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1994-2009 All Rights Reserved. Online Journal of Veterinary Research. You may not store these pages in any form except for your own personal use. All other usage or distribution is illegal under international copyright treaties. Permission to use any of these pages in any other way besides the before mentioned must be gained in writing from the publisher. This article is exclusively copyrighted in its entirety to OJVR publications. This article may be copied once but may not be, reproduced or re-transmitted without the express permission of the editor OJVR Online Journal of Veterinary Research Volume 13 (2):48-55, 2009 Effect of cage versus pen and stocking density on behavior and performance in rabbits T. M. Mousa-Balabel, DVM PhD* Dept. of Hygiene and Preventive Med., Fac. of Vet. Med., Kafr EL-Sheikh,University, Egypt. Present address: Department of Veterinary Pathology, Tottori University, Minami 4-101, Koyama- cho, Tottori-shi, Tottori 680-8553, Japan. ABSTRACT Mousa-Balabel TM, Effect of cage versus pen and stocking density on behavior and performance in rabbits, Online J Vet Res., 13 (2):48-55, 2009. The effect of cage versus pens and six stocking densities on behavior and performance was evaluated in 76 Weanling does New Zealand White rabbits. In one test, 10 does were reared in a straw bedded pen and 10 in a cage using the same floor space (2 m 2 for all animals/group). In another test six groups of 6 does each were stocked 4, 6, 8, 10, 12, and 16 rabbits/m 2, respectively, in cages. All rabbits were fed a commercial pellet diet of 16.5% crude protein, 2.5% crude fat and 14% fibers given twice daily at 9am and 5pm and water ad libitum. Rabbits were acclimatized for one week before experiments were started. Body weight, feed intake, feed conversion ratio and behavior parameters such as maintenance, locomotory, investigatory, agonistic, comfortable and stereotypic, were recorded daily. Results revealed that weanling rabbits reared in a cage system with 10 or higher high stocking density had lower growth rates and higher mortality. Keywords: behavior, housing system, Stocking density, New Zealand White rabbit. 48

INTRODUCTION Rabbits are intensively reared for production of meat. These animals are reared in cages as well as in pens, either individually or in groups of variable sizes. A vast majority of 85%, of rabbits prefer wire net housing over the deep litter system, quite independent of their age and stocking density (Orova et al. 2004). The rabbits kept in cages spend more time resting and less time in locomotion compared with groups of rabbits reared in pens. The lower time spend in locomotion is connected with the cage size (Martrenchar et al. 2001). Rabbits moreover, spend more time in eating and drinking in cages (Dal-Bosco et al. 2002). Welfare of animals is largely regulated by various intrinsic and extrinsic factors, among which stocking density plays a pivotal role in causing stress and affecting animal behavior. Although a high cage density attenuates costs of production, this might negatively influence growth rate and increases acts of aggression by the animals (Bigler and Oester, 1996). Single caging isolates rabbits from contact with others and severely restricts their freedom to carry out natural behaviors such as rearing up on the hind legs and allogrooming as well as nearly all locomotory activities (Batchelor, 1991), which lead to atypical activities such as gnawing at metal bars, fur-chewing, pawing in cage corners, and head weaving. When the rabbits are reared in larger groups, they move more, display frequent aggressive behavior and carry more injuries (Dal-Bosco et al. 2002), and demonstrate lower frequencies of investigatory, comfort and social behaviors (Mirabito et al. 1999). The aim of this study was to investigate the effect of two housing systems and six stocking densities on the behaviors and performances of rabbits. MATERIALS AND METHODS The present work was carried out in a private rabbitry in Menuofia Governorate of Egypt. A total number of 76 weanling does of New Zealand White rabbits (with an average age of 5 weeks and an average weight of 550 g) were employed in two