Energy requirements of Dorper×thin-tailed Han crossbred ewes during non-pregnancy and lactation

Journal of Integrative Agriculture 2015, 14(12): 2605–2617 Available online at www.sciencedirect.com

ScienceDirect

RESEARCH ARTICLE

Energy requirements of Dorper×thin-tailed Han crossbred ewes during non-pregnancy and lactation LOU Can1*, SI Bing-wen1*, DENG Kai-dong2, MA Tao1, JIANG Cheng-gang1, TU Yan1, ZHANG Nai-feng1, JI Shou-kun1, CHEN Dan-dan1, DIAO Qi-yu1 1

Feed Research Institute, Chinese Academy of Agricultural Sciences/Key Laboratory of Feed Biotechnology, Ministry of Agriculture, Beijing 100081, P.R.China 2 College of Animal Science, Jinling Institute of Technology, Nanjing 210038, P.R.China

Abstract This experiment was conducted to investigate the energy requirement of Dorper×thin-tailed Han crossbred ewes during non-pregnancy and lactation. Fifteen ewes after parturition were randomly assigned to three treatments: ad libitum (100%) feed intake and 80 or 60% ad libitum intake, and another nine non-pregnant ewes were assigned to a blank control group. Digestibility trials were performed in the non-pregnant ewes and in the lactating ewes on the 20th, 50th, and 80th d of lactation. In parallel with the digestibility trial, a respirometry experiment was conducted to determine the methane and carbon dioxide production with an open-circuit respirometry system that was equipped with respiratory chambers. The net energy (NE) and metabolizable energy (ME) requirements for maintenance and growth were calculated using the carbon and nitrogen balance method. The results revealed that the carbon (C) and nitrogen (N) excretions and energy losses at faeces and urine, as well as the output of methane and CO2, increased significantly with decreasing feed intake (P<0.01). The apparent digestibilities of C in the stages of non-pregnancy and early, middle and late lactation were 55.8–58.3%, 62.5–73.8%, 64.8– 71.3%, and 61.7–65.0%, respectively, and the apparent digestibilities of N were 45.2–51.3%, 73.7–82.7%, 72.8–80.5%, and 73.6–76.5%, respectively. The corresponding energy apparent digestibilities were 52.0–56.3%, 60.7–76.6%, 61.0–68.8%, and 61.4–67.7%, respectively. The ME/DE (digestible energy) values were 79.5–85.9%, 79.4–83.5%, 81.0%–85.3% and 78.6–82.9%, respectively. The maintenance requirements of NE, ME, and the efficiencies of ME utilisation for maintenance during the stages of non-pregnancy and early, middle and late lactation were 215.5, 253.1, 247.7, and 244.7 kJ kg–1 BW0.75 d, and 372.4, 327.1, 320.9, and 362.0 kJ kg–1 BW0.75 d, and 0.58, 0.77, 0.77, and 0.68, respectively. The ME requirement for the growth of non-pregnant ewes was 31.3 MJ kg–1 BW gain. Keywords: net energy, metabolizable energy, ewe, lactation, digestible energy

1. Introduction Received 23 September, 2014 Accepted 11 February, 2015 LOU Can, E-mail: [email protected]; Correspondence DIAO Qi-yu, Tel: +86-10-82106055, E-mail: [email protected] * These authors contributed equally to this study. © 2015, CAAS. All rights reserved. Published by Elsevier Ltd. doi: 10.1016/S2095-3119(14)60963-1

The feeding management of sheep in China is largely based on a foreign nutritional system, such as NRC (2007). However, China is such a huge country with various forage resources and sheep breeds that it is practically unreasonable to cover all the situations with a foreign standard.

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The study of the nutrition requirements of lactation is key in mutton production, which is consistently weak in China, directly influencing the performance of ewes and lambs. Livestock-developed countries that have studied the energy and protein requirements of various species of lactating ewes attach great importance to their feeding standards and update the databases constantly (Fernandes et al. 2007). The energy requirements for the maintenance of ewes are constant (AFRC 1993; NRC 2007); however, there are significant differences in metabolism among different physiological periods. In China, the studies of nutrient requirements in sheep are mainly confined to the growth of fattening sheep, which is rare in lactating sheep. A limited amount of research has focused on native breeds of sheep. Moreover, there is a large gap in research methods and conditions compared to the developed countries, particularly in the use of a facemask in the determination of methane. Furthermore, there are many reports of methane emission in lactating cows (Jentsch et al. 2007; Aguerre et al. 2011) and adult sheep (Zhao et al. 2012), but few focus on lactating ewes. Currently, comparative slaughter is the primary method to research the energy requirements of ruminants (Marshall 1981); however, this study indicates the energy requirements for the maintenance of crossbred ewes using carbon and nitrogen methods during non-pregnancy and lactation, which coincides with animal welfare, as well as the methane emissions as measured by an open-circuit respirometry system. This study will provide the basic data for determining the feed standards of mutton sheep in China.

