Effect of housing conditions on production, carcass and meat quality traits of growing rabbits

Meat Science 96 (2014) 41–46

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Effect of housing conditions on production, carcass and meat quality traits of growing rabbits Zs. Matics a, Zs. Szendrő a,⁎, M. Odermatt b, Zs. Gerencsér a, I. Nagy a, I. Radnai a, A. Dalle Zotte c a b c

Faculty of Animal Science, Kaposvár University, PO Box 16, 7401 Kaposvár, Hungary Olivia Ltd, Mizse 94, 6050 Lajosmizse, Hungary Department of Animal Medicine, Production and Health, University of Padova, Agripolis, Viale dell'Università 16, 35020 Legnaro (PD), Italy

a r t i c l e

i n f o

Article history: Received 1 March 2013 Received in revised form 12 June 2013 Accepted 2 July 2013 Keywords: Growing rabbit Pen Platform Production Carcass traits Meat quality

a b s t r a c t Production, carcass traits and meat quality of rabbits housed in cages or in different pens were compared. Rabbits (n = 579) were sorted into 5 groups: C = cage (2 rabbits/cage); pen without platform: P11 = 9 rabbits/pen; P16 = 14 rabbits/pen; pen with platform: PW = wire net platform, 14 rabbits/pen; PD = platform with straw-litter, 14 rabbits/pen. Feed intake and average daily gain between 5 and 11 weeks, and body weight at 11 weeks were significantly higher in C rabbits than that of the mean of pen-housed groups, while the PD group had the lowest growth performance. C rabbits had the smallest hind part to reference carcass (P b 0.001) and the largest percentage of perirenal and scapular fat (P b 0.001). The meat/bone ratio was the largest in group C (P b 0.05). Differences were recorded in a* value and lipid content of m. Longissimus dorsi. Rabbits housed in cages generally had the best performance whereas those housed in pens with platform exhibited the worst. © 2013 Elsevier Ltd. All rights reserved.

1. Introduction An increasing proportion of consumers recognize animal welfare aspects of livestock production and prefer to buy meat of animals kept in an environment with adequate housing. However, the human idea of the optimal housing conditions of a certain species may not coincide with the real needs for that species. Thus animal behavior and animal welfare are research areas with several unanswered questions. According to the survey of EFSA (European Food Safety Authority (EFSA), 2005) and also more recent studies (Szendrő & Luzi, 2006) there are several experiments that need to be conducted in rabbit production before specific directives can be given. In small cages, rabbits have limited space for moving (Szendrő & Dalle Zotte, 2011), however, numerous experiments conducted with growing rabbits have shown that higher group size results in higher stress, lower feed intake and weight gain, decreased slaughter performance, increased infection and mortality, and higher occurrence of lesions on the body due to aggression (Szendrő & Dalle Zotte, 2011). In the larger groups the dressing out percentage was poorer, the ratio of fore part to reference carcass decreased, while the hind part increased, fat deposits and meat/bone ratio also decreased (Combes, Postollec, Canquil, & Gidenne, 2010; Dal Bosco, Castellini, & Mugnai, 2002; Dalle Zotte, Princz, Metzger, et al., 2009; Szendrő et al., 2009). Because of

⁎ Corresponding author. Tel.: +36 82 505800; fax: +36 82 505 986. E-mail address: [email protected] (Z. Szendrő). 0309-1740/$ – see front matter © 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.meatsci.2013.07.001

