Effect of an outdoor rearing system on the welfare, growth performance, carcass and meat quality of a slow-growing rabbit population

Meat Science 83 (2009) 691–696

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Meat Science

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Effect of an outdoor rearing system on the welfare, growth performance,carcass and meat quality of a slow-growing rabbit population

M. D’Agata a, G. Preziuso a, C. Russo a, A. Dalle Zotte b, E. Mourvaki c, G. Paci a,*

a Department of Animal Production, University of Pisa, Viale Piagge 2, 56100 Pisa, Italyb Department of Animal Science, University of Padova, Agripolis, Viale dell’Università 16, 35020 Legnaro, Padova, Italyc Department of Applied Biology, University of Perugia, Borgo XX Giugno 74, 60123 Perugia, Italy

a r t i c l e i n f o a b s t r a c t

Article history:Received 2 March 2009Received in revised form 29 July 2009Accepted 3 August 2009

Keywords:RabbitOutdoor rearing systemAntioxidant enzymesMeat qualityFatty acid profile

0309-1740/$ - see front matter � 2009 Elsevier Ltd. Adoi:10.1016/j.meatsci.2009.08.005

* Corresponding author. Tel.: +39 050 2216903; faxE-mail address: [email protected] (G. Paci).

The effect of Outdoor or Indoor housing systems on the growth, welfare and carcass and meat quality of alocal rabbit population was investigated. The slaughter age was 103 ± 2 days. Open-field tests showed aneffective capacity of the Outdoor group to combat stressors. Compared to Indoor rabbits, Outdoor rabbitsshowed better growth performance and higher slaughter weight (SW) (2535 vs 2137 g; P < 0.01). Outdoorhousing conditions increased the physical activity of rabbits and their hind legs were more developed(36.1% vs 34.9%; P < 0.01). Slaughter yield was lower in Outdoor rabbits (57.8% vs 58.4% SW; P < 0.05)due to the higher skin proportion (17.2% vs 15.6% SW; P < 0.05). Outdoor rabbit meat showed lower L*

value (L. lumborum: 55.6 vs 59.2; P < 0.01; B. femoris: 53.0 vs 55.5; P < 0.01) and cooking loss (L. lumbo-rum: 15.9% vs 18.1%; P < 0.05). Outdoor rabbit hind leg meat was characterized by lower water (74.5% vs75.1%; P < 0.01) and higher protein (22.9% vs 22.6%; P < 0.01) and fat (1.4% vs 1.1%; P < 0.01) contents; lip-ids were lower in SFA and higher in MUFA. Outdoor rearing seems to be a possible alternative housingsystem that allays the ethical concerns of modern consumers while also providing good meat quality.

� 2009 Elsevier Ltd. All rights reserved.

1. Introduction

Rabbit meat has long been appreciated in Mediterranean coun-tries and the consumption trend depends on changes in the life-styles of consumers and their interest in products obtained byalternative rearing systems that should assure higher standardsof animal welfare along with high meat quality. In consequence,interest in obtaining rabbit meat from less intensive rearing sys-tems has increased in the last decade. Rabbit welfare can be safe-guarded by different management systems. Although severalauthors have studied the effect of alternative rearing systems onthe live performance, behaviour, oxidative stress and carcass andmeat quality of rabbits grown in either intensive or extensive con-ditions, most have used hybrids or genetic lines selected for fastgrowth (Cavani et al., 2004; Dal Bosco, Castellini, & Bernardini,2000; Dalle Zotte et al., 2009; Lambertini, Vignola, & Zaghini,2001; Metzger et al., 2003; Paci et al., 2005; Pla, 2008; Princzet al., 2009; Xiccato et al., 1999).

In light of the high variability of environmental conditions,when alternative housing systems are adopted, local breeds orpopulations are better suited than commercial hybrids because oftheir high adaptability to unfavourable environmental conditions

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: +39 050 2216901.

