animal
Animal (2013), 7:10, pp 1600–1606 & The Animal Consortium 2013 doi:10.1017/S1751731113001146
Effects of water restriction on growth performance, feed nutrient digestibility, carcass and meat traits of rabbits F. Bovera1, A. Lestingi2-, G. Piccolo1, F. Iannaccone1, Y. A. Attia3,4 and A. Tateo2 1
Department of Veterinary Medicine and Animal Science, University of Napoli Federico II, Via F. Delpino 1, 80137 Napoli, Italy; 2Department of Veterinary Medicine, University of Bari Aldo Moro, S.P. Casamassima km 3, 70010 Valenzano (Ba), Italy; 3Arid Land Agriculture Department, Faculty of Meteorology, Environment and Arid Land Agriculture, King Abdulaziz University, PO Box 80208, Jeddah 21589, Saudi Arabia; 4Animal and Poultry Production Department, Faculty of Agriculture, Damanhour University, Damanhour 22516, Egypt
(Received 1 October 2012; Accepted 19 April 2013; First published online 28 June 2013)
The study investigates the effects of a post-weaning water restriction on performance, nutrient digestibility, carcass traits and meat quality of 84-day-old rabbits. A total of 1388 weaned rabbits (35 days) were randomly divided into two groups on the basis of BW and sex. The two groups were fed the same diets ad libitum both in the post-weaning (35 to 60 days) and fattening (61 to 84 days) periods. In the post-weaning period, one group (AL) also received drinking water ad libitum, whereas the other (WR) had a water restriction from 35 to 41 days 2 h/day; from 42 to 48 days 2.5 h/day; from 49 to 55 days 3 h/day; and from 56 to 60 days 4 h/day. During the fattening period, both groups had water-free access. Individual live weights and feed intake per cage were recorded weekly for 32 cages randomly chosen per group (64 rabbits) to calculate the BW gain, feed intake and feed conversion ratio (FCR). The apparent digestibility values of nutrients were measured using acid-insoluble ash. Carcass data were collected from 16 rabbits (8 males and 8 females) per group selected for similar final BW in both groups. Mortality from 35 to 60 days was higher in the AL group (10.1% v. 5.2%, for AL and WR, respectively, P , 0.0001). BW gain was higher for the AL group during both the post-weaning (122.4%, P , 0.01) and the entire period (17.5%, P , 0.05). Water restriction reduced feed intake both in the post-weaning (217.4%, P , 0.0001) and in the entire period (29.9%, P , 0.05). During the fattening period, FCR was lower for the WR group (5.15 v. 5.75 g/g, for WR and AL, respectively, P , 0.05). The apparent digestibilities of dry matter, organic matter, NDF, ADF and cellulose were greater in the restricted rabbits (14.7%, 14.5%, 110.2%, 118.8% and 112.8%, P , 0.01, P , 0.01, P , 0.05, P , 0.01, P , 0.05, respectively). Perirenal and scapular fat percentages were higher in the AL rabbits (130.7% and 1116.6%, P , 0.01 and P , 0.001, respectively). Water restriction increased saturated fatty acids (C16:0, 112.9%, P , 0.05), lauroleic acid (C12:1, 175.0%, P , 0.01), n-3 polyunsaturated fatty acids (C20:5, 150.0%, P , 0.01 and C22:5, 116.6%, P , 0.05) and the n-3/n-6 ratio (128.6%, P , 0.05). The applied water restriction between 35 and 60 days executed during the winter months improved the digestive health of rabbits, with no negative effects on carcass traits, or physical and chemical meat characteristics. However, from the animal welfare point of view, a water restriction can be criticized as a method to restrict feed intake. Keywords: carcass traits, digestibility, fatty acid profile of meat, drinking access, rabbit
Implications Alternatives to antibiotics have become important topics in view of the restriction applied by the European Union, owing to the increasing antibiotic resistance of some bacteria. In rabbit breeding, the use of nutrition strategies, such as feed restriction, could improve digestive health. Water restriction is an indirect way to reduce both feed intake and the mortality in the post-weaning period. The confirmation of water restriction as an alternative to antibiotics, without negative -
E-mail:
[email protected]
1600
effects on animal welfare, can reduce the environmental and social impacts of rabbit production, giving greater confidence to consumers, with a positive economic impact for the rabbit industry. Introduction Owing to the potential development of antibiotic-resistant bacteria (Roe and Pillai, 2003), antibiotic growth promoters in feed for farm animals have been banned in the European Union since 2006 (European Union, 2005), and their use is