2. Results 2.1. Digestibility and metabolizability of dietary carbon The effects of different feeding levels on the metabolizability of the dietary carbon of non-pregnant and lactating Dorper×thin-tailed Han crossbred ewes are shown in Table 1. The carbon intake (CI), faecal carbon excretion (FC), urinary carbon loss (UC), methane carbon (CH4-C) and carbon dioxide output (CO2-C) showed significant differences among the three groups and were affected by the feeding levels (100%>80%>60%, P<0.01). The retained carbon in the 100 and 80% groups was greater than in the 60% group during the three periods of non-pregnancy, middle lactation and late lactation (P<0.05); in contrast, an opposite trend was observed during early lactation. During the periods of non-pregnancy and lactation, the apparent digestibility of carbon in the 60% group was significantly higher than that in the 100% group (P<0.05); the digestibility during the periods of non-pregnancy and early, middle and late lactation were 55.75–58.33%, 62.54–73.84%, 64.80–71.25%, and

61.73–65.03%, respectively. Consequently, the percentage of FC/CI exhibited a downtrend with decreasing feeding levels. Meanwhile, the UC/CI was significantly lower in the 100% group compared to the 80 and 60% groups except for during late lactation (P<0.05). The CH4-C/CI decreased with decreasing feed intake and during lactation differed significantly (P<0.01). Conversely, the CO2-C/CI increased with the decreasing feed intake and was significantly different between the 60% group and the other two groups during the three periods of non-pregnancy and early and late lactation (P<0.05). The CI, UC, CH4-C, CO2-C and apparent digestibility obviously decreased as lactation progressed and was the highest during early lactation and lowest during the period of non-pregnancy.

2.2. Digestibility and metabolizability of dietary nitrogen The results of the digestion and metabolism analyses of the nitrogen of ewes during non-pregnancy and lactation are listed in Table 2. The nitrogen intake (NI), faecal nitrogen (FN) and digested nitrogen (DN) significantly decreased with decreasing feed levels (P<0.01). The NI and DN significantly decreased with lactation progression (P<0.05) and were, in fact, higher during lactation than during non-pregnancy (P<0.05). The urinary nitrogen (UN) significantly decreased with decreasing feed levels during lactation (P<0.01) and was also higher during lactation than during non-pregnancy (P<0.05). The nitrogen in the milk was nonsignificant among the three feeding levels (P>0.05) but decreased significantly with lactation progression (P<0.05). There was a trend of nitrogen apparent digestibility that increased with decreasing feed intake and was higher during lactation than during non-pregnancy (P<0.05). The retained nitrogen (RN), RN/NI and RN/DN significantly decreased with decreasing feed levels during lactation (P<0.05). The RN during lactation was significantly higher than during non-pregnancy (P<0.05), and the RN/NI was similar during the different periods (P>0.05); in addition, the RN/DN was higher during lactation, and in the 100 and 80% groups, the difference was significant (P<0.05).

2.3. Digestibility and metabolizability of dietary energy The energy balance from the digestibility trials of the non-pregnant and lactating ewes is shown in Table 3. The gross energy intake, faecal energy (FE) and methane energy (CH4-E) decreased with decreasing feed intake and were significantly different among the three groups (P<0.01). The urinary energy was significantly influenced

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Table 1 Effects of different feeding levels on the C balance of ewes during different periods Items C intake (g d–1)

Periods

Non-pregnancy 20 d of lactation 50 d of lactation 80 d of lactation Non-pregnancy Faecal C (g d–1) 20 d of lactation 50 d of lactation 80 d of lactation Non-pregnancy Urinary C (g d–1) 20 d of lactation 50 d of lactation 80 d of lactation Non-pregnancy C in milk (g d–1) 20 d of lactation 50 d of lactation 80 d of lactation Non-pregnancy CH4-C (g d–1) 20 d of lactation 50 d of lactation 80 d of lactation Non-pregnancy CO2-C (g d–1) 20 d of lactation 50 d of lactation 80 d of lactation Non-pregnancy Retained C (g d–1) 20 d of lactation 50 d of lactation 80 d of lactation Apparent Non-pregnancy digestibility (%) 20 d of lactation 50 d of lactation 80 d of lactation Losses percentage of C intake (%) Faecal C Non-pregnancy 20 d of lactation 50 d of lactation 80 d of lactation Urinary C Non-pregnancy 20 d of lactation 50 d of lactation 80 d of lactation Methane C Non-pregnancy 20 d of lactation 50 d of lactation 80 d of lactation Non-pregnancy CO 2-C 20 d of lactation 50 d of lactation 80 d of lactation