sets of experiments. In the first set of experiments we employed 20 does that were divided into two equal groups (10 each). The does of the first group in this experiment were reared in a straw bedded pen and the does of the second one were reared in a cage to study the effect of housing on their behaviors and performances. The floor space for both the types of housing systems remained the same at 2 m2. In the second set of experiments a total number of 56 does were used. These animals were randomly divided into six groups, beginning from Group I to Group VI, to establish stocking densities of 4, 6, 8, 10, 12, and 16 rabbits/m 2, respectively. ANIMALS of each group in this set of experiments were reared in a separate cage system to study the effect of stocking density on their behaviors and performances. The caged rabbits were housed in commercial hutches that came complete with feeders 49

and automatic drinkers. They were fed a commercial pelleted diet, which contained 16.5% crude protein, 2.5% crude fat and 14% fibers (Cairo Company). The diet was served twice daily at 9 a.m. and 5 p.m. in an ad libitum amount and the drinking water was also made available ad libitum. All rabbits were allowed a stay of one week to become accustomed to their new cages. MEASUREMENTS: Individual body weights of the does at the beginning and at the end of the experiment were recorded. Amount of food served was recorded daily. Feed conversion ratio (feed efficiency) was calculated. Behavior Observation: Behaviors of the rabbits were recorded by a video camera. Observations were made for one hour every week for each group (one hour/week/each group). The hour-long observation was made in three periods of 20 minutes duration, during the same day at morning, afternoon, and evening, beginning at 08:00, 12:00, and 16:00 hours. The animal behaviors were continuously recorded during these periods of observation. These observation times were chosen in order to give us a representative sampling of the rabbits natural activity pattern (Gunn and Morton, 1995). For observation purposes, the animals in each group were labeled by markings on their ear with a nontoxic permanent marker to facilitate behavioral observations. Some animals were re-marked as and when necessary. The observed behaviors were recorded in six different categories, namely, maintenance, comfort, agonistic, investigatory, locomotory and stereotypic. Maintenance behaviors relate to self-maintenance of the animal and included standing, resting, drinking and eating (Fraser, 1980). Any motionless animal performing no discernible activity was considered at rest. Comfort behaviors relate to body care (self-grooming, scratching, head shaking and stretching). Agonistic behaviors refer to the complex of aggression, threat, appeasement, and avoidance behavior that often occur during encounters between members of the same species and include biting another individual and chasing (McFarland, 1981). Investigatory or exploratory behaviors are those which may be aimed at a particular commodity or environmental situation. Locomotory behaviors are voluntary movements that displaced the entire body, such as hopping. Stereotypic behaviors are performed repeatedly in a fixed manner and in response to no discernible stimulus and with no discernible goal, and include clawing at cage walls or corners, and biting cage bars or food hoppers (Murphy, 1978). PERCENTAGE (%) FREQUENCY OF BEHAVIOR: The total number of occurrences of a particular behavior for each rabbit constituted a frequency value. For example, out of 288 recordings for one rabbit, 63 were noted as Doze. Frequency values were then converted into 50