Water restriction in growing rabbits under consideration around the world. This is a great problem in rabbit production as the Epizootic Rabbit Enteropathy (ERE), a complex enteritis that is the first cause of mortality in the European rabbit industry (Dewree et al., 2003), is responsible for high mortality rate (up to 70%) in the post-weaning period. As ERE can be controlled by using a preventive antibiotic medication, it is very important to identify alternative feeding strategies as replacements for antibiotics. Feed restriction can be used in rabbit production as a strategy to reduce cost and control digestive troubles. Although BW gain, and sometimes the weight at slaughter, is impaired by feed restriction, nutrient digestibility and feed conversion are more favourable in restricted rabbits (Di Meo et al., 2007). Feed restriction can be practically applied by limiting access time to the feeders or reducing the amount of administered feed (Saleh et al., 1996). As the feed intake is directly correlated with the water consumption (Gidenne and Lebas, 2006), recent studies have evaluated the effects of water restriction on digestive health (Boisot et al., 2004; Ben Rayana et al., 2008). In practical conditions, with growing rabbits, the access to drinking water can be limited between 1 and 4 h/day, reducing food intake, mainly as a result of short duration of watering (Gidenne et al., 2010). However, under hot climatic conditions, it is essential that the water restriction is not severe as it can have a negative impact on animal welfare (Gidenne et al., 2012). The aim of our work was to study the effects of a water restriction programme, applied during winter from weaning up to 60 days of age, on rabbit growing performance, nutrient digestibility, carcass and meat traits. Material and methods All procedures involving animals were performed according to the Italian laws on animal welfare in scientific experiments. The trial was conducted at a private rabbit farm (Benevento, Italy; 418160 000 N, 148550 000 E, and 667 m above sea level) during January to February 2011. A total of 1388 weaned hybrid Hyla rabbits (35 days old), with an average initial BW of 954.3 6 67 g, were divided into two treatment groups homogeneous for BW and sex. The rabbits were housed in the same building and placed in cages (26 3 46 3 35 cm). The cages were placed in two different but adjacent rows; the average temperature in the building was 218C 6 28C, and the lighting programme provided 16 h of light. There were two rabbits (one male and one female) in each cage and 347 cages per treatment group. The two treatment groups were fed the same diets ad libitum both in post-weaning (35 to 60 days) and fattening (61 to 84 days) periods. The ingredients and chemical–nutritional characteristics of the diets were reported in Table 1. One treatment group (AL) also received drinking water ad libitum. The other treatment group (WR) had restricted access to drinking water in the post-weaning period (35 to 60 days of age); the time of water distribution was progressively increased according to the increase in animal age and weight as follows: from 35 to 41 days of age 2 h/day (0900 to 1100 h); from 42 to
Table 1 Ingredients and analysed chemical composition of the diets fed to rabbits Item Ingredient composition (%; as-fed basis) Dehydrated alfalfa meal (17% CP) Wheat middlings Alfalfa hay Maize Sunflower meal (30% CP) Sugar cane molasses Toasted soybean meal (44% CP) Calcium carbonate Soybean oil Salt Vitamin–Mineral premix1 Chemical composition (dry matter basis)2 Dry matter (%; as fed) Ash (%) CP (%) Ether extract (%) Crude fibre (%) NDF (%) ADF (%) ADL (%) Cellulose (%) Hemicellulose (%) Digestible energy (MJ/kg dry matter)
Weaning diet
Fattening diet
32.00 29.00 12.00 10.00 8.00 4.00 3.00 1.00 – 0.50 0.50
31.00 30.00 11.00 10.00 8.00 4.00 3.00 1.00 1.00 0.50 0.50
88.67 8.62 17.02 2.86 18.52 42.30 22.80 5.27 17.53 19.50 9.62
89.12 8.35 16.59 4.60 15.35 38.20 19.54 5.09 14.45 18.66 10.30
1 Provided per kilogram of diet; Weaning diet: vitamin A, 8375 IU; vitamin D3, 1000 IU; vitamin E, 20 mg; vitamin K3, 1 mg; vitamin B1, 1 mg; vitamin B2, 2 mg; vitamin B6, 1 mg; nicotinic acid, 20 mg; choline chloride, 250 mg; magnesium, 290 mg; manganese, 20 mg; zinc, 60 mg; iodine, 1.25 mg; iron, 26 mg; copper, 10 mg; cobalt, 0.7 mg; Fattening diet: vitamin A, 6,375 IU; vitamin D3, 750 IU; vitamin E, 20 mg; vitamin K3, 1 mg; vitamin B1, 1 mg; vitamin B2, 2 mg; vitamin B6, 1 mg; nicotinic acid, 20 mg; choline chloride, 250 mg; magnesium, 290 mg; manganese, 20 mg; zinc, 60 mg; iodine, 1.25 mg; iron, 26 mg; copper, 10 mg; cobalt, 0.7 mg. 2 Unless indicated otherwise.
