Effects of feeding Atriplex halimus L. on growth performance and carcass characteristics of fattening Awassi lambs

Small Ruminant Research 137 (2016) 65–70

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Effects of feeding Atriplex halimus L. on growth performance and carcass characteristics of fattening Awassi lambs Belal S. Obeidat a,∗ , Kamel Z. Mahmoud a , Jumana A. Maswadeh a , Emad Y. Bsoul b a b

Department of Animal Production, Faculty of Agriculture, Jordan University of Science and Technology, Irbid 22110, Jordan Department of Biology and Biotechnology, The Hashemite University, Zarqa, Jordan

a r t i c l e

i n f o

Article history: Received 21 December 2015 Received in revised form 9 March 2016 Accepted 10 March 2016 Available online 11 March 2016 Keywords: Awassi lambs Atriplex halimus L. Growth performance Carcass characteristics

a b s t r a c t A study was conducted to determine the effect of partial replacement of wheat straw by Atriplex halimus L. (ATR) on growth performance, nutrient intake, digestibility, carcass characteristics and meat quality of Awassi lambs fed finishing diet. Twenty seven Awassi ram lambs (initial body weight 14.9 ± 0.54 kg) were divided randomly into three dietary groups. Group one served as a control and received no ATR (CON), group two (ATR75) and three (ATR150) received diet containing 75 and 150 g/kg ATR, respectively. Lambs were housed individually in shaded pen (1.5 × 0.75 m), and fed ad libitum isonitrogenous diets. Nutrient intakes were determined daily throughout the experimental period, which lasted for 91 days. On day 56, of the fattening period, 6 lambs from each group were chosen at random and housed individually in metabolism crates to determine nutrient digestibilities and N balance. At the end of the study, all lambs were slaughtered to evaluate carcass characteristics and meat quality. Intakes of dry matter (DM), organic matter (OM), crude protein (CP), and neutral detergent fiber (NDF) were similar among treatment diets as well as water intake. Growth performance parameters did not differ among all treatment diets although lambs fed on the CON diet had greater (P < 0.05) intake of acid detergent fiber (ADF) compared to lambs fed on ATR diets. Feeding cost was reduced (P < 0.05) when wheat straws was replaced by ATR. Digestibility of DM, OM, CP, NDF and ADF was similar among treatment diets. Nitrogen balance and fecal N was greater (P < 0.05) in ATR150 diet followed by CON and ATR75 diets. Rumen fluid pH and carcass characteristics showed similar values among all dietary treatments. The longissimuss muscle leaner dimensions and fat measurements were comparable among all treatment groups. Also, carcasses from different dietary groups scored similar pH, cooking loss, water holding capacity, shear force and color coordinates. Results of this study demonstrated the possibility of including A. halimus L. up to 150 g/kg in fattening diets of Awassi lambs without any adverse effects on growth performance, carcass characteristics and meat quality; whereas it reduced the cost of feeding. © 2016 Elsevier B.V. All rights reserved.

1. Introduction Wheat and barley straws, the extensively used forage in livestock diets in Jordan, are characterized by not only lower content of energy and crude protein as well as a lower digestibility, but also it is not cost effective when used in diets of growing and fattening lambs. Therefore, livestock producers tend to use alfalfa hay or other available forages. Even though, alfalfa hay is an excellent forage source in ruminant diets, but it’s not cost effective as well. Using alternative forages, such as olive cakes, tomato pomace, or Atriplex

∗ Corresponding author at: Department of Animal Production, Faculty of Agriculture, Jordan University of Science and Technology, P.O. Box 3030, Irbid 22110, Jordan. E-mail address: [email protected] (B.S. Obeidat). http://dx.doi.org/10.1016/j.smallrumres.2016.03.007 0921-4488/© 2016 Elsevier B.V. All rights reserved.

