provided with mirrors on their walls rather than the other half of the cage or pen with plastic panels either when raised singly in total isolation or in groups. We also attempted to investigate rabbit preference towards the mirrored half by age, part of the day considered, and two stocking densities because all these factors are believed capable of modifying rabbit choice. 2. Materials and methods Seventy-four 5-week-old Pannon White rabbits – selected at random from both sexes and from different litters – were housed in a closed climatized rabbitry (room) in Kaposva´r University (Hungary). The lighting period was 16L/8D (lights on: 6:00–22:00) and the temperature of the rabbitry was kept constant at 18 8C. The rabbits were fed a commercial pelleted diet ad libitum and water was available on demand from nipple drinkers. Eighteen rabbits were caged individually (cage size: 0.24 m2) while 56 rabbits were housed in pens with a basic area of 1 m2 and a stocking density of 16 rabbits/m2 (2 pens) or 12 rabbits/m2 (2 pens). Each cage and pen was made of wire net with net floor and divided into two halves. The walls of one half of the cages and pens were covered with mirrors while those of the other half were covered with white plastic panels and placed alternatively in order to avoid disturbing position effects (Figs. 1 and 2). The panels were odourless with flat surface. Cages and pens were ventilated through their wire net parts (top and floor); bedding was not furnished. In each half of the cage and pen, a feeder and two nipple drinkers were available. Animals could move freely between the two halves of cage or pen through swing doors. The individually caged rabbits were totally isolated from conspecifics by these vertical mirrors and plastic panels. The duration of the trial was of 6 weeks (from 5 weeks – weaning – to 11 weeks of age), which corresponds to the standard fattening period of commercial rabbits reared for meat production. The feed intake of nine individual cages and all pens was measured weekly by weighing separately the two feeders on the mirror and plastic halves, and was expressed as a percentage of the total weekly intake in each half. A 24 h video recording using infrared cameras was made twice a week. On these recording days, no one entered the room and the animals were controlled through a large window covered with a light-isolating curtain. During non-recording days, rabbits were scarcely distracted by humans during environmental and animal controls and feeding that lasted only a few minutes each day, and mirrors or plastic panels reduced rabbit visibility even further. Using the recordings, the number of rabbits in each half of the cage and pen was counted with a frequency of 15 min. Only the 6–6 middle hours of light (from 11:00 to 17:00, corresponding to the most resting period) and dark (from 23:00 to 5:00, corresponding to the most active period) were taken into consideration.
Fig. 1. Design of the cage.
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Table 1 Preference of individually caged growing rabbits for cages with or without mirrors depending on age (%) Age (weeks)
Mirrors b
Plastic panels a
S.E.
Prob.
5.5 6.5 7.5 8.5 9.5 10.5 S.E. Prob.
79.0 67.6 a 69.7 a 68.5 a 72.1b 72.0 b 0.66 <0.001
21.0 32.4 b 30.3b 31.5b 27.9 a 28.0 a 0.66 <0.001
2.37 1.43 1.43 1.43 1.43 1.43
<0.001 <0.001 <0.001 <0.001 <0.001 <0.001
5.5–10.5
71.5
28.5
0.66
<0.001
Means in a column with different superscripts (a and b) were significantly different (P < 0.05).
Fig. 2. Design of the pens.
2.1. Statistical analysis Preference data for the two half sections (mirror vs. plastic panel) in terms of percentages of rabbit occupancy and feed intake were analysed separately for individually caged and group-penned rabbits. Grouppenned rabbit data were also analysed separately for the two stocking densities (12 vs. 16/m2). The linear model of ANOVA adopted included the effect of the type of wall (mirror vs. plastic panels), age (5–11 weeks), part of the day (active vs. resting period), and their interaction. Variance analysis was performed using the GLM procedure of the SAS program (SAS Institute, 1990).