48 days 2.5 h/day (0900 to 1130 h); from 49 to 55 days 3 h/day (0900 to 1200 h); from 56 to 60 days 4 h/day (0900 to 1300 h). During the fattening period in both treatment groups, drinking water was supplied ad libitum. Throughout the experiment, the mortality rate in the groups was recorded daily. Individual live weights and feed intake per cage were recorded weekly for 32 cages randomly chosen per group (64 rabbits) to calculate BW gain, average daily feed intake (ADFI) and the feed conversion ratio (FCR). Each morning, any dead rabbits were removed before feeding, and the cages, in which one or both rabbits had died, were excluded from the experiment. The apparent digestibility values of organic matter (OM), CP, ether extract (EE), crude fibre (CF), NDF, ADF, cellulose and hemicellulose were determined using acid-insoluble ash (AIA) as an inert marker according to Vogtmann et al. (1975). The hard faeces were collected on 3 consecutive days (58 to 60 days of age). Nylon nets (5 3 7 mm mesh) were placed under the same 32 cages used for the growth experiment to separate faeces 1601
Bovera, Lestingi, Piccolo, Iannaccone, Attia and Tateo from urine. At the end of each day, faeces from each cage were collected, discarding caecotrophs, and dried in a draft oven at 608C to a constant weight. Dried faeces were pooled and ,50 g was used for chemical analysis. All animals were slaughtered at 84 days, after around 12 h fasting. Carcass data were collected from 16 rabbits/group (8 males and 8 females), selected to obtain similar final BW in both groups. All procedures followed the World Rabbit Science Association recommendations as described by Blasco and Ouhayoun (1996). The slaughtered rabbits were bled, and then the full gastrointestinal tract, skin, distal legs and tail, and urogenital tract with empty bladder were removed. The carcasses were weighed and then chilled to 48C for 24 h in a ventilated room. After 24 h chilling, the carcasses were weighed and the head, liver, the whole heart, lungs, oesophagus, trachea, thymus gland and kidney free of perirenal fat were removed to obtain the reference carcass. From the reference carcass hind legs were separated.
Physical criteria With a portable instrument (Model HI 9025; Hanna Instruments, Woonsocket, RI, USA) equipped with an electrode (FC 230C; Hanna Instruments), the value of pH after 1 h slaughtering was measured in the Biceps femoris muscle. The left hind leg was used to evaluate the percentage of meat, bone and fat. The crude meat was manually separated from bone and fat, and the meat to bone ratio was calculated as follows: meat/bone 5 (raw hind leg weight 2 bone weight)/bone weight. Instrumental meat colour was measured using a colorimeter (Minolta CR-300, illuminant D65 and 08 observer; Minolta Camera Co., Osaka, Japan) with the Hunter-Lab method by repeating the measurement three times, turning the sample three times by 908 and repeating the procedure at three different places. The instrument was normalized to a standard white tile provided with the instrument before performing analysis (Y 5 92.8, x 5 0.3162 and y 5 0.3322). The colorimetric measurements were taken 24 h post mortem on the samples dissected from the reference carcass on a fresh cut surface, made in the approximate anatomical centre of each m. biceps femoris. The arithmetic mean of the nine recordings obtained from the muscle sample was subjected to statistical analysis. The degree of tenderness was tested through Warner–Bratzler Shear Force (WBSF) on the raw meat from left hind leg. The WBSF was measured (Instron 1140; Instron, High Wycombe, UK) using a crosshead speed of 50 mm/min and a load cell of 50 N. The cut sample had a cylindrical form with a 1.27 cm diameter cut that was parallel to the muscle fibre direction. The force-deformation curve obtained served to calculate meat hardness. Shear forces were determined perpendicular to the fibre direction. Each sample was sheared three times and the arithmetic mean of the recordings obtained from each sample was subjected to statistical analysis. Chemical criteria Chemical analyses of the basal diets and faeces were performed using the following AOAC procedures (2004): Dry 1602
matter (DM, method 934.01), EE (method 920.39), ash (method 942.05), CP (method 954.01), CF (method 945.18), ADF and lignin resistent to acid detergent (ADL; method 973.18) and amylase-treated NDF (method 2002.04). Cellulose and hemicellulose contents were calculated, respectively, as: ADF–ADL and NDF–ADF. The content of AIAs were measured in the basal diets and in the faeces according to Vogtmann et al. (1975). The raw meat from the left hind leg dissection was ground, freeze-dried and analysed using the following AOAC procedures (1984): moisture (method 950.46), fat (method 930.27) and ash (method 950.153). Protein content, including glucidic molecules and their catabolities (0.25%; Bovera et al., 2012) was calculated by difference. Total lipids were extracted from the homogenized left hind leg meat samples using the chloroform/methanol method by Folch et al. (1957). Fatty-acid methyl esters were prepared by transesterification using methanol in the presence of 3% HCl in methanol (vol/vol). Gas–liquid chromatography used an automated apparatus (CE 8000 Top; Thermoquest, Milan, Italy) equipped with a flame ionization detector and a column (Supelco Omegawax 250 type capillary, 30 m length, 0.25 mm i.d. and 0.20 mm film thickness; Sigma-Aldrich, Mila, Italy). The injector and detector temperatures were both 2508C. The hydrogen flow was 1.60 ml/min (linear velocity: 40.22 cm/s at 2008C). Fatty acids (FA) were identified by comparing their retention times with those of known standard FA methyl ester mixtures (Mix C4–24, 18919- 1 AMP; Supelco, Bellafonte, PA, USA). Results were expressed as a percentage (wt/wt) of total FA methyl esters. Atherogenic and thrombogenic indexes were calculated according to Ulbricht and Southgate (1991) as follows: Atherogenic index ¼ ðC 1 2 : 0 þ 4 C 14 : 0 þ C 16 : 0Þ = hX i X X MUFA þ ðn-6Þ þ ðn-3Þ
Thrombogenic index ¼ ðC 14 : 0 þ C 16 : 0 þ C 18 : 0Þ = h X X 0:5 MUFA þ 0:5 ðn-6Þ i X X X þ 3 ðn-3Þ þ ðn-3Þ = ðn-6Þ where monounsaturated fatty acids (MUFAs) are monounsaturated fatty acids.