the higher frequency of aggressiveness, living under stressful conditions resulted in lower pHu and lighter colored meat. Not only fat deposition but the fat content of the meat decreased, while water content increased (Combes et al., 2010; Dal Bosco et al., 2002; Szendrő, Princz, et al., 2009). At the same time, the PUFA, n-6, n-3 and n-6/n-3 ratio increased with stressful housing conditions (Dal Bosco et al., 2002; Dalle Zotte, Princz, Metzger, et al., 2009). However, as reported by Dalle Zotte, Princz, Matics, et al. (2009) rabbits require social interactions. In this experiment cage-rearing with different types of pens is compared. The most critical element of rabbit housing is the floor type because the animals have direct and continuous contact with the floor (resting, locomotory behavior). In large scale rabbit breeding, keeping the animals on a wire mesh floor became widespread 40–50 years ago. This method avoids the animals contact with their feces thus hinders coccidia infection. There is a general belief that deep litter is an optimal floor type for rabbits; however, rabbits can consume the spoiled litter material (Dal Bosco et al., 2002; Jekkel & Milisits, 2009; Lambertini, Vignola, & Zagnini, 2001) which increases the risk of digestive diseases (primarily coccidiosis) and mortality (Dal Bosco et al., 2002). Because of litter consumption (containing low levels of nutrients) the rabbits consume less pellets and show decreased weight gain, body weight, dressing out percentage, meat/bone ratio and amount of fat deposits (Dal Bosco et al., 2002; Lambertini et al., 2001; Metzger et al., 2003; Trocino, Xiccato, Majolini, & Fragkiadakis, 2008). If provided with a free choice of location, above 15–16 °C the rabbits generally show a preference for wire mesh floors as opposed to deep litter (Morisse, Boilletot, & Martrenchar, 1999; Orova, Szendrő, Matics, Radnai, & Biró-Németh,

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2004) because digestive heat dissipation is easier on that surface (Bessei, Tinz, & Reiter, 2001). Thus there is a great difference between consumer expectations and the demands of real animal welfare with regard to optimal floor type for rabbits. A compromise could be achieved through the use of cages provided with both wire mesh and deep litter floors, but the negative aspects of litter consumption were still the same as described for deep litter floor (Jekkel, Milisits, & Biróné Németh, 2008; Morisse et al., 1999). Keeping the rabbits after weaning on wire net floors, and placing the deep litter into the pens only during the final period of growth (Jekkel et al., 2008; Kustos, Tóbiás, Kovács, Eiben, & Szendrő, 2003; Princz, Nagy, Radnai, Gerencsér, & Szendrő, 2008) seem to be a better solution. In this experiment a new combination of wire net and deep litter floor is tested, a wire-mesh pen with an elevated platform with deep litter on it. In order to answer the questions raised and surrounding this issue an experiment was conducted to compare production, slaughter and meat quality traits of growing rabbits housed in cages or in different types of pens (with or without an elevated platform; wire-net or deep-litter platform). The main questions were: What are the differences between the cage and pen housing, between pen housing with or without platform and among the five different housing systems? 2. Materials and methods 2.1. Animals, feeds, experimental design and management The experiment was conducted in three replications at the rabbit farm of the Kaposvár University using Pannon White growing rabbits (n = 579). The rabbits (weaned at the age of 5 weeks) received a commercial diet (5–9 weeks of age: 10.3 MJ DE/kg, 14.5% crude protein, 17.5% crude fiber, medicated with 1 ppm Clinacox (diclazuril), 500 ppm OTC, 50 ppm Tiamulin; at 9–11 weeks of age: 10.6 MJ DE/kg, 16% crude protein, 16% crude fiber). A continuous 16L:8D lighting schedule was applied, and the temperature ranged between 15 and 19 °C. At weaning, individually marked rabbits with ear tattoos were randomly assigned to the following 5 groups: Group C (control group): conventional cage (0.12 m2), wire net floor (60 cages of 2 rabbits/cage, 16.6 rabbits/m2; n = 120). Other rabbits were housed in pens (having a basic area of 0.86 m2), the floor type was wire net, the feeder was placed at the end of the pen while the two nipple drinkers were located at the opposite ends of the pen. The distance between the feeder and drinkers was 1.8 m. Pens without elevated platform: Group P11: 9 pens of 9 rabbits/pen, 10.5 rabbits/m2 (n = 81); Group P16: 9 pens of 14 rabbits/pen, 16.3 rabbits/m2 (n = 126). (The stocking density was 16.3 rabbits/m2 in the pens with platforms when the platform was not considered in the basic area of the pen. Taking into account the platform the stocking density was 10.9 rabbits/m2.) Pens with elevated platform: The elevated platforms, with an area of 0.43 m2, were placed at a height of 0.4 m from the pen floor, in the middle area of the pen. To facilitate access to the platform, a 0.20 × 0.25 m sized box (with a height of 0.2 m) was placed in each pen. Based on the platform types, two additional treatments were applied:

of 9 pens, which is equivalent to a stocking density of 16.3 (floor surface), and 10.9 (including the platform surface) rabbit/m2, respectively (n = 126). Individual body weight (BW) and feed intake (FI) per cage or pen were measured at 5, 7, 9 and 11 weeks. Mortality was recorded daily. Average daily gain (ADG), FI, feed conversion ratio (FCR) and mortality were calculated for every 2-week period and also for the total period between the ages of 5 and 11 weeks. Production traits were examined in all replications, but only the rabbits of the first replication were slaughtered. 2.2. Slaughter traits and muscle sampling At 11 weeks of age all rabbits were weighed at the experimental farm. One hundred and fifty five rabbits of the first replication (32, 18, 33, 36 and 36 rabbits for C, P11, P16, PW and PD groups, respectively) were randomly selected for carcass and meat quality analysis representing the average weight and variability of each group. Selected animals were transported to a slaughterhouse located 200 km from the rabbit farm. After removing the rabbits from the cages and pens they were slaughtered within 6 h. The slaughtering and carcass dissection procedures followed the recommendations of the World Rabbit Science Association (WRSA), described by Blasco and Ouhayoun (1996). At the slaughterhouse, rabbits were weighed (SW), electrically stunned and bled. Then, the skin, genitals, urinary bladder, gastrointestinal tract and the distal parts of the legs were removed. Carcasses (with head, thoracic cage organs, liver, kidneys, perirenal and scapular fat) were weighed (hot carcass; HC), then chilled at + 4 °C for 24 h in a ventilated room. After 24 hour chilling, the chilled carcasses (CCs) were weighed. The head, thoracic cage organs (thymus, trachea, esophagus, heart, lungs — LHW), liver and kidneys were removed from each carcass to obtain the reference carcass (RC), which includes the meat, bones and fat depots. The carcasses were then cut between the 7th and 8th thoracic vertebra and between the 6th and 7th lumbar vertebra to obtain the fore, mid, and hind parts, which were weighed separately. Also scapular and perirenal fat was dissected and weighed. The dressing out percentages (HC, CC and RC weight as % of SW) and the ratio of the organs and carcass parts to either the CC or to the RC weight were calculated as required. The Longissimus dorsi (LD) muscle of both sides and muscles of the hind leg (HL) of a randomly selected 15 rabbits per experimental group were separated and individually packed in polyethylene bags, sealed, ice-cooled in portable refrigerators and transported to the Department of Animal Medicine, Production and Health of the University of Padova (Italy) for meat quality analysis. During transportation, the temperature of the samples was maintained at +4 °C. The samples arrived at the Padova Department laboratory at 6.00 pm (36 h postmortem) and left HL and LD muscle were weighed and frozen (−20 °C) until water holding capacity (WHC), Warner–Bratzler shear force (WBSF) on HL, and proximate composition on LD, were determined. The right HL samples were stored in a ventilated refrigerator at +4 °C overnight. At 48 h postmortem the right HL was deboned, and the meat/bone ratio was calculated (Blasco & Ouhayoun, 1996), as well as the HL bone measurements (Section 2.3); then the raw meat was ground and used for heme iron determination. 2.3. Rheological and analytical measurements

Group PW: the elevated platform was made of wire mesh. Fourteen rabbits were placed in each of 9 pens. Stocking density was 16.3 (related to the floor surface), or 10.9 rabbits (including the platform surface) per m2 (n = 126). Group PD: the elevated platform was covered with a 5 cm layer of wheat straw. The straw was replaced weekly and when it was necessary dry straw was added. Fourteen rabbits were housed in each

Immediately after weighing the carcasses, the color of the 155 right LD muscles was measured on the cross section at the level of the 5th lumbar vertebra with a MINOLTA CR-300 colorimeter (light source: D65; L* [lightness], a* [redness] and b* [yellowness]) according to the CIE Lab color system (CIE, 1976). Values corresponded to the average of two measurements on each sample.