a percentage for each behavior (e.g. for one rabbit, the % frequency of Doze was 63/288 X 100, i.e. 21.9%). This particular rabbit dozed for 21.9% of its recording period. For each observed behavior, the percentage frequencies from individual rabbits were added together and divided by the number of rabbits under observation in each group to give a mean percentage (%) frequency (Gunn and Morton, 1995). The effect of floor type and stocking density on the various behaviors were evaluated by means of analysis of variance with multiple factors using the following model: BF(%)ij = µ+ Fi + SDj + eijk (BF = behavior, µ= grand mean, Fi = floor type (i = 1-2), SDj = stocking density (j = 1-6), eijk = residual). The analyses were conducted using the SPSS 10.0 software package (SPSS for Windows, 1999). RESULTS Behavior: The behavioral observations (Table 1) show that there were different average percentages of observed behaviors for penned and caged rabbits. Locomotory behavior was higher in caged rabbits (23. %) than that observed in penned ones (17.9%). The most common behaviors observed in caged rabbits was maintenance behavior (42. %) that was a lowly 25% for penned rabbits, while the reverse was true for comfort behaviors (22.5% and 42%, respectively). Investigatory behaviors were observed most often in penned rabbits (12.1% vs. 8.6% caged), whereas agonistic behaviors were less observed in caged rabbits (1.5%) than (2.5%) for penned ones, while the reverse was true for stereotypic behaviors (1.3 % and 0.5 %, respectively). Table 1: Effects of housing type on the frequency of some behaviors in weanling rabbits (%). Behavior Housing Type SE Significance Caged Penned Locomotory behaviors 23.8 a 17.9 b 0.263 <0.001 Maintenance behaviors 42.3 a 25 b 0.064 <0.001 Comfort behaviors 22.5 a 42 b 0.226 <0.001 Investigatory behaviors 8.6 a 12.1 b 0.361 <0.001 Agonistic behaviors 1.5 a 2.5 b 0.417 <0.001 Stereotypic behaviors 1.3 a 0.5 b 0.041 <0.001 abc Different letters in the same row within an examined effect mean significant differences (P<0.05) Stocking density also had a significant effect on the frequency of observed behaviors (Table 2). The locomotory, maintenance, comfort, agonistic and stereotypic behaviors showed an increase as the stocking density increased. There was, however, no effect of stocking density on the investigatory behaviors. 51

Table 2: Effects of stocking density on the frequency of some behaviors in weanling rabbits (%) Stocking density (rabbit/m2) Behavior SE Significance 4 6 8 10 12 16 Locomotory behaviors 23.53 a 23.59 a 23.47 a 23.42 a 17.61 b 17.38 b 0.246 <0.001 Maintenance behaviors 36.62 a 36.5 a 36.49 a 36.41 a 38.27 b 38.22 b 0.058 <0.001 Comfort behaviors 20.43 a 20.17 a 20.32 a 20.43 a 22.93 b 23.05 b 0.312 <0.001 Investigatory behaviors 17.41 a 17.54 a 17.58 a 17.51 a 17.42 a 17.55 a 0.451 0.006 Agonistic behaviors 2.0 a 2.16 a 2.13 a 2.18 a 3.55 b 3.59 b 0.346 <0.001 Stereotypic behaviors 0.01 a 0.04 a 0.01 a 0.05 a 0.22 b 0.21 b 0.052 <0.001 abc Different letters in the same row-within an examined effect -mean significant differences (P<0.05) Performance: The caged rabbits showed higher feed consumption and body weight gain and a lower percentage of mortality than the penned ones. The results of performance related to stocking density revealed that the feed consumption, body weight gain, feed conversion rate (feed efficiency) as shown in Table 3 decreased as the stocking densities increased. Table 3: Effects of housing type and stocking density on the performance of weanling rabbits (%) Housing type Stocking density (rabbit/m2) Significance Behavior Pen Cage 4 6 8 10 12 16 SE Housing type Initial BW(g) 555 a 556 a 555 a 553 a 553 a 552 a 553 a 554 a 0.236 0.005 0.006 Stocking density Final BW (g) 1765 a 1970 b 1655 a 1747 b 1746 b 1735 b 1527 c 1505 d 0.079 <0.001 <0.001 Body BW(g) 1210 a 1414 b 1100 a 1194 b 1193 b 1183 b 974 c 951 d 0.418 <0.001 <0.001 Feed consumption 3820 a 4300 b 3925 a 4255 b 4264 b 4215 b 3950 c 3745 d 0.426 <0.001 <0.001 (g) Feed 0.317 a 0.328 b 0.280 a 0.281 a 0.279 a 0.281 a 0.247 b 0.253 b 0.328 <0.001 <0.001 efficiency Mortality (%) 10 a 0 b 0 a 0 a 0 a 0 a 8.33 b 12.5 c 0.048 <0.001 <0.001 abc Different letters in the same row within an examined effect mean significant differences (P<0.05) DISCUSSION Housing system affected the welfare of does because of the scope it provided for performing species-specific behaviors. Locomotory behavior (Hopping), which is a basic movement of rabbits, occurred even when the rabbits were restricted in cage. The average hopping was higher in caged rabbits (23.8%) than that observed in penned ones. The present 52