3. Results and discussion 3.1. Individually caged rabbits Throughout the entire rearing period, 72% of the individually caged rabbits showed a preference for the cage half enriched with mirrors, although this preference decreased significantly from 79.0% to 67.6% between ages of 5.5 and 6.5 weeks and increased to 72.0% up to the week 10.5 (Table 1). The results permit the hypothesis that isolated rabbits are attracted to reflected images of themselves, at least until 11 weeks of age, and that mirror images might serve them as ‘‘companions’’, as has already been adopted for other social farm animals, such as horses (Mills and Davenport, 2002; McAfee et al., 2002), sheep (Parrott et al., 1988) and cattle (Piller et al., 1999). Great apes (Gallup, 1970), dolphins (Reiss and Marino, 2001), chimpanzees (Suarez and Gallup, 1981), bonobos (Povinelli et al., 1997), orangutans (De Veer and Van den Bos, 1999), dolphins and other marine mammals (Delfour and Marten, 2001) have been proven capable of selfrecognition in mirrors. It is generally believed that
primates and dolphins have greater cognitive powers than rabbits, and therefore according to literature (Jones and Phillips, 2005), rabbits are unlikely to prove capable of selfrecognition. Rabbits might interpret the image in the mirror as a conspecific (familiar or unfamiliar), however. Jones and Phillips (2005), in fact, found that individually caged adult rabbits with or without the possibility to see a conspecific in the adjacent cage were initially attracted to the mirror and spent more time sniffing and scrabbling at it, apparently in an attempt to reach the image. Over a 1week period, this increased sniffing of vertical boundaries indicated the mirror as a more interesting stimulus to the rabbits than a conspecific, presumably because a relationship with the conspecific had been established and confirmed the rabbit’s expectations, whereas the image in the mirror failed to exhibit the expected behaviour. Jones and Phillips (2005) also observed that the presence of a mirror decreased the frequency of ‘‘looking out of the cage’’ behaviour, indicating that a mirror may make the cage a more stimulating environment. The preference of the individually housed rabbits for the cage half provided with mirror walls was independent of the time of day (Table 2). During the active period, 71.5% of the rabbits were found in the mirrored half, even if this active period corresponds to the dark phase. Most likely, the rabbits memorised the part of the cage that gave them the best social perception of presence of conspecifics, and they found it in the dark navigating primarily by smell helped by tactile signals (whiskers). The rabbits probably associated that section with the presence of conspecifics and recognized it by following odour marks. Moreover, given that the rabbit can see in the dark to some degree by the presence of tapetum lucidum – a remarkable example of
Table 2 Preference of individually caged growing rabbits for cages with or without mirrors depending on part of day (%) Part of the day (h)
Mirrors
Plastic panels
S.E.
Prob.
23:00–05:00a 11:00–17:00b S.E. Prob.
71.5 71.5 0.66 0.958
28.5 28.5 0.66 0.958
0.93 0.88
<0.001 <0.001
a b
Active period. Resting period.
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276
Table 3 Feed intake proportion (%) of individually caged growing rabbits depending on wall type and age Age (weeks)
Mirrors
Plastic panels
S.E.
Prob.
5–6 6–7 7–8 8–9 9–10 10–11 S.E. Prob.
70.3 69.5 68.9 69.6 67.3 67.0 2.24 0.99
29.7 30.5 31.1 30.4 32.7 33.0 2.24 0.99
5.49 5.49 5.49 5.49 5.49 5.49
<0.001 <0.001 <0.001 <0.001 <0.001 <0.001
5–11
68.8
31.2
2.24
<0.001
Feed intake was recorded in nine cages.