Statistical analyses The data were subjected to ANOVA using the GLM procedure of SAS (SAS Institute Inc., 2000). The cage (one or two rabbits/cage) served as the experimental unit. The model included the fixed effect of water distribution, and the cage was specified as a random effect. Differences among means of treatments were compared using the Tukey’s test at P < 0.05. Mortality rate was analysed by the x2 test.
Water restriction in growing rabbits Results The mortality rate from 35 to 60 days was higher in the AL group (10.1% v. 5.2%, P , 0.0001). No analyses were performed to detect the cause of mortality; however, all dead rabbits showed signs of diarrhoea. After 60 days, and up to slaughter age (84 days), no mortality occurred in either group. Because of mortality, some cages in each group were discarded so that the number of cages used for statistical analysis was 29 and 31, respectively, for the AL and WR groups. Table 2 summarizes the in vivo performance recorded in the experimental period. BW gain was higher for the AL group during the post-weaning (38.2 v. 31.2 g/day, P , 0.01) and the entire period of the trial (34.4 v. 32.0 g/day, P , 0.05). No differences were recorded between the groups during the fattening period. The restricted access to drinking water reduced ADFI in the period 35 to 60 days by about 24 g/rabbit per day (217.4%). After 60 days of age, when the access to drinking water was free, no differences for ADFI were recorded between the groups up to slaughter age. However, considering the entire period of the trial (35 to 84 days of age), ADFI was higher in the AL group (155.8 v. 140.3 g/day, P , 0.05). Feed conversion ratio was affected by dietary treatment during the fattening period (61 to 84 days) and was more favourable for the WR group (5.15 v. 5.75, P , 0.05). The digestibility values (Table 3) showed that rabbits with free access to drinking water had a lower digestibility of dry matter, OM, NDF, ADF and cellulose (14.7%, 14.5%, 110.2%, 118.8% and 112.8%, respectively). The percentages of perirenal and scapular fat (Table 4) were higher in rabbits drinking ad libitum (130.7% and 1116.6%, respectively). No effect of water restriction was observed on the weight of the left hind leg of rabbits (overall mean 179.2 g). Furthermore, there were no differences Table 2 Effects of water restriction on in vivo performance of rabbits Days BW, g 35 60 84 BW gain, g/day 35 to 60 61 to 84 35 to 84 Feed intake, g/day 35 to 60 61 to 84 35 to 84 Feed conversion ratio, g/g 35 to 60 61 to 84 35 to 84
Water Ad libitum restricted r.m.s.e.1 P-value
947.0 1902 2637
961.5 1743 2528
38.2 30.6 34.4
31.2 32.7 32.0
135.7 175.9 155.8
112.1 168.7 140.3
3.55 5.75 4.53
3.59 5.15 4.39
66.9 78.6 118.1 2.75 1.98 2.51
0.456 0.008 0.005 0.003 0.198 0.014
7.56 ,0.001 13.1 0.090 8.47 0.012 0.29 0.68 0.51
0.629 0.015 0.392
r.m.s.e. 5 root mean square error. 1 n 5 29 and 31 cages, respectively, for the ad libitum and water-restricted groups (lost three and one cages, respectively, because of mortality).
between the WR and AL groups in L*, a* and b* colour and WBSF of the left hind leg meat (overall means 50.2, 4.9, 2.0 and 0.4 kg, respectively). The results also showed that the percentage of meat, bone and fat, as well as the meat to bone ratio in the left hind leg of rabbits did not differ between the WR and AL groups (overall means 76.0%, 21.9%, 2.1% and 3.6%, respectively). In addition, the time of access to drinking water produced no changes in either the chemical composition or the frozen loss of rabbit meat (overall means 72.7%, 22.3%, 3.3%, 1.3% and 1.2%, respectively, for moisture, protein, lipid, ash and frozen loss). Restricted rabbits showed a higher proportion of C16:0 (112.9%) and, as a consequence, a higher level of saturated fatty acids (112.5%) than the AL group (Table 5). Table 3 Effects of water restriction on apparent digestibility values (%) of the nutrients in rabbits at 60 days of age Item Dry matter Organic matter CP Ether extract NDF ADF Cellulose Hemicellulose
Ad libitum
Water restricted
r.m.s.e.1
P-value
59.0 59.5 77.5 73.4 33.3 27.6 31.3 40.7
61.8 62.2 76.6 73.2 36.7 32.8 35.3 41.6
1.71 1.74 1.19 3.12 3.13 2.89 2.85 4.74
0.006 0.009 0.159 0.920 0.049 0.003 0.032 0.708
r.m.s.e. 5 root mean square error. 1 n 5 29 and 31 cages, respectively, for the ad libitum and water-restricted groups (lost three and one cages, respectively, because of mortality).