100 641.4 Ba 969.0 Aa 935.5 Aa 748.9 Ba 283.8 Ba 362.7 Aa 329.4 ABa 286.7 Ba 23.5 Da 29.6 Aa 27.4 Ba 25.9 Ca – 138.8 A 48.8 B 10.2 B 37.7 Ca 54.9 Aa 53.6 Aa 42.8 BCa 279.2 CDa 387.7 Aa 328.4 Ba 306.3 BCa 17.21 Ca –6.61 C 147.9 Aa 83.8 Ba 55.8 Cb 62.5 ABb 64.8 Ab 61.7 Bb 44.3 Aa 37.5 BCa 35.2 Ca 38.3 Ba 3.67 Ab 3.09 BCb 2.94 Cc 3.46 ABc 5.88 Aa 5.67 Ba 5.73 Aa 5.72 Aa 43.5 Ab 40.0 B 35.2 C 40.9 Bb

Feeding levels (%)1) 80 531.8 Cb 723.1 Ab 659.8 Bb 615.7 Bb 229.7 Bb 241.4 Ab 228.6 Bb 223.2 Bb 21.4 Db 26.5 Ab 24.9Bb 23.2 Cb – 96.5 A 44.4 B 2.9 C 30.1 DEb 37.3 ABb 34.2 BCb 32.8 CDb 240.1 BCb 309.4 Ab 238.4 BCb 253.4 Bb 10.44 Cb 12.1 C 89.3 Ab 80.9 ABa 56.8 Dab 66.7 Ab 65.4 ABb 63.8 ABa 43.2 Aab 33.3 BCb 34.6 BCa 36.3 Cb 4.03 Aa 3.67 Ba 3.78 ABb 3.77 ABb 5.66 Aab 5.17 Bb 5.18 Bb 5.32 Ba 45.2 Ab 42.9 C 36.2 D 41.2 BCb

60 444.4 Cc 599.9 Ac 509.2 BCc 530.9 ABc 185.2 c 158.3 c 148.6 c 185.6 c 17.3 Cc 23.9 Ac 22.8ABb 21.7 Bc – 113.6 A 52.3 B 6.8 C 22.7 Dc 30.8 ABc 24.5 CDc 25.5 CDc 212.2 BCc 258.6 Ac 202.8 BCc 237.0 ABb 7.10 Cb 14.7 C 58.2 Ac 54.3 ABb 58.3 Ca 73.8 Aa 71.3 ABa 65.0 BCa

SEM2)

P-value

5.90 27.70 39.20 8.06 3.44 21.60 18.50 5.25 0.30 0.22 0.65 0.29 – 14.10 12.10 2.06 0.97 1.33 2.04 0.97 6.04 11.60 8.28 4.94 1.29 14.10 17.70 5.56 0.54 1.97 1.10 0.60

<0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 0.005 <0.001 – 0.197 0.902 0.307 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 0.006 0.508 0.022 0.022 0.056 0.006 0.010 0.021

41.7 Ab 26.2 Cc 28.8 BCb 35.0 ABb 3.89 a 3.99 a 4.55 a 4.09 a 5.10 Ab 5.15 Ab 4.82 Bc 4.80 Bb 47.8 Aa 43.2 AB 40.4 B 44.6 ABa

0.54 1.97 1.10 0.60 0.04 0.15 0.18 0.04 0.15 0.17 0.05 0.12 0.55 1.03 1.26 0.56

0.056 0.006 0.010 0.021 0.003 0.005 0.001 <0.001 0.041 0.087 <0.001 0.005 0.007 0.099 0.097 0.015

1)

Ad libitum (AL, 100%) or restricted to 80 or 60% of the AL intake. SEM, standard error of means. The values with small letters in the same row indicate significant differences (P<0.05). The values with capital letters in the same column indicate significant differences (P<0.05). –, no data. The same as below. 2)

by the different feeding levels (P<0.05) and was the highest in the 100% group and lowest in the 60% group. The di-

gestible energy (DE) and metabolizable energy (ME) in the 60% group were greater than in the 100% group (P<0.05).

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Table 2 Effects of different feeding levels on the N apparent digestibility of ewes during different periods Items1) N intake (g d–1)

Faecal N (g d–1)

Urinary N (g d–1)

N in milk (g d–1)

Digested N (g d–1)

Apparent digestibility (%)

Retained N (g d–1)

RN/NI (%)

RN/DN (%)

1)

Periods Non-pregnancy 20 d of lactation 50 d of lactation 80 d of lactation Non-pregnancy 20 d of lactation 50 d of lactation 80 d of lactation Non-pregnancy 20 d of lactation 50 d of lactation 80 d of lactation Non-pregnancy 20 d of lactation 50 d of lactation 80 d of lactation Non-pregnancy 20 d of lactation 50 d of lactation 80 d of lactation Non-pregnancy 20 d of lactation 50 d of lactation 80 d of lactation Non-pregnancy 20 d of lactation 50 d of lactation 80 d of lactation Non-pregnancy 20 d of lactation 50 d of lactation 80 d of lactation Non-pregnancy 20 d of lactation 50 d of lactation 80 d of lactation