neural cell and tissue specialization as an adaptation to a dim light environment – (Ollivier et al., 2004) and because the experimental room adopted was not completely dark, recognition was probably aided by the partial sight of reflected rabbits in the mirror (the dim light of the videocamera LED and the white coloured room walls might have been sufficient for the rabbits to perceive their reflection). Our findings are supported by the observation of Sherwin (2004) on mice: the same behaviour observed during the illuminated phase (avoidance of feeding from the feeder next to the mirror) was noticed during the dark phase as well. The feed intake proportion of the individually caged rabbits was significantly higher in the cage half with mirrors (69% of the total feed intake) regardless of the
rabbit’s age (Table 3), indicating that when the rabbits stayed in the mirrored half of the cage they also fed there. This feeding behaviour could represent a positive sign of welfare diametrically opposed to the negative effect that mirrors appeared to have on mouse feeding habits (Sherwin, 2004). The results of our study seem to show that mirrorimage stimulation could be a partial conspecific substitute for prepubertal individually housed rabbits, as observed by Parrott et al. (1988) in sheep. Further study could quantify how important mirrors are to individual- and group-reared young rabbits by using economic demand theory, e.g. attaching weights to the push door, as recently assessed by Seaman et al. (2008) in individually caged adult female rabbits, in order to test their motivation to reach a platform, social contact, or food. 3.2. Group-penned rabbits Rabbits housed in pens with different stocking densities (16 vs. 12 rabbits/m2) showed a clear preference for the part of the pen enriched with mirrors by all age groups considered (Table 4). Averaging the ages, 66% of the rabbits living at 16/m2 rabbit density and 63% of those living at 12 rabbit/m2 density were found on the side with mirrors (P < 0.001). Preference for the mirrored half was highest at 5.5 weeks of age (about 87%) but significantly decreased (P < 0.001) with age to 55.8 and 52.8% at 16 and 12 rabbit/ m2 density, respectively. This result was unexpected because the presence of conspecifics should have theoretically reduced interest in
Table 4 Preference of group-penned growing rabbits for pens with or without mirrors depending on age and stocking density (%) Age (weeks)
Stocking density 16 rabbits/m2
12 rabbits/m2
Mirrors
Plastic panels
S.E.
Prob.
Mirrors
Plastic panels
S.E.
Prob.
5.5 6.5 7.5 8.5 9.5 10.5 S.E. Prob.
87.0 d 71.5 c 62.0 b 62.3 b 58.9 b 55.8 a 0.40 <0.001
13.0 a 28.5 b 38.0 c 37.7c 41.1c 44.2 d 0.40 <0.001
1.29 0.91 0.91 0.91 0.91 0.91
<0.001 <0.001 <0.001 <0.001 <0.001 <0.001
86.7d 70.7 c 59.3 b 58.9 b 50.5 a 52.8 a 0.43 <0.001
13.3 a 29.3b 40.7c 41.1c 49.5 d 47.2d 0.43 <0.001
1.38 0.97 0.97 0.97 1.00 0.97
<0.001 <0.001 <0.001 <0.001 1.000 0.004
5.5–10.5
66.2
33.8
0.40
<0.001
63.1
36.9
0.43
<0.001
Means in a column with different superscripts (a, b, c and d) were significantly different (P < 0.05).
Table 5 Preference of group-penned growing rabbits for pens with or without mirrors depending on part of day and stocking density (%) Part of day (h)
Stocking density 16 rabbits/m2
23:00–05:00a 11:00–17:00b S.E. Prob. a b
Active period. Resting period.
12 rabbits/m2
Mirrors
Plastic panels
S.E.
Prob.
Mirrors
Plastic panels
S.E.
Prob.
75.9 56.6 0.40 <0.001
24.1 43.4 0.40 <0.001
0.56 0.56
<0.001 <0.001
73.0 53.2 0.43 <0.001
27.0 46.8 0.43 <0.001
0.60 0.60
<0.001 <0.001
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Table 6 Feed intake proportion (%) of group-penned growing rabbits depending on wall type, age, and stocking density Age (weeks)
Stocking density 16 rabbits/m2
12 rabbits/m2
Mirrors
Plastic panels
S.E.
Prob.
Mirrors
Plastic panels
S.E.
Prob.
5–6 6–7 7–8 8–9 9–10 10–11 S.E. Prob.