Z. Matics et al. / Meat Science 96 (2014) 41–46

The raw femur and tibia bones of the right HL were measured for weight, length (only the femur bone), diameter, and Warner–Bratzler fracture toughness (WBFT). Bone diameter was measured using a dial caliper (±0.02 mm) at the level of minor thickness at the mid-diaphysis corresponding to the breaking point. For the WBFT measurement, the femur bones were submitted to a three-point flexure test conducted with a universal testing machine (Instron 1000). The distance between the two fulcrum points supporting the bones was 45 and 38 mm, for the femur and tibia bones, respectively; the load rate was 5 mm/min. The bones were constantly oriented for testing with their natural convex shape downwards. The flexure attachment provided by Instron was specific for testing bone fracture toughness. Left HL was weighed again either after thawing (for 24 h at +4 °C) and after cooking to determine the thawing loss (as the ratio of thawed weight/48 h postmortem weight), and the cooking loss (the cooked/ thawed weight ratio), respectively. Total loss was represented as a sum of thawing and cooking losses. In order to determine the cooking loss, the HLs were individually packed in sealed bags and cooked in a water bath (core temperature 80 °C; Ouhayoun & Dalle Zotte, 1996) and then the meat was used for the shear force (WBSF) measurements on cores (1.25 cm diameter) sheared perpendicularly to the muscle fiber direction with a Warner– Bratzler cell fitted on a universal testing machine. WBSF was calculated by averaging 6 measurements per sample, representative of the total muscle mass of each hind leg. Right HL meat samples were analyzed for heme iron content as proposed by Hornsey (1956) and expressed as mg/kg of fresh tissue. LD meat was freeze-dried and analyzed for moisture, fat and ash (AOAC, 2000) using methods 950.46, 991.36 and 920.153, respectively. Protein content – including glucidic molecules and their catabolites (0.25%) (Ouhayoun, Delmas, Monin, & Roubiscoul, 1990) – was calculated by difference. 2.4. Statistical analysis Production, slaughter and meat quality traits were first analyzed by means of one-way analysis of variance (GLM) (housing conditions). Preliminary analyses showed that replication had no effect, therefore it was not considered in further analyses. Because the examined traits of the P11 and P16 groups did not differ significantly these two groups were combined (group P). Data of 4 groups (C, P, PW and PD) were statistically analyzed. The GLM model for the analyzed traits was: yijkl ¼ μ þ Ai þ εi where yij = observation j in housing condition i, A (i = 1, 2, 3 and 4), and εij = random error. In the case of feed intake and feed conversion ratio the experimental unit was the cage or pen, but in any other case individual data were analyzed. Mortality was evaluated by Chi2-test. All analyses were performed using SAS 9.1 software packages. 3. Results 3.1. Production traits Pooled results of the 3 replications are summarized in Table 1. Comparing all groups, for the ages of 5–7 and 7–9 weeks the highest average daily gains (ADGs) were found in the C and PW groups, respectively. The worst performances were recorded in the PD rabbits between weeks 5 and 9 (P b 0.05). Considering the whole growing period (5–11 weeks) the ADG of the C, P and PW groups did not differ, but the PD rabbits showed lower growth rates (P b 0.001).

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Table 1 Effect of housing conditions on production traits of growing rabbits. Age, weeks

Cage

C No. of rabbits 120 No. of cages/ 60 pens Body weight, g 5 971 7 1683c 9 2249b 11 2851b Average daily gain, g/day 5–7 48.6c 7–9 42.4a 9–11 42.0 5–11 44.7b Feed intake, g/day 5–7 115b 7–9 146b 9–11 168 5–11 142b