(Lambertini, Vignola, Paci, Morittu, & Zaghini, 2006), whereas com-mercial hybrids show reduced ability to cope with decreased im-mune-competence and increased susceptibility to environmentalstress (McNitt, Way, Way, & Forrester-Anderson, 2003). Because lo-cal genotypes are also characterized by slow growth rates and car-cass weight is fixed by the market, these rabbits are slaughtered atan older age with all the advantages offered by more matureanimals.

The aim of this study was to investigate the effect of two hous-ing systems (Outdoor vs Indoor) on the productive performance,welfare, carcass and meat quality of a local rabbit population char-acterized by slow growth.

2. Materials and methods

2.1. Animal and housing system

Grey coloured local rabbits (agouti or wild-type) were utilized:this rabbit population has been reared for more than thirty years inseveral small sized farms in central Italy (Tuscany). At the Pisa Uni-versity Rabbitry Station where the study was carried out, about 20females and 10 males, representative of this local population, werebred for ten years. This population had the following characteris-tics: high rusticity, fertility about 90%, total born/delivery 8.2 ±2.8n, adult live weight 4000 ± 100 g (male) and 3400 ± 200 g

692 M. D’Agata et al. / Meat Science 83 (2009) 691–696

(female), weaning weight 890 ± 155 g (35d), slaughter weight2500 ± 300 g, and carcass weight about 60% (Lambertini et al.,2006; Paci, Lisi, Cini, & Bagliacca, 2004).

Seventy-six weaned rabbits 35 days old with average weight of840 g were used. Up to 57 days of age, the rabbits were reared incolony cages (cm 65 � 40 � 32 h) at a density of 15 rabbits/m2

(4 animals/cage) in a forced-ventilation rabbitry and given a pel-leted feed and alfalfa hay ad libitum. Afterwards, 48 of the rabbitswere divided into two groups of 24 of similar average live weightas follows: an ‘‘Indoor group”, housed in 6 colony cages sized as de-scribed above, and an ‘‘Outdoor group”, housed in 3 wire net floorcolony cages (cm 100 � 150 � 76 h), at a density of 5 rabbits/m2

(8 animals/cage) in an outdoor pen built to provide the animalswith protection against predators and shelter from sun and rain.The study was conducted during the winter with daily averagetemperatures of 12 and 9 �C Indoor and Outdoor, respectively. Col-ony cages were equipped with feeders and nipple drinkers. Rabbitsreceived the same dietary treatment throughout the study until103 ± 2 days of age. From 57 to 103 days of age, individual liveweights and cage feed intakes of the pelleted diets and alfalfahay were recorded every week and the feed to gain ratiocalculated.

2.2. Behavioural tests and oxidative stress

To evaluate animal welfare, all rabbits underwent Tonic Immo-bility (TI) and Open Field (OF) tests at the ages of 90 and 97 days,respectively. TI is defined as a state of motor inhibition and areduction of response to external stimuli induced by fear obtainedby a brief period of physical restraint: this response is naturallyused by animals when they are captured by a predator. The TI testwas conducted by placing the rabbit upside down in a V-shapedwooden cradle with its head hanging over the edge and restrainedfor 50 s with one hand placed on the sternum and the other handcovering the head. A trained operator applied a pressure propor-tional to the rabbit’s resistance by hand, and this pressure wasgradually decreased: if the rabbit still moved, the induction wasconsidered unsuccessful and a other induction period started, ifthe rabbit remained immobile a chronometer was activated tomeasure the duration (in seconds) of the response, which endedwhen the rabbit resumed the upright position; the maximumduration of the test was 180 s. The test was repeated a maximumthree times: if the rabbit moved during all inductions, the TI testwas scored as 0 and the number of inductions was consideredequal to 3 (Zucca, Bonazza, Heinzl, Luzi, & Verga, 2008).