Table 4 Effects of water restriction on carcass traits in slaughtered rabbits (84 days of age) Item Body weight, g Carcass length, cm Carcass circumference, cm Reference carcass, g pHBF1 % of BW Skin Gastrointestinal tract Hot dressing out Chilled dressing out % of reference carcass Liver Kidney Hearth* Head Perirenal fat Inguinal fat Scapular fat
Water Ad libitum restricted r.m.s.e.1 P-value 2155 32.4 18.9 1217 6.9
2207 32.7 19.0 1239 6.9
140.7 1.08 1.02 100.6 0.09
0.232 0.612 0.768 0.395 0.892
15.4 19.7 60.1 59.9
15.2 21.2 59.3 59.0
0.53 2.15 1.82 1.81
0.895 0.542 0.639 0.321
6.6 1.3 2.1 11.4 1.7 0.52 1.3
6.5 1.3 2.0 11.4 1.3 0.54 0.65
0.96 0.751 0.15 0.214 0.25 0.625 1.33 0.951 0.12 0.003 0.02 0.503 0.11 ,0.001
r.m.s.e. 5 root mean square error. 1 n 5 16 (8 males and 8 females) per group. pHBF1 5 pH of m. biceps femoris measured 1 h after slaughtering. *5means the whole heart, lungs, oesophagus, trachea, thymus gland.
1603
Bovera, Lestingi, Piccolo, Iannaccone, Attia and Tateo Table 5 Effects of water restriction on fatty acid profile (% of total fatty acid methyl esters) and indexes related to human health of hind leg rabbit meat Fatty acids C12:0 C14:0 C16:0 C18:0 Total SFA C12:1 C16:1 C18:1 Total MUFA C18:2 n-6 C18:3 n-6 C18:3 n-3 C20:4 n-6 C20:5 n-3 C22:5 n-3 C22:6 n-3 Total PUFA Total n-3 Total n-6 n-3/n-6 Atherogenic index Thrombogenic index
Ad libitum Water restricted r.m.s.e1 P-value 1.1 5.1 28.6 0.60 35.3 0.41 8.8 17.3 26.5 32.9 1.3 0.39 0.54 0.42 1.2 0.55 37.1 2.5 34.6 0.07 0.81 0.46
1.1 5.7 32.3 0.55 39.7 0.73 9.7 14.8 25.1 30.3 1.8 0.41 0.58 0.63 1.4 0.59 35.6 2.9 32.7 0.09 0.92 0.54
0.65 0.76 2.88 0.11 3.27 0.15 1.33 3.37 3.46 3.42 0.90 0.13 0.34 0.09 0.17 0.14 3.01 0.33 2.99 0.01 0.10 0.06
0.875 0.152 0.026 0.368 0.023 0.004 0.225 0.173 0.456 0.168 0.322 0.576 0.418 0.001 0.033 0.650 0.339 0.035 0.231 0.024 0.022 0.031
SFA 5 saturated fatty acids; MUFA 5 monounsaturaterd fatty acids; PUFA 5 polyunsaturated fatty acids; r.m.s.e. 5 root P mean square P error; Atherogenic index 5 (C12 : 0 1 4 3 C14 : 0 1 C16 : 0) / [ MUFA 1 (n-6) 1 P P (n-3)]; Thrombogenic index 5 (C14 : 0 1 C16 : 0 1 C18 :0) / [ 0.5 3 MUFA 1 P P P P 0.5 3 (n-6) 1 3 3 (n-3) 1 (n-3) / (n-6)]. 1
n 5 16 (8 males and 8 females) per group.