halimus L. to replace part or all of forages may be economically advantageous to reduce the feeding costs. Thus, appropriate use of feeds alternative is important to profitable livestock production. A. halimus L. (Mediterranean saltbush) is shrub native to Jordan and represent almost 650 g/kg of saltbush ranch in the Middle East (Le Houerou, 1991), that have a good ability to tolerate drought and salinity (Le Houerou, 1992), and well adapted to live in semiarid and arid conditions (McKell, 1975). A. halimus L. contains good levels of CP [up to 200 g/kg dry matter (DM)] and metabolizable energy (2.75–5.6 Mcal/kg DM) which makes it a good forage source for ruminants (Barrett-Lennard et al., 2003). However, a major limitation of feeding sheep on A. halimus L. is its high salt content, which may negatively affect intake and digestibility (Ben Salem et al., 2005).

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Previous studies showed that feeding sheep on A. halimus L. alone does not increase growth rate and as a result feeding A. halimus L. as a sole diet may be appropriate to be used only as maintenance feed (Chriyaa et al., 1997). Ben Salem et al. (2005), Ahmed et al. (2001) and Shawket et al. (2001) concluded that when lambs fed only on A. halimus L., they lose weight and must accompanied with another source of energy. The available literature regarding to the effect of feeding A. halimus L. on sheep performance, A. halimus L. may change the characteristics and meat quality. Feeding A. halimus L. produces leaner carcass (Hopkins and Nicholson, 1999), reduces carcass fat content (Kraidees et al., 1998), increases hot carcass weight, as well as no change in meat quality (Pearce et al., 2008). Therefore, we hypothesized that the partial inclusion of A. halimus L. in growing and fattening diets may improve meat quality characteristics without negatively affecting growth performance. The objective of this experiment was to study the effect of partial replacement of wheat straw by A. halimus L. on growth performance, nutrient intake, digestibility, and carcass and meat characteristics of Awassi lambs fed finishing diet. 2. Material and methods 2.1. Study area This study was conducted at the Agricultural Research and Training Unit (ARTU) at Jordan University of Science and Technology (JUST). The study area is classified as semi-arid area at latitude 32◦ 30 N and elevation of 510 m above the sea level. All samples and carcass characteristics measurements were conducted in the Nutrition and Meat laboratories in the Department of Animal Production at the Faculty of Agriculture. All experimental procedures were approved by JUST Institutional Animal Care and Use Committee. 2.2. Experimental design, animals and diets Twenty seven newly weaned Awassi ram lambs (BW = 14.9 ± 0.54 kg and 2–3 months of age) were assigned randomly to one of three dietary groups. First group fed the control (CON) diet; second group (ATR75) and third group (ATR150) received 75 and 150 g/kg DM A. halimus L., respectively, to replace wheat straw as indicated in Table 1. Lambs were purchased from a single commercial sheep farm and transported 100 km to the ARTU/Farm Animal Research Facility at JUST. Upon arrival at the study location, lambs were individually weighed, ear tagged, dipped and treated against internal and external parasites. A. halimus L. was harvested from JUST campus, sun dried and grind before it incorporated in the diet. The chemical composition of A. halimus L. that were used in current study was 368, 121, 392 and 200 g/kg for DM, crude protein (CP), neutral detergent fiber (NDF) and acid detergent fiber (ADF), respectively. All diets were iso-nitrogenous and formulated to have 160 g/kg CP (DM basis) and to meet the requirements for fattening Awassi Lambs (NRC, 2007). Lambs were housed individually in shaded pen (1.5 × 0.75 m), and fed at 08:00 h. The study lasted for 91 days (7 days were used as adaptation followed by 84 days for data collection). Diets were mixed biweekly during the study and were sampled upon mixing to ensure the consistency in their chemical composition. A total mixed ration diet was offered ad libitum (110% of the previous day’s intake) to all animals with free access to fresh water for the duration of the study. For each lamb, individual refusals of feed were weighed daily during the 84-day period and stored (−20 ◦ C) until analyzed for DM and other nutrients to evaluate daily nutrients intake. Lambs were weighed at the beginning of the study and biweekly, thereafter, before the morning feeding throughout the

Table 1 Ingredients and chemical composition of diets fed to fattening Awassi lambs. Item