The OF test is widely used to assess fear and novelty response indomestic species: the OF equipment consisted of a square enclo-sure (100 � 100 cm) with paperboard walls and a rubber floor di-vided into nine squares (33 � 33 cm each) by perpendicular linesand marked by numbers. The light source illuminated the areaequally. Each rabbit was placed in an enclosed box outside the areabut communicating with it by a sliding opening: after 1 min, thebox was opened and the time required for the rabbit’s first move-ment was recorded as latency time (s) while the time spent be-tween the opening of the box and the first active escape was alsomeasured. Escape attempts, movement at the sides or in the centreof the square enclosure, and total activities were observed andmeasured as frequencies (f). The behaviours recorded measuredas frequencies and expressed as percentage of total activity were:digging (scratching with the forelegs on the floor or wall), box bit-ing, rearing (forefeet raised from the floor, the rabbit stands on itsheels), exploration (head movements indicating investigation ofthe environment), hitting (alarm behaviour, the hind feet arethumped on the floor), and sitting up (rear end and forepaws onfloor with forelimbs straight) (Ferrante, Verga, Canali, & Mattiello,1992; Meijsser, Kersten, Wiepkema, & Metz, 1989).

To study oxidative stress, blood samples were collected inEDTA-K tubes from the ear vein of rabbits aged 100 days. The anti-oxidant status and oxidative stress markers analyzed on erythro-cytes were superoxide dismutase (SOD), catalase (CAT),glutathione peroxidase (GPx) and thiobarbituric acid reactive sub-stances (TBARS). One ml of blood was centrifuged (1000�g for15 min) and the cells were washed three times in saline solution;the erythrocytes were lysed by hypotonic buffer (pH 7.4) and cen-trifuged (2500�g for 15 min). SOD activity was analyzed on sam-ples obtained in this way by the Flohe and Otting method(1984); CAT and GPx activities and TBARS were determined usinga commercial kit (Randox Laboratories Ltd., Crumlin UK).

2.3. Slaughter traits and muscle sampling

At 103 ± 2 days of age, 20 rabbits per group were weighed (SW),electrically stunned, and slaughtered. The slaughtering and carcassdissection procedures followed the World Rabbit Science Associa-tion (WRSA) recommendations described by Blasco and Ouhayoun(1996). The slaughtered rabbits were bled, and then the skin, gen-itals, urinary bladder, gastrointestinal tract and the distal part oflegs were removed. Carcasses (with head, thoracic cage organs, li-ver, kidneys, perirenal and scapular fat) were weighed (hot car-cass), then chilled at +4 �C for 24 h in a ventilated room. Thechilled carcasses (CC) were weighed and the drip loss percentagecalculated. The head, thymus, trachea, oesophagus, heart, lungs, li-ver and kidneys were removed from each carcass to obtain the ref-erence carcass (RC). The slaughter yield (CC weight as percentageof SW) and the ratio of the organs and carcass parts to either theCC or to the RC weight were calculated as required. The RC was di-vided into joints: left and right hind legs (HL), and loin region (be-tween the first and the seventh lumbar vertebrae) according to Plaand Dalle Zotte recommendations (2000). The left HL was carefullydeboned and the meat to bone ratio calculated (Blasco & Ouha-youn, 1996) whereas the right HL and both sides of the Longissimuslumborum (LL) muscle were used for meat quality determinations.

2.4. Meat quality parameters

The ultimate pH (pHu) was determined in situ on the LL muscleat the level of the 5th lumbar vertebra and on the Biceps femoris(BF) muscle with a portable pH-meter (Hanna) equipped with aglass electrode (3 mm diameter conic tip) suitable for meatpenetration.

At 24 h post mortem, instrumental meat colour expressed as L*

(lightness), a* (redness), and b* (yellowness) according to CIElabsystem (CIE, Commission Internationale de l’Eclairage, 1976) wasmeasured with a Minolta CR300 chromameter (Minolta, Osaka, Ja-pan) on a transversal section of the LL muscle and on the BF musclesurface; the illuminant was D65 with an incident angle of 0. Valuescorresponded to the average of three measurements per sample.

Water holding capacity (WHC) was determined according to thefilter paper press method on both the LL and BF muscles, and ex-pressed as the ratio of meat area to total area (M/T ratio) after com-pression (50 kg/cm2) of 300 ± 5 mg of meat for 5 min (Grau &Hamm, 1957); WHC was also measured as drip loss and cookingloss (AMSA, 1995; Honikel, 1998) on six samples of LL muscleper experimental group.