100 30.4 Ca 70.8 Aa 67.2 Aa 47.7 Ba 16.7 Aa 18.8 Aa 18.3 Aa 12.6 Ba 9.08 C 27.2 Ba 30.7 Aa 26.7 Ba – 13.7 A 6.14 B 1.14 B 13.8 Ca 51.9 Aa 48.9 Aa 25.1 Ba 45.2 Cc 73.7 Ab 72.8 ABb 73.6 A 4.67 Ca 11.1 A 12.0 Aa 7.97 Ba 15.4 ABa 15.6 Aa 17.7 Aa 16.7 Aa 34.0 Aa 21.3 BCa 24.4 Ba 22.7 BCa

Feeding levels (%) 80 25.3 Eb 52.8 Ab 48.6 Bb 39.4 Cb 13.1 Ab 12.8 Ab 11.6 ABb 10.4 BCb 8.89 B 23.1 Ab 24.2 Ab 23.8 Ab – 11.0 A 5.33 B 0.85 C 12.2 Db 40.1 Ab 37.1 Bb 29.0 Cb 48.2 Cb 75.9 Ab 76.1 Ab 73.6 AB 3.26 Cb 6.00 AB 7.56 Ab 4.95 BCb 12.9 Ba 11.3 Bb 15.6 ACa 12.6 Bab 26.8 Ab 14.9 Bb 20.6 ABa 17.1 Bab

60 21.1 Dc 40.0 Ab 37.4 Ac 33.9 ABc 10.3 Ac 7.01 Bc 7.33 ABc 7.97 ABc 9.25 B 19.4 Ac 20.5 Ab 21.7 Ac – 10.16 A 5.33 B 0.30 C 10.8 Cc 33.0 Ac 30.0 ABc 25.9 Bc 51.3 Ca 82.7 Aa 80.5 ABa 76.5 BC 1.57 BCc 3.44 ABC 4.20 ABc 3.30 ABCb 7.46 b 8.27 b 11.0 b 9.74 b 14.5 c 10.1 b 13.8 b 12.7 b

SEM

P-value

0.36 3.12 2.65 0.46 0.35 1.33 0.90 0.50 0.14 1.37 1.21 0.39 – 1.37 1.28 0.23 0.11 2.00 2.00 0.49 0.65 1.41 1.15 1.20 0.21 0.84 0.84 0.50 0.74 2.32 1.29 1.23 1.63 3.03 1.76 1.63

<0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 0.002 0.383 0.008 <0.001 0.001 – 0.199 0.879 0.254 <0.001 <0.001 <0.001 <0.001 0.002 0.002 0.004 0.285 <0.001 <0.001 <0.001 0.002 0.002 0.004 0.024 0.037 <0.001 0.002 0.010 0.020

RN, retained nitrogen; NI, nitrogen intake; DN, digested nitrogen.

The milk energy decreased with decreasing feed intake; however, there were no significant differences among the groups. Affected by decreasing feed intake, the CH4-E as a percentage of the GE significantly decreased (P<0.01) but was similar in the four experiments. The digestibility of the GE (DE/GE), the metabolic rate of the GE (ME/GE) and the metabolic rate of the digestible energy (ME/DE) in the 100% group were significantly lower than in the 60% group (P<0.01). The DE/GE during lactation (60.74–76.62%, 60.97– 68.82%, and 61.43–67.74%, respectively) was higher than during the period of non-pregnancy (52.00–56.32%), and the ME/DE was similar in the four experiments (79.53–85.89%, 79.40–83.49%, 80.99%–85.33%, and 78.55–82.93%, respectively).

2.4. Energy requirements for maintenance The established regression relationships between the log of heat production (HP) and metabolizable energy intake (MEI) are shown in Figs. 1 to 4 during the periods of non-pregnancy and early, middle and late lactation, respectively. Because the HP was measured at three levels of feed intake, it was possible to estimate the HP at zero feed intake by extrapolation. Therefore, the antilogs of the intercept in the equations were the net energy for maintenance (NEm) during the different periods. The metabolizable energy for maintenance (MEm) was calculated by iterative computation with the above equations. When the HP was equal to the MEI, the value of MEI was MEm, and the efficiency of the ME utilisation for

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Table 3 Effects of different feeding levels on the energy digestibility of ewes during different periods Items1) GE intake (MJ d–1)

FE (MJ d–1)

UE (MJ d–1)

Milk-E (MJ d–1)

CH4-E (MJ d–1)

DE (MJ d–1)

ME (MJ d–1)

CH4-E/GE (%)

DE/GE (%)

ME/GE (%)

ME/DE (%)

1)