The lauroleic acid (C12:1) was also significantly higher in the WR group (175.0%), but the total MUFA proportion was unaffected. In addition, total polyunsaturated fatty acids (PUFAs) were unaffected by water restriction, although C20:5 and C22:5 fatty acids (both n-3 FA) were higher in the WR group (150.0% and 116.6%, respectively). Meat from WR rabbits also had higher proportions of total n-3 (116.0%) and a higher n-3/n-6 ratio (128.6%) than the AL group. Finally, both atherogenic and thrombogenic indexes were significantly higher in the WR group. Discussion The limitation of the access to drinking water as a way to reduce feed intake is obviously not in line with one of the five rules of the Farm Animal Welfare Council (in particular: freedom from hunger and thirst). However, the group submitted to the water restriction showed a lower mortality rate and, as a consequence, the freedom from pain, injury or disease was impaired. The positive effect of water restriction on mortality rate was also observed by Gidenne et al. (2009a and 2009b) who showed, according to our results, a reduction of almost half in the mortality rate when rabbits were submitted to a feed restriction of 20%. Martignon (2010) 1604
underlined that the favourable effect on mortality rate was because of the reduction of the feed intake independently from the distribution procedure of the feeds. Water restriction was confirmed as an effective way to reduce feed intake. This result agrees with the findings of El Maghraby et al. (2011) who reported that feed intake of rabbits was reduced by 19.1% when the access to water was reduced to 2 h/day in the period from 35 to 63 days of age. The same authors found that feed intake was reduced by 13.3% in the entire growing period of rabbits slaughtered at 77 days of age. Boisot et al. (2004) also reported that feed intake was reduced by 18% when the access to water was reduced to 2 h/day. The growth rate of the rabbits was reduced as a consequence of feed intake reduction, both in the period when access to water was limited and in the entire period of the experiment, without an evident compensatory growth in the fattening period, when all rabbits had ad libitum access to water. Despite the higher estimated digestibility values of dry matter and organic matter obtained in the WR group in the post-weaning period, calculated intake of nutrients in the same period, particularly digestible energy and protein intakes, were higher in the AL group than in the WR one (0.68 v. 0.59 MJ/day and 15.8 v. 12.9 g/day, respectively, for AL and WR groups). The higher intake of nutrients in rabbits of the AL group explains their higher BW gain in the post-weaning period. However, in the same period, FCR was not different according to the groups. In our trial, the higher digestibility of dry matter and organic matter was tied to a higher digestibility of NDF and, in particular, of the cellulose. Several authors (Di Meo et al., 2007; Gidenne et al., 2009a) found that feed restriction can affect nutrient digestibility, also improving fibre digestion. It is well established that a reduction of feed intake induces higher retention time of the diet in the digestive tract and also could change the caecal microbial population and/or activity affecting the fibre digestion. In a recent study, Gidenne et al. (2012) reported that the level of intake had no significant effect on the number of bacterial 16S rDNA copies/g of caecal content, and did not influence the bacterial community structure or diversity, although the same authors noted that the performed CE-SSCP profile analysis only takes into account the major bacterial populations. Therefore, it is possible that the reduction of feed intake, besides stimulating a high retention time of the diet through the digestive tract (Gidenne et al., 2012), may have affected the caecal microbial population and/or activity, also stimulating a more intense cellulose digestibility. Most of the carcass traits were unaffected by dietary treatment, probably because of the progressively increasing time of water distribution during the post-weaning period. In general, it is thought that feed restriction leads to changes in the growth of internal organs such as the liver and digestive tract. In particular, it has been reported that digestive tract development is affected by feed restriction (Saleh et al., 1996; Tumova et al., 2006) and that, after the restriction period, the growth of digestive organs is very rapid (Gidenne et al., 2012). Gidenne et al. (2012) reported a
Water restriction in growing rabbits final weight of the entire digestive tract (organ 1 digesta) about 10% higher in AL rabbits than in restricted rabbits. Bergaoui et al. (2008) also found no significant differences in the digestive tract percentage of rabbits fed ad libitum or restricted to 85% from 42 to 77 days of age (20.1% v. 21.1%), whereas significant differences were found for rabbits restricted to 70% during the same period. Probably, a moderate level of feed restriction had a lower influence on the digestive tract development. The development of the digestive tract in restricted rabbits is also linked to changes in feeding behaviour, as a lower number of meals are consumed and a higher intake of feed per meal is recorded in comparison with rabbits fed ad libitum (Gidenne et al., 2012). Moreover, the technique used for feed restriction is very important. Gidenne et al. (2012) reported that when the restriction was directly applied to the feeds (reduction of the total amount or reduction of the time of access to the trough), the rabbit adapted very quickly to the restriction