The raw meat from the left HL was ground and scanned induplicate by Near Infrared Reflectance Spectroscopy (NIRS) usinga Foss NIRSystems 5000 system. Ten samples were selected byNIR for proximate composition (AOAC, 1995) and fatty acids (FA)profile analyses. For this purpose, the samples were frozen andfreeze-dried.

Chemical data were processed by WINISI software to improve aprevious calibration set and to predict the proximate composition

Table 1Effect of housing system on productive performances.

Indoor Outdoor P

Initial rabbits, No. 24 24Live weight (57 d), g 1235 ± 37.9 1311 ± 41.2 nsMortality, No. 4 1Final rabbits, No. 20 23Live weight (103 d), g 2103 ± 68.6 B 2485 ± 60.3 A **

Daily weight gain, g/d 19.0 ± 1.27 B 26.3 ± 1.12 A **

Cages, No. 6 3

Feed intakeComplete feed, g/d 75.0 ± 5.59 B 117.3 ± 8.54 A **

Alfa–alfa hay, g/d 19.2 ± 2.25 B 33.3 ± 3.44 A **

Total, g/d 94.1 ± 7.38 B 150.6 ± 11.27 A **

Feed to gain ratio 5.1 ± 0.23 5.8 ± 0.35 ns

±: Standard error of the least squares means.A, B: means with unlike superscripts within row differ.ns: non significant.** Significant at the level of P < 0.01.

M. D’Agata et al. / Meat Science 83 (2009) 691–696 693

and the FA profile of the non-chemically analyzed samples (Ber-zaghi, Dalle Zotte, Jansson, & Andrighetto, 2005; Dalle Zotte, Ber-zaghi, Jansson, & Andrighetto, 2006). The calibration andvalidation statistics for proximate composition and FA profile arereported elsewhere (Dalle Zotte et al., 2008).

Protein content – including glucidic molecules and their catabo-lites (0.25%) (Ouhayoun, Delmas, Monin, & Roubiscoul, 1990) – wascalculated by difference in accordance with A.O.A.C. standards(1995).

The FA profile was analyzed by Gas Chromatography after Folchextraction (Folch, Lees, & Sloane Stanley, 1957). Transmethylationwas carried out using a blend of methanol, benzene and sulphuricacid (75:25:4). Gas liquid chromatography was performed on anautomated apparatus (CE 8000 Top, Thermoquest, Milan, Italy)equipped with flame ionisation detector and a Supelco Omegawax250 type capillary column (30 m � 0.25 mm ID). The characteristicoperating conditions were the following: injector temperature:250 �C, detector temperature: 250 �C; hydrogen flow: 1.60 ml/min (linear velocity: 40.22 cm/s at 200 �C). Fatty acids (FA) wereidentified by comparing their retention times to those of authenticFA methyl ester standards (Mix C4–24, 18919–1AMP, Supelco,Bellefonte, PA, USA). Results were expressed as a percentage (w/w) of total FA methyl esters.

TBARS (thiobarbituric acid reactive substances) were measuredon the meat from the left HL using the following method: 5 g ofminced muscle were homogenized with 15 ml of a TCA solution(trichloroacetic acid) and DTPA (Diethylenetriaminepentaceticacid) in distilled water for two minutes. After distillation, 4 ml ofdistilled were added to 4 ml TBA reagent, heated in a boiling waterfor 60 min, and then cooled under running tap water for 10 min.Absorbance was measured at 532 nm against a blank. Lipid oxida-tion products were quantified as malondialdehyde equivalents(mg/kg of muscle) (Ke, Ackman, Linke, & Nash, 1977; Tarladgis,Watts, & Younathan, 1960).

2.5. Statistical analysis

Data were analyzed by analysis of variance, considering therearing system as the main categorical factor nested within cage;slaughter traits were analyzed as weight and expressed as percent-age and covaried for the reference variable whenever significant.Statistical significance of differences was assessed by the t-test(SAS, 2002). Data of Tonic Immobility and Open-Field tests wereanalyzed using a non-parametric analysis of variance (Wilcoxon-Kruskall-Wallis tests).