70.3 57.6 57.5 60.2 55.2 57.6 1.36 0.134
29.7 42.4 42.5 39.8 44.8 42.4 1.36 0.134
3.33 3.33 3.33 3.33 3.33 3.33
<0.001 0.473 0.509 0.065 1.000 0.478
67.2 bc 62.4b 53.6 ab 54.8 ab 49.0 a 51.1ab 0.73 0.002
32.8 a 37.6 ab 46.4 bc 45.2 bc 51.0c 48.9bc 0.73 0.002
1.80 1.80 1.80 1.80 1.80 1.80
<0.001 <0.001 0.953 0.189 1.000 1.000
5–11
59.7
40.3
1.36
<0.001
56.4
43.6
0.74
<0.001
Means in a column with different superscripts (a, b and c) were significantly different (P < 0.05).
this form of enrichment. The highest preference for the mirrored part of the pen in most animals from 5.5 to 8.5 weeks of age confirms that young rabbits like to congregate and huddle together (Matics et al., 2004) and the perception of being present in greater number than in reality does not appear stressful for them. Contrary to the behaviour observed in individually caged rabbits, group-penned rabbits showed a greater preference for mirrors during the active (dark) period (P < 0.001), and although such preference remained statistically significant (P < 0.001; Table 5) during the resting (light) period (11:00–17:00), it was of lower magnitude. This appears to be in contrast with the behaviour observed in wild rabbits, which huddle together during the resting period but disperse around the rabbit hole to feed during the active period (Williams et al., 1995). The question arises whether rabbits in mirrored pens consider the reflected images only as other rabbits or whether they feel the cage is larger as well. As age increased, group-housed rabbits spent less time in the mirrored pen half. Matics et al. (2004) observed that although young rabbits like to huddle together in a little cage, after 6–7 weeks of age, more and more rabbits prefer to occupy larger cages that meet their need for more space. Our study indicated the opposite tendency: fewer and fewer rabbits preferred the seemingly larger mirrored half while more and more stayed in the pen without mirrors as age increased. This might mean either that the ‘‘enlarging effect’’ of mirrors has less effect on rabbit choice or that the apparently double group size generated by mirror reflections causes a feeling of crowding in older rabbits close to age of dispersal. In this study, all four sides of the cage and pen half were covered with mirrors, and the feeling of overcrowding generated by the multiple reflection probably began disturbing the older rabbits. It derives that mirrors on only one side of the cage and pen could be enough to provide some advantage to the welfare of reared rabbits. The average feed intake proportion of group-penned rabbits was to the favour of the half of the pen provided with mirrors in both 16 (59.7%) and 12 rabbits/m2 (56.4%) stocking densities (P < 0.001; Table 6). This preference for feeding in the mirrored half was statistically different in the first week of age in 16 rabbits/m2 stocking density and
in the first 2 weeks of age in 12 rabbits/m2 stocking density. This behaviour might be due to the constantly diminishing space available caused by rabbit growth around the feeder in the mirrored half, and this could have encouraged some of the rabbits to feed at the other feeder. 3.3. Conclusion This study has brought us to several conclusions. The application of mirrors in one half of the cage or pen affected rabbit preference. Both isolated and grouped-living rabbits preferred to stay and eat in the cage/pen half covered with mirrors. Although this high preference towards the mirrored half did not change with age in isolated-living rabbits, it decreased significantly with age in grouppenned rabbits, probably due to the less and less livingspace in the mirrored half as the rabbits grew. Both isolated and group-penned rabbits significantly preferred the mirrored half also during the dark phase, and this could have depended on the fact that the rabbit positively associated the area with the presence of conspecifics and recognized it by their senses. Further research is needed to evaluate rabbit behaviour and investigate the reasons behind their preference for mirrored walls in greater depth. The results suggest that the presence of mirrors offers some advantages, perhaps related to comfort and welfare, and that they could be used as environmental enrichment for fattening rabbits and advised for rabbits caged individually for long periods, such as those reared as laboratory or exhibition animals. Acknowledgements Research supported by the Italian-Hungarian Intergovernmental (Ministry of Foreign Affairs) Science and Technology cooperation programme (OMFB-00607/2005). The authors wish to thank Dr. Barbara Contiero of the Department of Animal Science (University of Padova, Italy) for helping with statistical analysis, Prof. Bruno Cozzi of the Department of Experimental Veterinary Science (University of Padova, Italy) for valuable discussion while the manuscript was in preparation, and two anonymous referees for comment on the manuscript.
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