Periods Non-pregnancy 20 d of lactation 50 d of lactation 80 d of lactation Non-pregnancy 20 d of lactation 50 d of lactation 80 d of lactation Non-pregnancy 20 d of lactation 50 d of lactation 80 d of lactation Non-pregnancy 20 d of lactation 50 d of lactation 80 d of lactation Non-pregnancy 20 d of lactation 50 d of lactation 80 d of lactation Non-pregnancy 20 d of lactation 50 d of lactation 80 d of lactation Non-pregnancy 20 d of lactation 50 d of lactation 80 d of lactation Non-pregnancy 20 d of lactation 50 d of lactation 80 d of lactation Non-pregnancy 20 d of lactation 50 d of lactation 80 d of lactation Non-pregnancy 20 d of lactation 50 d of lactation 80 d of lactation Non-pregnancy 20 d of lactation 50 d of lactation 80 d of lactation

100 32.7 Ba 43.8 Aa 43.7 Aa 34.4 Ba 15.7 ABa 17.3 Aa 17.0 Aa 13.3 Ba 0.86 Ba 1.44 Aa 1.54 Aa 0.87 Ba – 61.9 A 24.4 B 25.6 B 2.78 Ca 3.99 Aa 3.94 Aa 3.15 BCa 9.34 Cb 11.6 ABb 11.0 Bc 11.0 Bc 7.34 Cb 9.25 ABb 8.75 Bc 8.94 ABc 8.49 a 9.11 a 9.01 a 9.15 a 52.0 Bb 60.7 Ab 61.0 Ac 61.4 Ac 40.9 Bb 48.4 Ab 48.4 Ac 49.8 Ac 78.6 Bb 79.5 ABc 79.4 ABb 81.0 Ac

Feeding levels (%) 80 27.1 Cb 33.6 Ab 30.9 Bb 28.4 Cb 12.3 Ab 11.6 Aab 11.0 ABb 10.0 Bb 0.72 Bb 1.19 Aab 1.06 Ab 0.68 Bb – 52.9 A 23.0 B 24.3 B 2.21 Db 2.74 ABb 2.52 BCb 2.39 CDb 9.78 Cab 12.5 Ab 11.6 Bb 11.6 Bb 7.84 Cb 10.3 Ab 9.5 ABb 9.70 ABb 8.17 ab 8.17 b 8.15 b 8.41 b 54.5 Bab 65.5 Ab 64.2 Ab 64.8 Ab 43.6 Cb 53.8 Ab 52.7 ABb 54.0 Ab 80.1 Bb 82.1 ABb 82.0 ABa 83.3 Ab

60 22.6 Bc 30.5 Ab 24.2 Bc 24.5 Bc 9.9 ABc 7.1 Cc 7.5 BCc 7.9 BCc 0.51 Cc 1.00 Ab 0.93 Ab 0.56 BCc – 46.1 A 20.2 B 24.1 B 1.67 Cc 2.28 Ac 1.80 BCc 1.87 BCc 10.1 Ca 14.7 Aa 12.4 Ba 12.2 Ba 8.39 Ca 12.6 Aa 10.4 Ba 10.4 Ba 7.37 b 7.47 c 7.46 c 7.66 c 56.3 Ca 76.6 Aa 68.8 Ba 67.7 Ba 46.7 Ca 65.9 Aa 57.5 Ba 57.8 Ba 82.9 a 85.9 a 83.5 a 85.3 a

SEM

P-value

0.30 0.95 1.93 0.33 0.10 0.93 0.48 0.24 0.02 0.09 0.09 0.02 – 6.91 5.90 1.28 0.06 0.09 0.15 0.07 0.13 0.43 0.13 0.10 0.12 0.44 0.14 0.13 0.16 0.08 0.06 0.19 0.74 2.24 0.73 0.58 0.66 2.29 0.79 0.72 0.39 0.69 0.50 0.38

<0.001 <0.001 <0.001 <0.001 <0.001 <0.001 0.027 <0.001 <0.001 0.016 0.006 <0.001 – 0.322 0.884 0.871 <0.001 <0.001 <0.001 <0.001 0.051 0.001 <0.001 0.001 0.009 <0.001 <0.001 <0.001 0.041 <0.001 <0.001 0.004 0.051 0.001 <0.001 0.001 0.009 <0.001 <0.001 <0.001 0.003 <0.001 0.001 <0.001

GE, gross energy; FE, fecal energy; UE, urinary energy; CH4-E, methane energy; DE, digestible energy; ME, metabolizable energy.

maintenance (km) was deduced from the NEm/MEm. All of the values of NEm, MEm and km are shown in Table 4.