Pens without platform

Pen with platform Wire-net

Deep-litter

P

PW

PD

207 18

126 9

126 9

971 1592b 2187b 2799b

971 1564ab 2187b 2802b

971 1541a 2100a 2698a

42.4b 44.1ab 43.7 43.5b 104a 143ab 174 139ab

40.5ab 46.0b 43.7 43.6b 97a 147ab 171 137ab

38.9a 41.0a 42.8 41.1a 94a 128a 161 127a

Feed conversion ratio 5–7 2.38 7–9 3.50 9–11 4.13 5–11 3.21

2.47 3.29 3.95 3.21

2.37 3.21 3.95 3.16

2.42 3.15 3.79 3.10

Mortality, % 5–7 7–9 9–11 5–11

1.9 3.0ab 1.5 6.3

1.6 4.0ab 1.7 7.1

0.8 7.2b 0.0 7.9

0.8 1.7a 2.6 5.0

SE

P-value

3.50 7.43 9.41 11.5

1.000 b0.001 b0.001 b0.001

0.41 0.47 0.44 0.26

b0.001 0.002 0.478 b0.001

1.60 1.71 1.82 1.32

b0.001 0.024 0.306 0.006

0.02 0.05 0.07 0.02

0.542 0.051 0.465 0.572

NS b0.05 NS NS

a,b,c Means in the same row with different superscripts differ (P b 0.05), NS = not significant; SE: standard error of the mean.

At the age of 7 weeks the C rabbits were the heaviest (P b 0.05), followed by group P, whereas the other groups had similar live weight. At the ages of 9 and 11 weeks the C, P and PW groups had the same BW which was significantly higher than that of the PD rabbits. Differences of FI were registered between the ages of 5–7 (the C rabbits consumed more feed compared to the P, PW and PD groups) and 7–9 and 5–11 weeks (the highest FI was found in group C, and the PD rabbits consumed the least amount of feed, P b 0.05). FCR of the groups did not differ in any period. Mortality ratio showed differences only between the ages of 7 and 9 weeks when a significantly higher mortality rate was observed in group PD compared with group C.

3.2. Carcass traits The ratios of the different body parts and organs compared to slaughter weight (SW), chilled carcass (CC) and reference carcass (RC) weight are shown in Table 2. Dressing out percentages and percentage of head, liver, kidneys and LHW to the CC did not differ among the different experimental groups. Rabbits of the C group had the largest percentage of the mid part when referred to the RC, significant differences were detected when compared to the P and PD groups, however the percentage of m. Longissimus dorsi did not differ among the groups. The percentage of the hind part and hind legs were larger for most of the pen-housed rabbits compared to the C group (P b 0.05), however the performance of the PW group was intermediate. On the contrary, fat depots were higher in caged than in pen-housed rabbits (P b 0.001). The measured and calculated traits of the right HL are presented in Table 3.

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Table 2 Effect of housing conditions on carcass traits (ratio of body parts and organs). Traits

Cage

C No. of rabbits 32 Slaughter 3071b weight (SW), g % SW 62.6 Hot carcass1, g 61.1 Chilled carcass2 (CC), g 50.7 Reference carcass3 (RC), g % CC Head Liver Kidneys LHW4 % RC Fore part5 Mid part5 Hind part5 Hind legs L. dorsi muscle Perirenal fat Scapular fat

Pen without platform

Pen with platform Wire-net

Deep-litter

P

PW

PD

51 2800a

36 2853a

36 2755a

SE

P-value

24.3

b0.001

62.0 60.5

62.6 61.1

61.7 60.2

0.42 0.41

0.845 0.833

50.2

50.7

49.8

0.36

0.796

8.56 5.46 1.07 1.36

8.95 5.14 1.07 1.36

8.81 5.11 1.04 1.35

8.98 5.24 1.06 1.33

0.07 0.07 0.01 0.02

0.219 0.369 0.760 0.908

26.9 34.6b 35.6a 33.9a 11.8 3.11b 0.86b

27.5 33.4a 37.2b 35.4b 12.1 1.96a 0.61a

27.4 33.9ab 36.5ab 34.9b 11.9 2.31a 0.66a

27.2 33.8a 37.1b 35.5b 12.0 2.04a 0.59a

0.11 0.12 0.13 0.13 0.04 0.08 0.02

0.210 0.002 b0.001 b0.001 0.086 b0.001 b0.001

Means in the same row with different superscripts differ (P b 0.05); SE: standard error of the mean. 1 Hot carcass = carcasses with head, thoracic cage organs, liver, kidneys, perirenal and scapular fat. 2 Chilled carcass = hot carcass chilled at +4 °C for 24 h. 3 Reference carcass = chilled carcass without head, thoracic cage organs, liver and kidneys. 4 LHW: thymus, trachea, esophagus, lungs and heart. 5 Fore ,mid and hind parts were separated between the 7th and 8th thoracic vertebra and between the 6th and 7th lumbar vertebra.