results agree with the finding of Morisse et al. (1999) who explained the preference of rabbits for the wire net floor instead of the straw bed because of the importance the rabbits attached to the maintenance of a clean fur. The most common behavior observed in caged rabbits was maintenance behavior (42.3%), which was a lowly 25% for penned rabbits, while the reverse was true for comfort behavior (22.5% and 42%, respectively). It is reasonable that straw as a substrate is more comfortable than wire net, which in some cases can cause injuries to rabbits` feet. These results are in agreement with that of Podberscek et al. (1991) who recorded that the maintenance behaviors were observed more often in caged rabbits than in penned rabbits and do not coincide with the findings recorded by Postollec et al. (2003). This difference may be attributed to cage size. Investigatory behaviors were observed most often in penned rabbits (12.1% vs. 8.6% caged), agonistic behaviors were less observed in caged rabbits (1.5%) than (2.5 %) for penned ones, while the reverse was true for stereotypic behaviors (1.3 % and 0.5 %, respectively). Stocking density affected the frequency of locomotion. A stocking density of 12 and 16 rabbits/m² significantly lowered the observed locomotory behavior. This may be explained by the lower number of animals/m2, which allowed higher locomotor activity (Verga et al. 2004), and this result is in accordance with that of Mormerde (1988) who found that the high stocking density may be related to lower movement frequency. The frequency of maintenance (rest, drinking and eating) and comfort (grooming, scratching, head-shaking and stretching) behaviors were significantly affected by stocking density; they increased as the stocking density increased. This observation may be attributed to the higher stocking densities that caused overcrowding, which restricted the freedom of movement and forced the rabbits to spend more time in eating and grooming. There was no significant difference in investigatory behaviors (stamping, rearing and licking the wall) among the six groups with different stocking densities. But, the agonistic behaviors (biting and chasing) were more observed in groups with high stocking densities. A higher innate motivation of the rabbits to be more active in exhibiting more frustration especially during chronic close confinement could be a possible cause for such behaviors. Alternately such behaviors may reflect the lack of ability to socialize among rabbits to assert their position in the hierarchy of dominance. Stereotypic behavior significantly increased as the stocking density increased. This observation could be explained due to frustration, lack of stimuli and/or restriction in movement the rabbits experienced, which did not stimulate the animals enough to prevent stereotypies from developing (Broom, 1983). Verga et al., (2004) moreover, have 53

demonstrated that the animals reared in conditions rich in stimuli are more calm, which decreases the occurrence of stereotyped behavior. The behavioral results related to the stocking density do not coincide with the observations of Morisse and Maurice (1997), who reported that the behavioral patterns of rabbits kept at 6 weeks of age were only slightly affected by stocking density. But, at 10 weeks of age, social interactions, feeding, locomotory behaviors were reduced, while resting, comfort and investigatory behaviors were more noticeable when the stocking density was higher. This can most likely be attributed to the breed of the animals observed, and stocking density, as their stocking density ranged from15 to 23 rabbits/m 2. Analysis of the growth performance shows that the penned rabbits showed lower feed consumption than their caged counterparts. This could be due to consumption of straw, which may have reduced the feed intake. The caged rabbits obtained higher body weight gain than those reared in pens. The reduction of growth rate for rabbits housed in pens could be explained by the greater physical activity or the lower feed intake. Also, Morisse et al. (1999) hypothesized that straw ingestion was a possible cause of reduction in weight gain observed in rabbits raised on straw litter. In addition, the rate of mortality was higher in penned rabbits than the caged ones. This could be