strategy, with a very high intake just after the feed distribution, which reached 40% of the daily intake (within 2 h from the first access to the feed) only 8 days after the introduction of the feed restriction. The rabbit fed freely shows a relatively smooth intake behaviour with numerous meals characterized by a maximum of 10% of the daily intake 2 to 4 h after the lights have been switched off, and a minimal intake 2 to 4 h after they have been switched on, which probably correspond to the caecotrophy period (Gidenne et al., 2012). In our trial, feed intake was reduced by limiting access to water so that this effect was less evident. In fact, as reported by Ben Rayana et al. (2008), when water was supplied 2 h/day, the feed intake of rabbits reached the 40% of the total intake 4 h after access to water – double the time of feed restriction. El Maghraby (2011), also applying a water restriction at 2 or 1 h/day, did not find significant differences in the full gastrointestinal tract between restricted and AL rabbits. The restricted group had significantly lower percentages of perirenal and scapular fats. In subcutaneous and internal adipose tissues, feed restrictions depress the rate of de novo lipogenesis and the activities of numerous enzymes involved in the synthesis of fatty acids or responsible for generating nicotinamide adenine dinucleotide phosphate (NADPH) for the support of lipogenesis (Gondret et al., 2000). The reduction of perirenal and scapular fat is of great interest, in view of the fact that perirenal fat is correlated with the total fat of the carcass (Ouhayoun et al., 1984). In rabbits, the endogenous fatty acids (synthesized from carbohydrates) are mainly C16:0, C18:1 and C18:0 (Ouhayoun, 1998). PUFA of the rabbit meat result primarily from the ingestion of exogenous lipids (Ouhayoun, 1998), even though the synthesis of n-3 PUFA is possible from its diet precursor in the liver, and the amount produced depends on the dietary n-6/n-3 ratio (Peiretti and Meineri, 2008). However, according to Castellini et al. (2002), the fatty acid composition of the feed and animal tissues can be modified as a result of the action of the gastrointestinal microflora because the gut microorganisms are able to hydrogenate
unsaturated organic acids into more saturated ones, or even to desaturate some organic acids. Castellini et al. (2002) highlighted the role of caecal microflora, showing that the ingestion of soft faeces by rabbits induced a greater concentration of n-3 long-chain PUFA in the meat. In the current experiment, the main reason for the differences in the fatty acid profile in meat is that the concentrations of saturated fatty acids (SFA, mainly C16:0) and of n-3 PUFA (mainly C20:5 and C22:5) increased when water restriction was applied. Therefore, it may be that changes occurred in the caecal microflora (supported also by the changes in cellulose digestibility) and microorganisms with different preferences for fatty acid synthesis may have been favoured, affecting the fatty acid composition of the meat in the rabbits. As a consequence, the meat from restricted rabbits seemed to be healthier for humans because of the higher proportion of n-3 and the higher n-3/n-6 ratio. However, the meat from rabbits with ad libitum access to water had more favourable atherogenic and thrombogenic indexes because of the lower content of C16:0. From this point of view, the meat of rabbits from the water-restricted group appeared less healthy than that from the ad libitum group: there is epidemiological and experimental evidence indicating that a diet high in SFA (C12:0, C14:0 and C16:0) is associated with high levels of serum cholesterol, which in turn are related to high incidences of coronary heart disease. Conclusions Limiting the drinking access in the post-weaning period may lead to advantages for the digestive health of the growing rabbit, as mortality rate is reduced. Despite higher final live weights of rabbits drinking ad libitum, water restriction had no negative effects on carcass traits from animals of both groups with similar final weight, and carcasses from restricted rabbits had a lower content of perirenal and scapular fats. Physical and chemical meat characteristics also seem unaffected by water restriction, although fatty acid composition provides contradictory results: in fact, the meat of restricted rabbits not only had higher proportions of palmitic acid but also higher proportions of n-3 fatty acids and a higher n-3/n-6 ratio. Water restriction can be effectively used as a way to improve the sanitary status of the digestive system of young rabbits, when applied during the winter months. However, from the animal welfare point of view, a water restriction can be criticized as a method to restrict feed intake.
References Association of Official Analytical Chemists (AOAC) 1984. Official methods of analysis, 14th edition. AOAC, Washington, DC. Association of Official Analytical Chemists (AOAC) 2004. Official methods of analysis, 18th edition. AOAC, Arlington, VA, USA. Ben Rayana A, Ben Hamouda M and Bergaoui R 2008. Effect of water restriction times of 2 and 4 hours per day on performances of growing rabbits. In Proceedings of the 9th World Rabbit Congress (ed. G Xiccato, A Trocino and SD Lukfahr), June 10–13, 2008, pp. 541–545, Verona, Italy, Fond. Ini. Zooprofilattiche E Zoot. publ. Brescia Italy. Retrieved June 20, 2012, from http://world-rabbit-science.com/WRSAProceedings/Congress-2008-Verona/Papers/N-BenRayana.pdf.
1605