3. Results and discussion

3.1. Performance

Live performance is reported in Table 1. Rabbits reared Out-doors showed the best performance, were able to overcome thedigestive disorders that occurred during the study, and alsoshowed lower mortality. In fact, four Indoor group rabbits andone Outdoor group rabbit died during the trial after 57 d: thiswas probably due either to the better sanitary conditions in theopen-air environment or the Outdoor system’s greater spaceavailability.

These two conditions could have improved animal welfare andconsequently health, as observed by Cozzi et al. (2000) in calves.

3.2. Behavioural tests and oxidative stress

The two housing systems did not appear to induce statisticaldifferences in TI induction or duration (Table 2). The Open-Field

(OF) test demonstrated the lower fear level in Outdoor rabbitsmore clearly compared to Indoor rabbits, Outdoor rabbits exhib-ited higher digging activity (26.9% vs 20.8%; P < 0.05) and escapeattempts (0.9% vs 0.6%; P < 0.05) and lower biting activity (0.1%vs 1.6%; P < 0.01) (Table 2). As reported by others (Ferrante et al.,1992; Meijsser et al., 1989), this response could be considered apositive reaction to a new environment.

The Outdoor-reared animals, which were probably exposed togreater numbers of strange stimuli and were reared at a lowerstocking density, appeared to be less emotional, and therefore ap-peared better adapted to combat stressors (Hansen & Berthelsen,2000). On the contrary, rabbits reared conventionally showedgreater sensitivity to stress and reacted to environmental stimuliwith passive responses that were probably related to overcrowding(Ferrante et al., 1992; Verga, Ferrante, & Norcen, 1994).

The housing system did not affect significantly the in vivo anti-oxidant status (Table 3).

3.3. Carcass and meat quality

Outdoor rabbits had higher slaughter weights than Indoor rab-bits (2535 g vs 2137 g; P < 0.01) (Table 4). Outdoor housing pro-vided rabbits with lower slaughter yield (57.8% vs 58.4%;P < 0.05) mainly due to the higher skin percentage (17.2% vs15.6%; P < 0.05) ascribed to the different environmental conditionsin the two systems.

Drip loss was significantly lower (2.1% vs 2.4%; P < 0.05) in Out-door rabbits, and probably linked to the higher carcass fatnessaccumulated to withstand the cold season. The perirenal fat con-tent was only slightly higher in Outdoor rabbits (1.4% vs 0.8%RC), even if the significantly higher fat content of the HL meat(1.4% vs 1.1%; P < 0.05; Table 6) would appear to suggest generallyhigher carcass fatness.

Despite the lower slaughter yield found in Outdoor rabbits,their reference carcass percentage (RC%) was significantly higher(83.9% vs 82.1%; P < 0.01), while head (P < 0.01) and liver(P < 0.05) were significantly lower.

HL incidence (% RC) was significantly higher in Outdoor rabbits(36.1% vs 34.9%; P < 0.01), possibly as a result of the greater loco-motory activity promoted by lower stocking density (Dal Bosco,Castellini, & Mugnai, 2002; Dal Bosco et al., 2000; Pla, 2008). Gond-ret, Hernandez, Rémignon, and Combes (2009) have proved thatwhen submitted to jump exercise for about 5 weeks, growing rab-bits show a significant increase in the hind part of the body com-pared to rabbits not subjected to exercise.

Table 2Effect of housing system on behavioural tests: Tonic Immobility test and Open-Field test.