Dieta CON

ATR75

ATR150

Ingredients (g/kg DM) Barley Soybean meal Wheat straw Atriplex halimus L. Salt Limestone Vitamin-mineral premixb

490 190 300 00 10 10 +

508 172 225 75 10 10 +

525 155 150 150 10 10 +

Feed cost/ton (US$)c

345

316

288

Nutrients (g/kg DM) Dry matter Organic matter Crude protein Neutral detergent fiber Acid detergent fiber

934 869 161 348 170

937 894 161 323 144

931 893 161 299 121

a Diets were (1) no Atriplex halimus L. (CON), (2) 75 g/kg Atriplex halimus L. (ATR75), and (3) 150 g/kg Atriplex halimus L. (ATR150). b Composition per kg contained (vitamin A, 600,000 IU; vitamin D3, 200,000 IU; vitamin E, 75 mg, vitamin K3, 200 mg; vitamin B1, 100 mg; vitamin B5, 500 mg; lysine 0.5%; DL-methionine, 0.15%; manganese oxide, 4000 mg; ferrous sulphate, 15,000 mg; zinc oxide, 7000; magnesium oxide, 4000 mg; potassium iodide, 80 mg; sodium selenite, 150 mg; copper sulphate, 100 mg; cobalt phosphate, 50 mg, dicalcium phosphate, 10,000 mg. c Calculated based on the prices of diet ingredients of the year 2015.

study to determine average daily gain (ADG) and feed conversion ratio (FCR; DM intake: gain). 2.3. Laboratory procedures Diets and refusal samples were dried at 55 ◦ C in a forced-air oven to reach a constant weight, air equilibrated, and then ground to pass 1 mm screen (Brabender OHG Duisdurg, Kulturstrase 51–55, type 880845, Nr 958084, Germany) and kept for further analysis. A. halimus L., feeds and refusals were analyzed for DM, CP, NDF and ADF. Following AOAC (1990) procedures, samples were analyzed for DM (100 ◦ C in air-forced oven for 24 h), and CP (Kjeldahl procedure). Neutral detergent fiber and ADF were analyzed according to procedures described by Van Soest et al. (1991) with modifications for use in the ANKOM2000 fiber analyzer apparatus (ANKOM Technology Cooperation, Fairport, NY). Neutral detergent fiber analysis was conducted using sodium sulfite and alpha amylase (heat stable) and expressed with residual ash content. 2.4. Digestibility and N balance trial On day 56, of the fattening period, 6 lambs from each group were chosen at random and housed individually in metabolism crates (1.05 × 0.80 m) to evaluate nutrient digestibilities and N balance. Animals were allowed a period of five days to adapt the metabolism crates, and then followed by collection period of five days; where feed intake and refusals were recorded and sampled for further analysis. Daily fecal output was collected, weighed and recorded, and then 10% was kept for subsequent analyses. Using plastic containers, urine was collected, weighed and recorded, and then 5% was kept (−20 ◦ C) to evaluate N balance. Each bottle had 50 mL of 6 N HCL to prevent ammonia losses. Fecal samples were dried at 55 ◦ C in a forced-air oven to reach a constant weight, air equilibrated, and then ground to pass 1 mm screen (Brabender OHG Duisdurg, Kulturstrase 51–55, type 880845, Nr 958084, Germany) and kept for further analysis. Feed, refusals and feces were analyzed for DM, CP, NDF and ADF as described pre-