Bovera, Lestingi, Piccolo, Iannaccone, Attia and Tateo Bergaoui R, Kammoun M and Ouerdiane K 2008. Effects of feed restriction on the performance and carcass of growing rabbits. In Proceedings of the 9th World Rabbit Congress (ed. G Xiccato, A Trocino and SD Lukfahr), June 10–13, 2008, pp. 547–550, Verona, Italy, Fond. Ini. Zooprofilattiche E Zoot. publ. Brescia Italy. Retrieved June 20, 2012, from http://world-rabbit-science.com/ WRSA-Proceedings/Congress-2008-Verona/Papers/N-Bergaoui.pdf. Blasco A and Ouhayoun J 1996. Harmonization of criteria and terminology in rabbit meat research. Revised proposal. World Rabbit Science 4, 93–99. Boisot P, Duperray J, Dugene´tais X and Guyonvarch A 2004. Interest of hydric restriction times of 2 and 3 h per day to induce feed rstriction in growing rabbits. In Proceedings of the 8th World Rabbit Congress (ed. C Becerril and A Pro), pp. 759–764. Colegio de Postgraduados for WRSA, Puebla, Mexico. Retrieved January 30, 2012, from http://world-rabbit-science.com/WRSA-Proceedings/ Congress-2004-Puebla/Puebla-2004-a.htm. Bovera F, Lestingi A, Iannaccone F, Tateo A and Nizza A 2012. Use of dietary mannanoligosaccharides during rabbit fattening period: effects on growth performance, feed nutrient digestibility, carcass traits, and meat quality. Journal of Animal Science 90, 3858–3866. Castellini C, Dal Bosco A and Mugnai C 2002. Effect of caecotrophy on the fatty acid profile of rabbit meat. Progress in Nutrition 4, 125–130. Dewree R, Licois D, Coudert P, Lassence C, Vindevogel H and Marlier D 2003. L’ente´ropathie e´pizootique du lapin (EEL): e´tude du role des infections par Clostridium perfringens dans l’e´tio-pathoge´nie de ce syndrome. In Proceedings of 10e`mes Journe´es de la Recherche Cunicole (ed. ITAVI - AFSSA), November 2003, pp. 251–254, Itavi Service Diffusion Publications, Paris, France. Di Meo C, Bovera F, Marono S, Vella N and Nizza A 2007. Effect of feed restriction on performance and feed digestibility in rabbits. Italian Journal of Animal Science 6, 765–767. El Maghraby MMA 2011. Effect of restricted access to drinking water on growth, feed efficiency and carcass characteristics of fattening rabbits. Asian Journal of Animal Sciences 5, 136–144. European Union 2005. Ban on antibiotics as growth promoters in animal feed enters into effect. Retrieved December 22, 2005, from http://europa.eu/ rapid/pressReleasesAction.do?reference5IP/05/1687&format5HTML&aged5 0&language5EN&guiLanguage5en.PDF. Folch J, Lees M and Sloane-Stanley H 1957. A simple method for the isolation and purification of total lipids from animal tissues. Journal of Biological Chemistry 226, 497–502. Gidenne T and Lebas F 2006. Feeding behaviour in rabbits. In Feeding in domestic vertebrates. From structure to behaviour (ed. V Bels), pp. 179–209. CABI Publishing, Wallingford, UK. Gidenne T, Combes S and Fortun-Lamothe L 2012. Feed intake limitation strategies for the growing rabbit: effect on feeding behaviour, welfare, performance, digestive physiology and health: a review. Animal 6, 1407–1419.
1606
Gidenne T, Garcia J, Lebas F and Licois D 2010. Nutrition and feeding strategy: interactions with pathology. In Nutrition of the rabbit (ed. C De Blas and J Wiseman), pp. 179–199. CABI Publishing, UK. Gidenne T, Combes S, Feugier A, Jehl N, Arveux P, Boisot P, Briens C, Corrent E, Fortune H, Montessuy S and Verdelhan S 2009a. Feed restriction strategy in the growing rabbit. 2. Impact on digestive health, growth and carcass characteristics. Animal 3, 509–515. Gidenne T, Murr S, Travel A, Corrent E, Foubert C, Bebin K, Mevel L, Rebours G and Renouf B 2009b. Effets du niveau de rationnement et du mode de distribution de l’aliment sur les performances et les troubles digestifs postsevrage du lapereau. Premiers re´sultats d’une e´tude concerte´e du re´seau GEC. Cuniculture Magazine 36, 65–72. Gondret F, Lebas F and Bonneau M 2000. Restricted feed intake during fattening reduces intramuscular lipid deposition without modifying muscle fiber characteristics in rabbits. Journal of Nutrition 130, 228–233. Martignon MH 2010. Consequences of a feed intake control on digestive physiopathology and on feeding behaviour. PhD thesis, Institut National Polytechnique de Toulouse, 194pp. Retrieved January 30, 2012, from http:// ethesis.inp-toulouse.fr/archive/00001486/. Ouhayoun J 1998. Influence of the diet on rabbit meat quality. In The nutrition of the rabbit (ed. C De Blas and J Wiseman), pp. 177–195. CABI Publishing, Wallingford, UK. Ouhayoun J, Gidenne T and Demarne Y 1984. Evolution postnatale de la composition en acides gras des lipids du tissue musculaire chez le lapin en regime hypolipidique. Reproduction Nutrition Development 25, 505–509. Peiretti PG and Meineri G 2008. Effects on growth performance, carcass characteristics, and the fat and meat fatty acid profile of rabbits fed diets with chia (Salvia hispanica L.) seed supplements. Meat Science 80, 1116–1121. Roe MT and Pillai SD 2003. Monitoring and identifying antibiotic resistance in bacteria. Poultry Science 82, 622–626. Saleh K, Attia YA and Younis H 1996. Effect of feed restriction and breed on compensatory growth, abdominal fat and some production traits of broiler chicks. Archiv Fu¨r Geflu¨gelkunde 60, 153–159. SAS Institute Inc. 2000. SAS/STAT users guide: statistics. SAS Institute Inc., Cary, NC. Tumova E, Zita L and Stolc L 2006. Carcass quality in restricted and ad libitum fed rabbits. Czech Journal of Animal Science 51, 214–219. Ulbricht TL and Southgate DAT 1991. Coronary heart disease: seven dietary factors. The Lancet 338, 985–992. Vogtmann H, Frirter P and Prabuck AL 1975. A new method of determining metabolizability of energy and digestibility of fatty acids in broiler diets. British Poultry Science 16, 531–534.