No differences were observed for HL weight. The weight and ratio of HL bones, femur and tibia were lowest in group C compared to the pen-housed rabbits (P b 0.05 and P b 0.001). Meat/bone ratio was largest in group C and it exceeded that of the P and PD groups (P b 0.05). Although, no significant differences were recorded for femur length and diameter among the groups, the femur fracture toughness (WBFT) was lower in C and P than PW rabbits (P b 0.05). Rabbits housed in pens with platforms (PW and PD) exhibited significantly thicker tibia than the rabbits in cages (C).

Table 3 Effect of housing conditions on the characteristics of the right hind leg (HL). Cage

C

Pen with platform SE Pen without Wire-net Deep-litter platform P

No. of samples 15 30 Hind leg, g 285 286 Bones, g 30.8a 33.8b Bones, % HL 10.8a 11.8b Meat/bone ratio 8.30b 7.49a Femur, g 12.8a 13.8b Femur, % HL 4.49a 4.84b Femur length, mm 92.4 91.7 Femur smallest ∅, mm 6.50 6.78 Femur WBFT, kg 33.0a 35.3a Tibia, g 8.32a 9.07b Tibia, % HL 2.92a 3.18b Tibia, smallest ∅, mm 5.27a 5.44ab a,b,c

Meat quality characteristics are given in Table 4. The HL meat thawing loss, as well as its WBSF and heme iron content, were similar among experimental groups, however significant differences were found in cooking and total loss between groups C and PD, with higher values in PD rabbits (P b 0.05). Comparing the different groups, the L*, a*, b* values of the LD meat, showed no significant differences. As regards the proximate composition of the LD meat, water, protein and ash contents were similar among groups. The C and P rabbits showed the highest, and PW and PD rabbits the lowest lipid contents (P = 0.051). 4. Discussion

a,b

Traits

3.3. Meat quality traits

PW

PD

15 285 32.8ab 11.5ab 7.72ab 13.7ab 4.83b 91.9 6.87 41.1b 8.97b 3.16b 5.65b

15 275 33.5b 12.3b 7.22a 13.9b 5.09b 92.2 6.87 36.9ab 9.10b 3.34b 5.63b

2.43 0.32 0.12 0.09 0.12 0.04 0.21 0.05 0.80 0.08 0.03 0.04

P-value

0.348 0.006 b0.001 b0.001 0.006 b0.001 0.710 0.057 0.009 0.003 b0.001 0.002

Means in the same row with different superscripts differ (P b 0.05); SE: standard error of the mean.

4.1. Production traits Based on data in the literature (Szendrő & Dalle Zotte, 2011) the ADG of pen-housed rabbits kept on wire net floors is almost always lower than that of rabbits caged in pairs. Although the ADG of group C was not significantly different compared to the P and PW groups between 5 and 11 weeks, these results were similar to several other studies (Dal Bosco et al., 2002; Lambertini et al., 2001; Princz et al., 2009; Szendrő, Princz, et al., 2009). In the present study the ADG of rabbits in group C exceeded that of the P and PW groups by 1.1–1.2 g/day between the ages of 5 and 11 weeks, whereas the previously mentioned authors found a difference of 4.3 g/day on average. The ADG of the PD rabbits, where pens were provided with platforms covered with straw-litter, was significantly lower than that of the other groups between the ages of 5 and 11 weeks because these rabbits may have consumed the litter material on the platform (Dal Bosco et al., 2002; Jekkel & Milisits, 2009; Lambertini et al., 2001), demonstrated by their significantly lower FI. This resulted in the lowest BW. The decrease of the ADG was the same as that of Lambertini et al. (2001) and Trocino et al. (2008) but lower than the value reported by Dal Bosco, Castellini, and Bernardini (2000) and Dal Bosco et al. (2002). Table 4 Effect of housing conditions on meat quality. Traits

No. of samples HL1 Thawing loss, % Cooking loss, % Total loss, % WBSF, kg/cm2 Heme Iron, mg/100 g LD3 Color of LD muscle4 L* value4 a* value4 b* value4 Proximate composition Water, % Protein, % Lipids, % Ash, % a,b