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viously. Urine samples were analyzed for CP (Kjeldahl procedure) to calculate N retention. 2.5. Slaughtering procedure At the end of the 91-days period, all lambs were slaughtered at the Center for Agriculture and Production facilities at JUST to evaluate carcass characteristics. Lambs were slaughtered at 9:00 h by trained personnel using a standard slaughter procedure, which was approximately 18 h after last feeding. Fasted live weight was recorded immediately before slaughter, and hot carcass weight was recorded after slaughter. Cold carcass weight was recorded after carcasses were chilled at 4 ◦ C for 24 h. Dressing percentage was calculated as the percentage of cold carcass weight/fasted live weight. Non-carcass edible components were removed and weighed directly after slaughter. Non-carcass components included lungs and trachea, heart, liver, spleen, kidneys, kidneys fat, mesenteric fat and testes. Immediately after slaughtering the animals, rumen fluid samples were collected from each animal. Samples were filtered using 4 layer of cheese cloth and pH was measured (pH Spear, Eutech Instrument, USA). On the next day, the following linear dimensions were taken on the chilled carcasses and longissimus muscle: tissue depth (GR), rib fat depth (J), eye muscle width (A), eye muscle depth (B), eye muscle area, and fat depth (C). Carcasses were then cut into four parts (shoulder, rack, loin and leg cuts). Upon cutting, leg cut was dissected and longissimus muscle excised from the loin cut and vacuum-packed immediately and stored at −20 ◦ C for 2 weeks until the time of meat quality assessment. 2.6. Meat quality measurements Meat quality parameters measured were pH, color (CIE L*a*b* coordinates), cooking loss, water holding capacity (WHC), and shear force values. Frozen longissimus muscles were thawed in a chiller at 4 ◦ C overnight while still in plastic bags. Each muscle was divided into slices of specific thickness and each slice was used for specified meat quality measurement as described by Obeidat et al. (2008, 2009). Color was measured on slices of 15 mm thick, all slices were placed on a polystyrene tray and covered with permeable film and allowed to oxygenate for 2 h at 4 ◦ C. Cooking loss (CL) was measured on duplicate-slices of 25 mm thickness, slices were weighed before cooking, placed in plastic bags and cooked in water bath at 75 ◦ C for 90 min and re-weighed after cooking to calculate the percentage of water lost on cooking. The cooked slices were stored at 4 ◦ C over night, then 6 cores, with the size of 1 mm3 were cut from the slices to measure shear force values. Cooked meat cores were sheared in a perpendicular direction of muscle fiber using Warner-Bratzler (WB) shear blade with the triangular slot cutting edge mounted on Salter Model 235(Warner-Bratzler meat shear, GR manufacturing Co. 1317 Collins LN, Manhattan, Kansas, 66502, USA) to determine the peak force (kg) required to shear the cores. pH was measured after thawing by pH meter. Water holding capacity was measured using the procedure describe by Grau and Hamm (1953). Approximately, 5 g of raw meat was cut into small pieces and placed between 2 filter paper and 2 quartz plates, and pressed with a weight of 2500 g for 5 min, then meat was removed and weighed, WHC was calculated as a percent of the initial weight WHC% = (initial wt − final wt) × 100/initial wt. 2.7. Statistical methods Data were analyzed using MIXED procedure of SAS (Version 8.1, 2000, SAS Inst. Inc., Cary, NC). For all data, the fixed effects included only treatment. Least square means were separated using

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Table 2 Effects of feeding Atriplex halimus L. on nutrient and water intakes and growth performance of fattening Awassi lambs. Item

Dieta CON

ATR75

ATR150

SE

930 802 154 291 137a

875 781 144 249 95b

981 873 161 252 85b

55.5 48.8 10.1 17.4 8.9

Water intake (Liter/day)

3.39

3.48

3.89

0.293

Initial weight (kg) Final weight (kg) Total gain (kg) Average daily gain (g/day) FCR Cost/kg (US$)

15.1 33.3 18.3 217 4.32 1.49a

14.6 31.9 17.3 206 4.29 1.36b

14.9 33.4 18.5 220 4.50 1.30b

0.54 1.40 1.23 14.6 0.163 0.052

Nutrient intake (g/day) Dry matter Organic matter Crude protein Neutral detergent fiber Acid detergent fiber

a Diets were (1) no Atriplex halimus L. (CON), (2) 75 g/kg Atriplex halimus L. (ATR75), and (3) 150 g/kg Atriplex halimus L. (ATR150). b Means within a row without a common superscript differ significantly (P < 0.05).