due to an increased infection and the contact with excreta, which increases the possibility of contamination and explains the higher mortality (Mirabito, 1998). The highest stocking density of more than 10 rabbits/m 2 tends to reduce feed intake, which could be attributed to the reduced space available for movement. Consequently the body weight gain was reduced, resulting in a decrease in feed efficiency. Moreover, mortalities were observed only among the rabbits with stocking densities of 12 and 16 rabbits/m 2 and this may be due to an increase in aggressive behavior in these groups. These findings agree with those obtained by Trocino et al. (2004), who recorded that reducing the stocking density improved the growth performance of weanling rabbits. CONCLUSION Based on the results of this experimentation, it can conclude that the welfare of the rabbits is best achieved by rearing them in cage system as opposed to raising them in pens, and the stocking density of the rabbits should not be more than 10 per square meter. REFERENCES Batchelor, G.R. 1991. Group housing on floor pens and environmental enrichment in sandy lop rabbits. Anim. Tech. 42 (2): 109 120. Bigler, L., and H. Oester.1996. Group housing for male rabbits In: Proc. 6th World Rabbit Congress, 1996 July, Toulouse, France, Vol. 2: 411-415. 54

Broom, D.M. 1983. Stereotypies as animal welfare indicators. In: D. Smidt (Editor), Indicators relevant to Farm Animal Welfare. Martinus Nijhoff, The hague, pp. 81-87. Dal-Bosco, A., C. Castellini, and C. Mugnai, 2002. Rearing rabbits on a wire net floor or straw litter: behaviour, growth and meat qualitative traits, Livest. Prod. Sci. 75: 149 156. Fraser, A. 1980. Farm Animal Behaviour. Baillitre, Tindall and Cassell, London, pp. 89-148. Gunn, D. and D.B. Morton, 1995. Inventory of the behaviour of New Zealand White rabbits in laboratory cages. Appl. Anim. Behav. Sci. 45: 277 292. Martrenchar, A., E. Boilletot, J.P. Cotte, and J.P. Morisse, 2001. Wire-floor pens as an alternative to metallic cages in fattening rabbits: influence on some welfare traits, Anim. Welfare 10: 153 161. McFarland, D. 1981. The Oxford Companion to Animal Behaviour. Oxford University Press, Oxford, pp: 1013. Mirabito, H. 1998. Bien-étre du lapin: les orientations. Cuniculture. 25: 73-78. Mirabito, H., P. Galliot, C. Soulhet, and V. Pierre, 1999. Logement des lapins en engraissement en cage de 2 ou 6 individuals: étude du budget-temps, Proceedings of the 8émes Journ. Rech. Cunicole Paris, France, pp. 55 58. Morisse, J.P. and R. Maurice, 1997. Stereotypies as animal welfare indicators. Appl. Anim. Behav. Sci. 54: 1351-1357 Morisse, J. P., E. Boilletot, and A. Martrenchar, 1999. Grillage oulitière: choix par le lapin et incidence sur le bien-ètre. In: 8èmes Journ. Rech. Cunicole Fr., Paris, pp. 63-66. Mormerde, P. 1988. Neuroendocrine stress responses. Rec Med. Vet., 164 (10): 723-741. Murphy, L.B. 1978. A Review of Animal Welfare and Intensive Animal Production. Queensland Department of Primary Industry, Brisbane, Qld., 67 pp. Orova, Z., Zs. Szendrõ, Zs. Matics, I. Radnai, and E. Biró-Németh, 2004. Free choice of weanling rabbits between deep litter and wire net floor in pens, Proceedings of the 8th World Rabbit Congress, Puebla, Mexico, pp. 1263 1265. Podberscek, A.L., J.K. Blackshaw, and A.W. Beattie, 1991.The behaviour of group penned and individually caged laboratory rabbits. Appl. Anim. Behav. Sci., 28: 353-363. Postollec, G., E. Boilletot, R. Maurice, and V. Michel, 2003. Influence de l apport d une structure d enrichissement (plate-forme) sur les performances zootechniques et le comportement des lapins d engraissement élevés en parcs, Proceedings of the 10ème Journ. Rech. Cunicole Paris, France, pp. 173 176. SPSS for Windows 1999. Version 10.0, Copyright SPSS Inc. Trocino, A., G. Xiccato, P.I. Queaque, and A. Sartori, 2004. Group housing of weanling rabbits: effect of stocking density and cage floor on performance, welfare and meat quality, World Rabbit Sci. 13: 138 139. Verga, M., I. Zingarelli, E. Heinzl, V., Ferrante, P. A. Martino, and F. Luzi, 2004. Effect of housing and environmental enrichment on performance and behaviour in fattening rabbits. World Rabbit Sci. 13: 139-140. 55