2.5. Energy requirement of the non-pregnant ewes for growth During the period of non-pregnancy, the ME of the diet was partly used for MEm and the remaining for the production of

weight gain (MEg). The MEg was simply the energy that was deposited in the gain; the regression relationship between average daily gain (ADG) and MEI is shown in Fig. 5. The equation was as follows: MEI=31.2785(±5.1926)×ADG– 8 828.96(±549.8) (RMSE=589.5, r2=0.838, n=9, P<0.001), where MEI was in kJ d–1, and ADG was in g d–1. The MEg requirement of the non-pregnant ewes was 31.28 MJ kg–1 ADG.

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2.80

log10HP (kJ kg–1 BW0.75 d)

log10HP (kJ kg–1 BW0.75 d)

2610

2.76 2.72 2.68 2.64 2.60 450

500

550

600

650

Metabolizable energy intake (kJ kg BW –1

0.75

d)

2.75 2.70 2.65 2.60

Fig. 3 The relationship between the log of HP and the MEI of Dorper×thin-tailed Han crossbred ewes during middle lactation. log10HP (kJ kg–1 BW0.75 d)=2.3940(±0.0329)+[0.00035(±0.00 0039)×MEI (kJ kg–1 BW0.75 d)]; r2=0.8891; root mean square error=0.0197; n=12; P<0.001.

2.96

2.84 log10HP (kJ kg–1 BW0.75 d)

log10HP (kJ kg–1 BW0.75 d)

2.80

2.55 500 600 700 800 900 1 000 1 100 1 200 Metabolizable energy intake (kJ kg–1 BW0.75 d)

700

Fig. 1 The relationship between the log of heat production (HP) and the metabolizable energy intake (MEI) of Dorper×thin-tailed Han crossbred ewes during non-pregnancy. log10HP (kJ kg–1 BW0.75 d)=2.3334(±0.0230)+[0.00064(±0.000040)×MEI (kJ kg–1 BW0.75 d)]; r2=0.9728; root mean square error=0.0074; n=9; P<0.001.

2.85

2.92 2.88 2.84 2.80 2.76 800

900

1 000

1 100

1 200

1 300

2.80 2.76 2.72 2.68 2.64 600

Metabolizable energy intake (kJ kg–1 BW0.75 d)

Table 4 The energy requirements of ewes during different periods NEm MEm km Periods (kJ kg–1 BW0.75 d) (kJ kg–1 BW0.75 d) (NEm/MEm) Non-pregnancy 215.5 372.4 0.58 Early lactation 253.1 327.1 0.77 Middle lactation 247.7 320.9 0.77 Late lactation 244.7 362.0 0.68 NEm, net energy for maintenance; MEm, metabolizable energy for maintenance; km, the utilisation efficiency of ME for maintenance.

3. Discussion 3.1. Dietary carbon balance The study of the C metabolism of ruminants has seldom contributed to establishing the connection between N and

Fig. 4 Respiration HP of different levels of MEI of Dorper×thintailed Han crossbred ewes during late lactation. log10HP (kJ kg–1 BW0.75 d)=2.3886(±0.0381)+[0.00047(±0.000050)×MEI (kJ kg–1 BW0.75 d)]; r2=0.9166; root mean square error=0.0145; n=10; P<0.001.

Metabolizable energy intake (kJ kg–1 BW0.75 d)

Fig. 2 The relationship between the log of HP and the MEI of Dorper×thin-tailed Han crossbred ewes during early lactation. log10HP (kJ kg–1 BW0.75 d)=2.4032(±0.0454)+[0.00045 (±0.000046)×MEI (kJ kg–1 BW0.75 d)]; r2=0.8890; root mean square error=0.0189; n=14; P<0.001.

650 700 750 800 850 900 Metabolizable energy intake (kJ kg–1 BW0.75 d)

14 000 13 500 13 000 12 500 12 000 11 500 11 000 10 500 10 000

0

50 100 150 Average daily gain (g d–1)

200

Fig. 5 Relationship between the metabolizable energy intake and the average daily gain of Dorper×thin-tailed Han crossbred ewes during the non-pregnancy period. MEI (kJ d –1)=31.2785(±5.1926)×Average daily gain (ADG, g d –1) –8 828.96(±549.8); root mean square error=589.5; r2=0.838; n=9; P<0.01.