Table 3 Effects of feeding Atriplex halimus L. on nutrient digestibility, N balance and rumen fluid pH of fattening Awassi lambs. Item

Dietsa CON

ATR75

ATR150

SE

Digestibility (%) Dry matter Organic matter Crude protein Neutral detergent fiber Acid detergent fiber

78.2 78.8 78.3 57.5 45.8

80.6 81.5 79.9 60.9 47.6

76.7 77.8 76.7 57.9 45.1

2.45 2.31 2.18 5.06 5.86

N balance N intake (g/day) N in feces (g/day) N in urine (g/day) N retained (g/day) Retention (g/100 g) Rumen fluid pH

30.4 9.2a,b 6.6 14.6 48.2 6.81

26.0 7.1b 5.3 13.6 51.8 6.79

31.1 11.1a 7.1 12.9 40.8 6.79

2.40 1.01 0.76 1.88 3.92 0.074

a Diets were (1) no Atriplex halimus L. (CON), (2) 75 g/kg Atriplex halimus L. (ATR75), and (3) 150 g/kg Atriplex halimus L. (ATR150). b Within a row, means without common superscripts differ (P < 0.05).

appropriate pair-wise t-tests if the fixed effects were significant (P < 0.05).

3. Results 3.1. Nutrient intakes and growth performance Nutrient and water intakes data of Awassi lambs fed finishing diets containing A. halimus L. are presented in Table 2. Dry matter intake was similar among treatment diets. Other nutrient intakes followed the same pattern except for the ADF intake. Acid detergent fiber intake was greater (P < 0.05) in lambs fed the CON diet compared to the ATR75 and ATR150 diets. Water intake averaged 3.39, 3.48 and 3.89 L/day for lambs fed on CON, ATR75 and ATR150 diets, respectively with no statistical differences (Table 2). Initial and final body weights, total gain weight, ADG and FCR did not differ among treatment diets. Cost of gain was reduced (P < 0.05) in lambs fed ATR diets compared to lambs fed the CON diet and averaged $1.49, 1.36 and 1.30 per kg of gain for CON, ATR75 and ATR150, respectively (Table 2).

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Table 4 Effects of feeding Atriplex halimus L. on carcass, non-carcass components, dissected leg carcass cut weights and percentages of fattening Awassi lambs. Item

Dietsa CON

Item ATR75

ATR150

32.0 15.5 14.7 45.8 1.4 12.5 2.2

30.6 14.9 13.8 45.2 1.3 12.4 1.8

31.5 15.4 14.7 46.6 1.4 12.7 1.9

1.54 0.96 0.83 0.70 0.06 0.70 0.30

Leg weight (kg) Subcutaneous fat (g/100 g) Intermuscular fat (g/100 g) Total fat (g/100 g) Total meat (g/100 g) Total bone (g/100 g) Meat to bone ratio Meat to fat ratio

2.5 13.7 2.7 16.4 56.2 20.6 2.8 3.7

2.4 13.0 3.1 16.1 55.2 21.1 2.6 3.9

2.4 14.7 2.7 17.3 54.2 21.9 2.6 3.2

1.40 1.55 0.18 1.56 1.61 1.05 0.15 0.41

a

Diets were (1) no Atriplex halimus L. (CON), (2) 75 g/kg Atriplex halimus L. (ATR75), and (3) 150 g/kg Atriplex halimus L. (ATR150). b Non-carcass components (Heart, liver, spleen, kidney, and lungs and trachea). c Carcass cut (shoulder, racks, loins, and legs).

Table 5 Effects of feeding Atriplex halimus L. on carcass leaner dimensions of fattening Awassi lambs.