Variable Indoor Outdoor P

Rabbits, No. 20 23

Tonic immobility testInductions, frequency 1.5 ± 0.30 1.1 ± 0.33 nsDurations, time, s 54.2 ± 12.37 29.0 ± 15.76 ns

Open-field test:Latency time, s 32.6 ± 6.44 18.9 ± 5.99 nsBox exit-escape attempt time, s 38.7 ± 6.19 32.6 ± 5.31 nsEscape attempt, frequency 0.6 ± 0.09 b 0.9 ± 0.09 a *

Movement at side, frequency 35.2 ± 1.99 31.2 ± 1.85 nsMovement in centre, frequency 4.6 ± 0.64 4.6 ± 0.60 nsTotal activity, frequency 33.1 ± 2.82 30.5 ± 2.69 nsDigging, % total activity 20.8 ± 2.27 b 26.9 ± 2.11 a *

Biting, % total activity 1.6 ± 0.37 a 0.1 ± 0.35 b **

Rearing, % total activity 11.5 ± 2.32 8.3 ± 2.16 nsExploration, % total activity 39.5 ± 1.63 42.3 ± 1.51 nsHitting, % total activity 1.5 ± 0.55 1.4 ± 0.51 nsSitting, % total activity 25.2 ± 2.93 20.9 ± 2.72 ns

±: Standard error of the least squares means.a, b Means with unlike superscripts within row differ.ns: Non significant.* Significant at the level of P < 0.05.** Significant at the level of P < 0.01.

Table 3Effect of housing system on antioxidant activity and lipid oxidation of rabbit bloodsamples.

Variable Indoor Outdoor P

Samples, No. 20 23SOD, U/mg Hgb 1.63 ± 0.086 1.70 ± 0.079 nsCAT, U/mg Hgb 0.96 ± 0.053 1.00 ± 0.048 nsGPx, U/g Hgb 17.55 ± 1.110 18.95 ± 1.018 nsTBARS, Pmol MDA/mg Hgb 3.74 ± 0.165 3.67 ± 0.151 ns

±: Standard error of the least squares means.ns: Non significant.

Table 4Effect of housing system on slaughter traits.

Variable Indoor Outdoor P

Rabbits, No. 20 20Slaughter weight (SW), g 2137 ± 40.3 b 2535 ± 36.0 a **

Skin, % SW 15.6 ± 0.19 b 17.2 ± 0.17 a *

Full gastrointestinal tract, % SW 19.8 ± 0.29 18.9 ± 0.26 nsHot carcass (HC), % SW 61.1 ± 0.43 a 60.4 ± 0.42 b *

Slaughter yield, % SW 58.4 ± 0.37 a 57.8 ± 0.36 b *

Drip loss, % 2.4 ± 0.24 a 2.1 ± 0.23 b *

Head, % CC 10.0 ± 0.15 a 9.0 ± 0.15 b *

Liver, % CC 5.0 ± 0.16 a 4.2 ± 0.16 b **

Kidney, % CC 1.0 ± 0.02 1.0 ± 0.02 nsReference carcass (RC), % SW 82.1 ± 0.24 b 83.9 ± 0.23 a **

Perirenal fat, % RC 0.8 ± 0.19 1.4 ± 0.18 nsLoin, % RC 24.4 ± 0.25 24.8 ± 0.25 nsHind leg, % RC 34.9 ± 0.24 b 36.1 ± 0.24 a **

Hind leg meat to bone ratio 4.3 ± 0.13 4.4 ± 0.12 ns

±: Standard error of the least squares means.a, b Means with unlike superscripts within row differ.ns: Non significant.* Significant at the level of P < 0.05.** Significant at the level of P < 0.01.

Table 5Effect of housing system on meat quality traits of Longissimus lumborum (LL) andBiceps femoris (BF) muscles.

Variable Indoor Outdoor P

Rabbits, No. 20 20

LL musclepHu 5.70 ± 0.051 5.83 ± 0.046 nsL* 59.15 ± 0.513 a 55.59 ± 0.459 b **

a* 2.08 ± 0.269 2.46 ± 0.240 nsb* 1.63 ± 0.198 1.81 ± 0.177 nsM/T2 0.46 ± 0.030 0.51 ± 0.028 nsDrip loss, % 2.52 ± 0.199 2.47 ± 0.207 nsCooking loss, % 18.14 ± 0.667 a 15.86 ± 0.696 b *

BF musclepHu 5.92 ± 0.037 5.90 ± 0.033 nsL* 55.50 ± 0.561 a 53.01 ± 0.502 b **

a* 2.20 ± 0.234 2.79 ± 0.209 nsb* 2.02 ± 0.137 2.28 ± 0.123 nsM/T2 0.45 ± 0.032 0.49 ± 0.029 ns

±: Standard error of the least squares means.a, b Means with unlike superscripts within row differ.ns: Non significant.* Significant at the level of P < 0.05.** Significant at the level of P < 0.01.