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energy metabolism. The quantity of carbohydrate in the body is less but stable; consequently, the C was utilised or deposited mainly in the forms of fat and protein. In our study, C losses in the forms of faeces, urine, CH4 and CO2 were significantly affected by the feeding levels during the periods of non-pregnancy and lactation. Chandramoni et al. (1999) reported that at approximately the maintenance level, the FC, CO2-C, and CH4-C were non-significantly different except for the UC of the sheep that were fed different roughage and concentrate ratios. Jentsch et al. (2009) demonstrated that the CO2 emission per kg of DM intake in cattle amounted to 0.55 kg (0.15 kg of C) and was relatively constant irrespective of the live weight and performance. Similarly, the output of CO2-C was greater at low levels of feeding and decreased as the feed intake increased (0.14 to 0.7 kg kg–1 DM) in this study. The CH4 emissions are relative to the special digestion characteristics of ruminants that are inevitable; therefore, the losses of CH4-C must be considered. In this experiment, the CH4 emissions fluctuated between 4.80 and 5.88%, which were greater than the value reported by Chandramoni (1999), possibly because of the differences in the diet, animal, feeding level, and/or physiological period. According to Hales (2012), as a proportion of the total C loss, increasing wet distiller grains with a soluble concentration in the diet caused a linear increase in the C excretion in urine and faeces, and the apparent digestibilities ranged from 64.6 to 74.3%. The total C loss was 75.5% when the sheep were fed at approximately the maintenance level (Blaxter and Wainman 1964); these values were close to the results of the early lactation group in this experiment. The urinary C and CH4-C losses as a percentage of the C-intake in our study were significantly greater in the results of Chandramoni (1999), but the values of CO2-C were similar. In addition to early lactation, the amount of retained C decreased significantly when the feed intake decreased, mainly due to the highest secretion of milk C in the 100% group. Simultaneously, much higher faecal C and CO2-C values were found in the 100% group than in the 80 and 60% groups. From early to late lactation, the UC, milk C, CH4-C and CO2-C decreased gradually with the decreasing CI; moreover, these values were the lowest during the period of non-pregnancy. However, their proportions of CI were always constant. Correspondingly, there was a similar trend in the apparent digestibility of the C in the diet. Therefore, it was obvious that lactating improved the digestion and absorption of diet C. During lactation, the metabolism of the mammary gland and hepatic gluconeogenesis were enhanced. The speed of lipid metabolism was increased; in contrast, the lipid synthesis rate in adipose tissue decreased, particularly during early lactation (McNamara 1994; McNamara and Baldwin 2000), as the body’s storage was used to meet the lactation requirement. Furthermore, the

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requirement for the matrix maintenance increased, resulting in a clearly significantly higher urinary excretion of C during lactation than during non-pregnancy.

3.2. Dietary nitrogen balance In our study, the FN, UN and RN decreased significantly with decreasing feeding levels, which was consistent with the results of Ma et al. (2014), in which the levels of feed intake directly influenced the outflow rate and microbial protein synthesis of the rumen in addition to the amount of amino acids in the duodenum, thereby affecting the digestion and metabolism of dietary nitrogen (Merchen et al. 1986). During lactation, the UN significantly decreased with decreasing feeding levels, in agreement with the results of Stobo et al. (1973), which could be explained by the higher ruminal absorption of N than during the production of urea cycle into the urea recycling due to a higher level of N intake. Therefore, the dietary N was extensively absorbed in the form of ammonia, which was used synthesised into urea in the liver and finally excreted in the urine (Sun et al. 2004). This absorption was the main reason that the UN during lactation was significantly higher than during non-pregnancy; moreover, lactation enhanced the metabolism of the body, which improved the protein requirement for maintenance, especially in the mammary glands. In our experiment, the apparent digestibility of N during lactation was significantly higher than during non-pregnancy; in addition, there was a decrease with lactation progression, indicating that lactation improved the digestion and absorption of the body. There was a strong relationship between this effect and the intensity of lactation. Regarding the milk excretion of N, there was a decreasing trend with decreasing feed intake; nevertheless, this decrease was significant with lactation progression and demonstrates that the increase in the feed intake contributed to lactation. However, the body storage of ewes could be consumed to meet the requirement of lactation (Robinson et al. 1970), thereby weakening the influence of feed intake on lactation. The RN decreased significantly with decreasing feeding levels not only during lactation but also during non-pregnancy, which was consistent with the results of other published studies (George et al. 2005; Singh et al. 2008). The available literature shows that the RN is closely related to the NI and ruminal fermentable energy, which are the limiting factors in microbial protein synthesis (Chandramoni et al. 2000); therefore, the rumen microbes will produce more bacterial proteins when they are abundant, thereby increasing the digestible and absorbable N of the ewes. The digestion and metabolism of C and N are inseparable. Orskov et al. (1970) found that the perfused available carbohydrates in the large intestine could increase the

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excretion of faecal and urinary N, thereby reducing the digestibility of N, indicating that the different sites of energy digestion could change the amount of absorbable N, ultimately influencing the digestibility of N (Owens et al. 1983). In accordance with findings in bulls (Kishan et al. 1986), the energy intake levels influenced the excretion of C and N in the urine, and there was a highly significant correlation between the urinary C and N excretion, consistent with our results (Blaxter and Wainman 1964). Thus, in this study, the UN gradually decreased with the decreasing feeding levels, possibly related to the decreasing C and energy in the urine.