Leg fat depth (L3) (mm) Tissue depth (GR) (mm) Rib fat depth (J) (mm) Eye muscle width (A) (mm) Eye muscle depth (B) (mm) Eye muscle area (cm2) Fat depth (C) (mm) Shoulder fat depth (S2) (mm)

Dietsa CON

ATR75

ATR150

SE

7.6 11.4 4.2 54.6 24.6 10.1 2.3 3.8

7.6 11.6 4.4 52.8 23.3 9.9 2.9 3.3

8.7 11.6 5.3 51.8 23.8 9.8 2.3 2.9

1.83 0.82 0.66 1.60 1.01 0.70 0.45 0.53

a Diets were (1) no Atriplex halimus L. (CON), (2) 75 g/kg Atriplex halimus L. (ATR75), and (3) 150 g/kg Atriplex halimus L. (ATR150).

3.2. Digestibility, N balance and rumen fluid pH Digestibility, N balances and rumen fluid pH results of Awassi lambs fed finishing diets containing ATR are summarized in Table 3. Digestibility of DM, OM, CP, NDF and ADF was similar among treatment diets. The collected data indicated that N intake, urinary N, retained N, and N retention percentage were similar among all treatment diets. However, fecal N was greater (P < 0.05) in ATR150 diet followed by CON and ATR75 diets. Rumen fluid pH averaged 6.81, 6.79, and 6.79 for the CON, ATR75 and ATR150, respectively without statistical differences.

3.3. Carcass and non-carcass characteristics and meat quality No significant differences were observed between treatment diets in fasting live weight, hot and cold carcass weight, dressing percentage, non-carcass components, carcass cuts weight, fat tail also in dissected leg carcass cut weights and percentages (Table 4). Also, the longissimuss muscle leaner dimensions and fat measurements were comparable among all dietary groups (Table 5). The characteristics of meat quality characteristics performed on longissimus muscle are presented in Table 6. The collected data showed that dietary inclusion of ATR did not influence longissimus muscle pH, cooking loss, water holding capacity, shear force and color coordinates.

Dietsa CON

ATR75

ATR150

SE

pH Cooking loss (g/100 g) Water holding capacity (g/100 g) Shear force (kg/cm2 )

5.91 48.6 28.7 5.73

5.83 50.6 26.8 4.91

5.84 49.3 28.4 5.30

0.040 0.881 1.27 0.777

Color coordinates L* (whiteness) a* (redness) b* (yellowness)

37.5 2.33 18.2

39.0 2.32 18.9

37.5 2.75 18.6

0.90 0.287 0.40

SE

Fasting live weight (kg) Hot carcass weight (kg) Cold carcass weight (kg) Dressing percentage Non-carcass components (kg)b Carcass cut weights (kg)c Fat tail (kg)

Item

Table 6 Effects of feeding Atriplex halimus L. on meat quality characteristics of fattening Awassi lambs.

b

a Diets were (1) no Atriplex halimus L. (CON), (2) 75 g/kg Atriplex halimus L. (ATR75), and (3) 150 g/kg Atriplex halimus L. (ATR150). b pH measured after thawing.