Cage

Pen with platform SE Pen without Wire-net Deep-litter platform

P-value

C

P

PW

PD

15

30

15

15

1.15 0.97 23.0a 24.1ab a 24.5 25.0ab 1.63 1.81 0.18 0.19

1.21 24.5ab 25.7ab 1.75 0.19

1.32 25.2b 26.5b 1.90 0.18

0.06 0.25 0.24 0.04 0.005

0.178 0.031 0.042 0.199 0.887

50.3 50.5 2.52 3.64 0.46 1.02

49.5 3.13 0.89

50.5 3.51 0.89

0.29 0.16 0.09

0.576 0.060 0.178

74.5 74.8 23.5 23.2 0.68 0.68 1.32 1.29

74.9 23.2 0.59 1.30

74.9 23.3 0.54 1.31

0.06 0.05 0.02 0.01

0.168 0.304 0.051 0.624

Means in the same row with different superscripts differ (P b 0.05); SE: standard error of the mean. 1 Hind leg meat. 2 WBFT: Warner–Bratzler fracture toughness, measured on 32, 51, 36 and 36 rabbits for C, P, PW and PD groups, respectively. 3 Longissimus dorsi muscle. 4 L* (lightness), a* (redness) and b* (yellowness) values.

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The BW of 7-week-old rabbits was significantly higher in group C compared to the other groups, whereas the 11-week-old PD rabbits had the poorest BW. These results are in accordance with the literature (see review of Szendrő & Dalle Zotte, 2011), although the differences found were generally smaller than those in other trials (Dal Bosco et al., 2000, 2002; Lambertini et al., 2001; Princz et al., 2009; Szendrő, Princz, et al., 2009). In previous studies (Lang & Hoy, 2011; Wagner, Weirich, & Hoy, 2009) it was observed that there was a high percentage of use of the elevated platform, however this behavior was not confirmed in this study (Szendrő et al., 2012) where, rabbits showed a low platform preference (in the case of wire net and deep litter platform these were 27% and 12%, respectively). This finding explains the smaller decrease in ADG and BW compared to other reports (Dal Bosco et al., 2000, 2002; Lambertini et al., 2001; Trocino et al., 2008). Group size affects not only the locomotory behavior but also the magnitude of stress. The more rabbits are housed in the pen the more lesions caused by aggression can be found on the bodies. The stress from agonistic behavior can affect FI and feed conversion efficiency (Szendrő & Dalle Zotte, 2011). Mortality was only different between the C and PD groups between the ages of 7 and 9 weeks (1.7 and 7.2%, respectively), which was probably caused by the consumption of the soiled litter material and the related digestive diseases (Dal Bosco et al., 2002). When taking into account the whole growing period no significant difference was found in mortality among the various groups. 4.2. Carcass traits No significant differences were observed among the groups for dressing out percentages, in agreement with Dal Bosco et al. (2002); Dalle Zotte, Princz, Metzger, et al. (2009) and Szendrő and Dalle Zotte (2011). However, others (Dal Bosco et al., 2000, 2002; Lambertini et al., 2001; Trocino et al., 2008) observed a significant reduction in dressing out percentage with deep litter use, which was probably caused by litter consumption. Because of the low platform preference (an average of 12%; Szendrő et al., 2012), in this study the rabbits may have consumed less litter material, consequently their dressing out percentage decreased to a lesser extent (0.3–0.9%). The dressing out percentage alone does not characterize the effects of group size or platform utilization because the ratio of certain carcass parts can also change depending on the housing condition. In accordance with several studies, the ratio of the fore part to RC was not significantly different among the groups (Dalle Zotte, Princz, Metzger, et al., 2009; Szendrő, Princz, et al., 2009; Szendrő et al., 2009). The proportion of the mid part to the RC was the largest in C rabbits, and that of the hind part and hind legs were larger in the pen-housed groups. The stronger hind legs of pen-housed rabbits were possibly related to their higher locomotory activity. Similar results were reported on rabbits (Combes, Postollec, Jehl, Canquil, & Carche, 2003; Dal Bosco et al., 2002; Dalle Zotte, Princz, Metzger, et al., 2009; Szendrő, Matics, et al., 2009, Szendrő, Princz, et al., 2009), although, in these studies no significant differences were observed. In poultry the positive relationship between animal locomotory activity and leg breaking strength was found in hens (Jendral, Korver, Church, & Feddes, 2008) but not in broilers when submitted both to a treadmill regime (Foutz, Griffin, Halper, & Rowland, 2007) and to movement around barriers for drinking and feeding (Bizeray, Estevez, Leterrier, & Faure, 2002), even though the latter treatment significantly increased the diameter of the tibia diaphysis, as observed in the present study. Perirenal and scapular fat percentage was larger in caged than in penned rabbits, as previously reported (Combes et al., 2003; Dal Bosco et al., 2002; Dalle Zotte, Princz, Metzger, et al., 2009; Jehl, Meplain, Mirabito, & Combes, 2003; Maertens & Van Oeckel, 2001; Szendrő, Matics, et al., 2009), and it can be explained by their less intense locomotor activity.