694 M. D’Agata et al. / Meat Science 83 (2009) 691–696

Meat quality traits are shown in Table 5. The pHu measured inLL and BF muscles was not affected by the housing system. This re-sult is in disagreement with other studies in which significant meatpHu differences were ascribed to voluntary exercise and open-airhousing (Cavani et al., 2000; Combes, Moussa, Gondret, Doutre-loux, & Remignon, 2005; Dal Bosco et al., 2002; Dalle Zotte & Ouha-youn, 1995; Paci et al., 2005).

As regards L*a*b* colour values, the LL and BF muscles of rabbitsreared Outdoor exhibited lower L* than those of rabbits reared In-door (55.6 vs 59.2 and 53.0 vs 55.5, respectively; P = 0.01). In thesame muscles, the a* value tended to be greater in Outdoor rabbitsthan Indoor rabbits, particularly in the BF muscle (2.8 vs 2.2), indi-cating an increase in muscle oxidative metabolism mainly attribut-able to increased animal locomotory activity (Gregory, 2003;Ouhayoun, 1998; Paci et al., 2005; Pla, 2008).

Among the three methods of water holding capacity (WHC), thefilter paper press method (M/T) and the drip loss determination inLL and BF muscles did not show differences attributable to thehousing system. Only the cooking loss of the LL muscle was lowerin Outdoor compared with Indoor rabbits (15.9% vs 18.1%;P < 0.05). This positive result together with the lower drip loss, sug-gests Outdoor rabbits could offer advantages to consumers interms of preserved weight and nutritional quality or certain sen-sory attributes.

Table 7Effect of housing system on hind leg meat fatty acid (FA) profile (% of total FA).

Variable Indoor Outdoor P

C10:0 0.13 ± 0.025 0.12 ± 0.022 nsC12:0 0.13 ± 0.022 0.13 ± 0.020 nsC14:0 1.46 ± 0.045 1.56 ± 0.041 nsC15:0 0.52 ± 0.005 a 0.51 ± 0.004 b *

C16:0 26.61 ± 0.513 25.70 ± 0.459 nsC17:0 0.74 ± 0.009 0.72 ± 0.008 nsC18:0 8.19 ± 0.112 8.22 ± 0.100 nsC20:0 0.13 ± 0.002 0.12 ± 0.002 nsTotal SFA1 37.85 ± 0.522 a 36.42 ± 0.467 b *

C14:1 0.04 ± 0.006 b 0.06 ± 0.005 a **

C16:1 1.55 ± 0.096 b 1.83 ± 0.086 a *

C17:1 0.20 ± 0.007 0.21 ± 0.007 nsC18:1 n�9 18.13 ± 0.332 b 19.31 ± 0.297 a *

C18:1 n�7 1.52 ± 0.011 1.51 ± 0.010 nsC20:1 n�9 0.22 ± 0.004 0.22 ± 0.004 nsTotal MUFA2 21.94 ± 0.323 B 23.22 ± 0.289 a **

C18:2 n�6 28.07 ± 0.383 27.77 ± 0.343 nsC18:3 n�6 0.05 ± 0.002 0.05 ± 0.001 nsC18:3 n�3 1.73 ± 0.100 1.75 ± 0.089 nsC20:2 n�6 0.28 ± 0.006 0.29 ± 0.005 nsC20:3 n�6 0.33 ± 0.008 0.32 ± 0.007 nsC20:3 n�3 0.08 ± 0.012 0.08 ± 0.011 nsC20:4 n�6 4.21 ± 0.146 a 3.73 ± 0.131 b *