4. Discussion The objective of this study was to evaluate the effect of partial replacement of wheat straw by A. halimus L. on growth performance, nutrient intake, digestibility, carcass characteristics and meat quality of Awassi lambs fed finishing diet. In addition, cost of gain was estimated to evaluate the effectiveness of inclusion A. halimus L. as an alternative feed in sheep industry compared to the conventional feed diet. The fact that greater levels of NDF in the diet might decrease the DM intake compared to diets containing lower NDF, suggests A. halimus L. as a good candidate to replace wheat straw since their NDF contents is lower (392 vs 700 g/kg). In addition, CP and ADF contents of A. halimus L. were 121 and 200 g/kg, respectively. In this study, nutrient composition of the three diets was similar except for the NDF and ADF content due to their low levels in A. halimus L. compared to wheat straw (Table 1). The shortage and the expensive prices of conventional feedstuffs from one side and great political and social pressure to reduce industrial pollution were the main driving forces behind the use of agro-industrial by products or alternative feedstuffs to be major line of research in our team for several years. In this paper we proved that the inclusion of the A. halimus L. decreased the cost of diets by 8.5 and 16.5 percentages for the ATR75 and ATR150 diets compared to the CON diet (Table 1). Previously, similar data were reported by our research team when barley grain was replaced by Prosopis Juliflora pods (Obeidat et al., 2008; Obeidat and Shdaifat, 2013), or when barley grain was replaced by carob pods (Obeidat et al., 2011); or when soybean meal was replaced by sesame meal and sesame hulls (Obeidat et al., 2009; Obeidat and Aloqaily, 2010; Obeidat and Gharaybeh, 2011) or when soybean meal was replaced by broiler litter (Obeidat et al., 2011, 2012). All experimental animals stayed in a sound health status throughout the experimental period with no signs of health problems. AbuZanat and Tabbaa (2006) reported the same health prominence although they replaced wheat hay by Atriplex species to a higher level (up to 500 g/kg). The similarity in intake results among the experimental groups confirmed the partial replacing possibility of wheat straw by A. halimus L. for Awassi lambs fed finishing diets with no adverse effects on nutrient intakes. However, Abu-Zanat and Tabbaa (2006) reported that DM intake increases when ewes at different physiological stages (late gestation, suckling and after weaning) fed diets containing either 500 or 1000 g/kg A. halimus L. compared to their counterparts ewes fed on control diet. Also, Al-Owaimer et al. (2011) reported an increase in DM intake in sheep fed on diet containing A. halimus L. at level 300 g/kg. The data from Abu-Zanat (2005), who included A. halimus L. at level 250 g/kg and Stringi et al. (2009), who used A. halimus L. as sole diet reported that sheep fed

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A. halimus L. had lower DM intake compared to A. halimus L. free diet. Consistent with the result in present study, Al-Owaimer et al. (2011) showed that ADF intake were lower when compared with CON diet. These results may be due to the lower ADF level content in A. halimus L. compared to the wheat straw. Contrary to the results reported in the herein study, AbuZanat (2005) reported that water intake increase is proportional to Atriplex inclusion to the diets. Similarly, Le Houerou (1991) found that daily water intake range between 7.4 and 10.9 L per lambs and Correal et al. (2000) found that 6.3 L per lambs when using high level of Atriplex in lambs diet, which surpasses the amount of water consumed by sheep fed on the control diets. In general, as the level of salt increase in the diet, water intake increases. This is due to the fact that salty diet increases the urine excretion by increasing the activity of sodium pumps which drives water from cells and to equate the water level, the brain signal to drink more water (Harper et al., 1997). In present study, the level of A. halimus L. was used in acceptable range and do not increase the salinity of diet compared to using in high level or as sole diet. Al-Owaimer et al. (2008) evaluated the effect of using Atriplex in feeding sheep and reported similar ADG among the different experimental diets. Mount of evidence in the literature associate between using Atriplex at higher levels (≥250 g/kg) and depression on performance parameters. For example, Ahmed et al. (2001) showed that ADG of lambs fed diet containing Atriplex species above 250 g/kg was lower than lambs fed diet containing hay. Ben Salem et al. (2005) and Stringi et al. (2009) reported that fed lambs only on Atriplex have reduced in BW due to lower DM intake and digestibility. Abu-Zanat (2005) reported that the addition 250 g/kg Atriplex in fattening diet reduced BW. It is noteworthy to mention that feeding animals on high Atriplex diet decreased DM intake, which necessary to increase the gain. Consistent with our study, Al-Owaimer et al. (2008) reported that digestibility of DM, OM, CP and ADF were not affected when using A. halimus L. compared to the control diet. On other hand, in the same study NDF digestibility were decreased compared with the control group. Munoz et al. (1996) concluded that the Atriplex digestibility showed a wide variability in relation to the physiological phase, and the ratio between stems and leaves. In contrast, Shawket (1999) found that the digestibility of DM, OM and CP was lower in diets containing Atriplex diets. Similarly, Abu-Zanat (2005) reported that digestibility of DM and OM reduced when A. halimus L. fed at level greater than 250 g/kg of dietary DM and this may be related to presence of high level of secondary chemical compounds such as phenols, and tannins. However, in the current study, the level of A. halimus L. that is included in the diets did not negatively impact the nutrient digestibility. In agreement with present study, Al-Owaimer et al. (2008, 2011) reported that Atriplex inclusion on sheep diets did not alter N balance. In our study, we noticed that sheep fed on Atriplex excreted more N in their feces. This may due to the presence of secondary metabolites in the Atriplex which form insoluble proteins, which lead to the formation of indigestible N and excreted in feces (Ben Salem, 1998). In general, N balance in ruminant depends on the availability of metabolizable energy and non-protein compounds in the Atriplex (Le Houerou, 1992). The degradation of non-protein compounds by rumen microorganism in the presence of sufficient amount of energy can improve the utilization and digestion by microorganisms and the host animal (Le Houerou, 1992) to synthesize microbial protein and as a result it stimulates carbohydrate digestion and detoxify secondary compounds (Mayberry et al., 2008; Norman et al., 2008). These compounds could be converted to ammonia in the rumen with inadequate energy in the diet, which is absorbed by the animal, converted to urea and excreted in the urine. In 2005, Ben Salem et al. found that N balance of sheep receiving Atriplex alone was negative while N retained by lambs given