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The smaller weight, ratio and diameter of the hind leg bones, femur and tibia, of group C compared to that of the pen-housed rabbits can also be explained by the different locomotory behaviors. Consequently, the rabbits in group C showed the highest meat/bone ratio. Dal Bosco et al. (2002) and Szendrő, Princz, et al. (2009) found similar results but the differences were not significant.

4.3. Meat quality Housing conditions minimally affected the meat quality. No differences were found among the experimental groups for thawing loss, WBSF of HL meat, although WBSF was numerically higher for pen-housed rabbits suggesting that, due to their higher locomotory activity, the meat became tougher. Significant differences were found only in cooking and total loss between C and PD groups. The color values (L*, a*, b*) of the LD meat were not significantly different among the groups. However, based on the contradictory results of different studies (Dal Bosco et al., 2000, 2002; Dalle Zotte, Princz, Metzger, et al., 2009; Paci, Preziuso, D'Agata, Russo, & Dalle Zotte, 2013; Szendrő, Princz, et al., 2009) it can be assumed that the housing conditions do not affect the meat color markedly when commercial rearing periods are adopted. The proximate composition of the LD meat varied among treatments only for lipid content (P = 0.051). The lowest value was found in the PD group, presumably as a result of their lower FI (litter consumption) than their higher locomotory activity, as reported previously (Dal Bosco et al., 2002; Szendrő, Princz, et al., 2009). Rabbit meat may contribute to human iron requirements (Dalle Zotte & Szendrő, 2011). In the present study the content of heme iron ranged from 0.18 to 0.19 mg/100 g in HL of the different groups, similar to that found in rabbit and pork meat (on average 0.25 mg/100 g) by Lombardi-Boccia, Martinez-Dominguez, and Aguzzi (2002). The presumably higher locomotory activity of pen-raised rabbits, due either to the lower number of rabbits/pen or to the presence of an elevated platform, did not increase the iron content in the meat related to a probable fast-to-slow transition in contractile myofiber characteristics. According to Gondret, Combes, Lefaucheur, and Lebret (2005) there is a threshold for induction of the adaptation process depending on exercise intensity.

5. Conclusions It can be concluded that some differences can occur in the production, carcass and meat quality traits of rabbits housed in cages (2 rabbits/cage) or in pens (group). No substantial difference was detected between the groups housed with and without platforms, and compared to previous results, relatively small differences were found between the wire mesh and deep litter platforms. It seems that utilization of a platform does not involve such a difference in activity that would alter the production, carcass and meat quality traits. The use of pens with platforms is suitable for increasing the basic area so there is an increased possibility of the rabbits carrying out locomotory behaviors. The platform with deep litter can be an alternative housing system, despite the slight decrease in some production, carcass and meat quality traits of the rabbits, compared to those reared in conventional pens.

Acknowledgment The financial help of TECH_08_A3/2-2008-0384 (NDA, National Development Agency) is gratefully acknowledged. The study was also supported by the MAE “XVII Executive Program of S&T Cooperation between Italy and Hungary 2008–2010” http://www.esteri.it/MAE/doc/ PE-ST-UNGHERIA-2008-2010.rtf.

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