C22:5 n�3 0.65 ± 0.028 a 0.57 ± 0.025 b *

Total PUFA3 34.74 ± 0.455 34.18 ± 0.407 nsPUFA/SFA 0.92 ± 0.022 0.94 ± 0.019 nsUFA4/SFA 1.50 ± 0.030 1.58 ± 0.027 nsn�6/n�3 10.52 ± 0.424 10.57 ± 0.379 ns

±: Standard error of the least squares means.a, b Means with unlike superscripts within row differ.ns: Non significant.* Significant at the level of P < 0.05.** Significant at the level of P < 0.01.

1 SFA: saturated FA.2 MUFA: monounsaturated FA.3 PUFA: polyunsaturated FA.4 UFA: unsaturated FA.

Table 6Effect of housing system on chemical composition of hind leg meat.

Variable Indoor Outdoor P

Samples, No. 20 20Water, % 75.12 ± 0.106 a 74.45 ± 0.095 b **

Protein, % 22.57 ± 0.074 b 22.94 ± 0.066 a **

Lipids, % 1.12 ± 0.071 b 1.40 ± 0.063 a **

Ash, % 1.20 ± 0.007 1.21 ± 0.006 nsTBARS, mg MDA/kg 0.40 ± 0.011 0.43 ± 0.011 ns

±: Standard error of the least squares means.a, b Means with unlike superscripts within row differ.*: Significant at the level of P < 0.05.ns: Non significant.** Significant at the level of P < 0.01.

M. D’Agata et al. / Meat Science 83 (2009) 691–696 695

The proximate composition of the HL meat (Table 6) indicatesthat the housing system significantly affected water (P < 0.01), pro-tein (P < 0.01) and lipid contents (P < 0.05): water content was low-er, whereas protein and lipids were higher in Outdoor than inIndoor rabbit meat (74.5% vs 75.1%, 22.9% vs 22.6% and 1.4% vs1.1%, respectively). The study underlines the excellent nutritive va-lue (high in protein and low in lipid) of the meat from this localrabbit population compared to that of hybrids and genetic lines se-lected for commercial meat production (Combes & Dalle Zotte,2005; Dalle Zotte, 2004; Dalle Zotte et al., 2009; Pla, 2008). TBARSvalues of the HL meat were similar between the two housingsystems.

The fatty acid (FA) composition of the HL meat is reported inTable 7. The meat derived from the Outdoor rabbits had a lower

fraction of saturated FA (SFA; 36.4% vs 37.9%; P < 0.05) and a higherfraction of monounsaturated FA (MUFA; 23.2% vs 21.9%; P < 0.01)than that of Indoor rabbits. As regards polyunsaturated FA (PUFA),Indoor rabbits showed significantly higher values for C20:4 n�6and C22:5 n�3 than Outdoor rabbits (4.2 vs 3.7 and 0.7 vs 0.6P < 0.05, respectively). The differences observed could be due tothe lower amount of intramuscular fat and hence to the greaterpercentage of phospholipids, which are richer in PUFA, particularlyC20 and C22 (Dal Bosco et al., 2002).

4. Conclusions

The Outdoor rearing system may be considered a favourablealternative housing system because it satisfies the specific require-ments of rabbits and also allays the ethical concerns of modernconsumers: behavioural tests showed that the better sanitary con-ditions, greater space available, and both the quantity and variabil-ity of environmental stimuli improved animal welfare. The morespace available and the greater freedom of movement leads to anincrease in physical activity that positively affects live perfor-mance, carcass meatiness and certain meat quality traits: the meatfrom Outdoor-housed rabbits appears less pale and has a higher li-pid content that is linked to reduced cooking loss. Moreover, theOutdoor housing system seems to reduce the SFA content and toincrease the MUFA level in the HL meat.

Acknowledgements

The research was supported by funding from Fondazione Cassadi Risparmio di Pisa and Ricerca Scientifica di Ateneo – Ex 60%(60A08-5085/07).

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