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barley grains as source of energy was positive; they concluded that the availability of energy source in the diet allowed better utilization of Atriplex nitrogen. This process increases the availability of good quality protein entering the small intestine and as a result it improves the N balance as noted in our study. The similarity in digestibility and the chemical composition of the diets influenced the activity of the rumen microbes and as a result it did not affect the pH of rumen fluid. Another possible explanation for the comparable rumen fluid pH values could be the similarity in NDF content in different diets (although the NDF content is slightly lower in the ATR diets compared to the CON diet). The uniformity in NDF contents will equate the time required to ruminate and thus to digest the fiber content with no change in rumen pH. Carcass characteristics and meat quality were comparable among all treatment diets. Consistent with our results, many studies reported that carcass characteristics were not affected when sheep or lambs fed ATR containing diets compared to the control diet (Swingle et al., 1999; Pearce, 2006). Similarly, Aganga et al. (2003) reported that muscle pH, meat color, juiciness, tenderness and overall acceptability were not affected by ATR diets. Hopkins and Nicholson (1999) reported that muscle pH and meat color was not affected, while moisture contents in meats was higher but the differences not significant in sheep that fed on A. halimus that supplemented with hay or grains. However, Al-Owaimer et al. (2008) reported that warm and cold carcass weights as well as fat percentage were lower in ATR containing diet in comparison with animal fed control diet. This result may due to dehydration that is believed to cause weight loss and reduce muscle and hot carcass weight (Pethick et al., 2005). In addition, Pearce et al. (2008) reported that greater lean content and lower carcass fat in sheep grazed saltbush compared to sheep grazed either a grain–hay-based diet or a pasture-stubble paddock. One plausible explanation for the observed differences in the fat content may be due to the high protein: energy ratio available for production (Pearce et al., 2010). The main target of using A. halimus L. in sheep diets is to reduce the cost of feed and/or to improve or at least not affecting carcass characteristics and meat quality. In the present study, using of A. halimus L. did not affect carcass characteristics or meat quality. This shown the possibility of using A. halimus L. as an alternative feedstuffs without causing any adverse effect on carcass characteristics and meat quality. 5. Conclusion Under the condition of the current study, inclusion 75 and 150 g/kg DM A. halimus L. in diets of fattening Awassi lambs did not affect nutrient intake, digestibility, performance or carcass characteristics and meat quality. However, cost of gain improved when A. halimus L. was fed at levels up to 150 g/kg when compared to control diet. Conflict of interest There is no conflict of interest with anyone regarding this manuscript. Acknowledgments The authors wish to thank the Deanship of Scientific Research JUST for the financial support of this project (226/2014). Appreciation is expressed to Majdi Abu Ishmais for assistance in conducting this experiment and laboratory analyses. Appreciation is also expressed to Ibrahim Tahat and the farm staff of the Agricultural Research and Training Unit at JUST.

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