3.3. Dietary energy balance It is very important to research the effect of the level of feeding in the energy metabolism of ruminants, particularly during lactation (Reid 1961; Wagner and Loosli 1965). We already know that losses of energy in the faeces and urine vary with the nature of the diet. The excretion of faecal energy increased with the increasing GE intake (Tyrrell et al. 1975; Ferrell et al. 1976), as well reflected in our experiments, mainly due to the increasing feed intake accelerating the speed of chyme moving through the intestine, thereby shortening the time between feeding and reaching the microbes or digestive enzymes, resulting in a lower digestibility (McDonald 2002). Chandramoni et al. (2000) found that when the sheep were fed at approximately the maintenance level (the roughage/concentrate of the diet was 50:50), the urinary E losses as a percent of GE intake were 2.9%, which was within the range of 2.25 to 3.85% of the 60% group in our experiment. The heat of combustion of the urine was 9.7 kcal g–1 C and did not vary with the diet (Blaxter et al. 1966); however, in our experiment, the values decreased with the decreasing feed intake and were 7.06–8.74, 10.01–11.64, 9.73–13.45 and 6.16–8.03 kcal g–1 C during the stages of non-pregnancy and early, middle and late lactation, respectively. Energy losses in the form of CH4 are a considerable proportion of the GE, but measuring using respiration chambers is difficult and costly; therefore, this value is generally estimated by empirical equations in most published studies (Yang et al. 1997). In this experiment, CH4 production was determined by an open-circuit respirometry system, as the ratio of GE intake ranged from 7.34 to 9.15% and decreased significantly with decreasing GE intake. This trend was contrary to some published studies (Blaxter and Wainman 1961; Deng et al. 2012; Xu et al. 2012). Luna et al. (2010) found that the apparent digestibilities of GE by Alpine dairy goats were 65.6, 67.8 and 70.8% of the ad libitum and 73.4, 75.0 and 77.4% of the intake near the maintenance level during early, middle and late lactation, respectively. Compared with our results, the values were similar; however, the trends were contrary as apparent

digestibilities ranked as follows: late
3.4. Energy requirements for maintenance One of the most widely acknowledged factors of the MEm is the level of feed intake leading to different levels of heat increase. Andersen (1980) demonstrated the effects of body weight, feeding level, genotype and sex on the maintenance requirements in detail. However, the effects of variations in the feeding level on the maintenance energy requirements occur slowly and could not be detected by short-term calorimetric studies. Calculating from a well-designed comparative slaughter experiment, the NEm and MEm of the sheep were 35 and 62 kcal kg–1 BW0.75 d (146.44 and 259.41 kJ kg–1 BW0.75 d), respectively; therefore, the km (NEm/MEm) was 0.56 (Garrett et al. 1959). There were large differences compared with Rattray’s (1973) results, in which the NEm and MEm ranged from 62.5 to 74.9 and from 96.7 to 124.4 kcal kg–1 BW0.75 d (261.50–313.38 and 404.59–520.49 kJ kg–1 BW0.75 d) for lambs, yearlings, ewes and wethers, respectively. The NEm represented the basal metabolism as calculated from the extrapolation of the regression line

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between the log10HP and ME intake values, which in our study were 215.5, 253.1, 247.7 and 244.7 kJ kg–1 BW0.75 d, and the corresponding MEm values were 372.4, 327.1, 320.9 and 362.0 kJ kg–1 BW0.75 d. Within the same sheep species, the NEm and MEm were 263 and 381 kJ kg–1 BW0.75 d as reported by Deng et al. (2012) and 271.0 and 345.01 kJ kg–1 BW0.75 d as reported by Xu et al. (2012), which were within the range in our experiment. Additionally, our NEm values were lower than the value (310.75 kJ kg–1 BW0.75 d) of tropical lambs (Silva et al. 2003), and the MEm values during lactation were similar to the estimated values (342 kJ kg–1 BW0.75 d) of Baluchi sheep (Kamalzadeh and Shaban 2007). From equation of 1-year-old lactating ewes as recommended by the AFRC (1993), NEm (MJ d–1)=1.0×0.23× (BW/1.08)0.75+0.0096×BW. There were hardly any differences among the values that were predicted by this equation (243.34, 243.42 and 243.92 kJ kg–1 BW0.75 d during early, middle and late lactation, respectively), although these values were very close to the results that were measured in practice. Nevertheless, all of these values were lower than estimated by CSIRO (2007; 272 kJ kg–1 BW0.75 d) in 1-year-old female sheep. In this experiment, there were large differences among the km (NEm/MEm) values during the periods of non-pregnancy and early, middle and late lactation, which were 0.58, 0.77, 0.77 and 0.68, respectively. For the diets that were finely mixed and pelleted, were all forage, or were primarily first cut forages, the ARC (1980) recommends a linear equation: km=0.35qm+0.503, where, qm=ME/GE. Meanwhile, the equation that is recommended by INRA (1989) is km=0.287qm+0.554. Thus, the km should be varied with the ME/GE as affected by the different intake levels and physiological periods in our study. In addition, different approaches to calculating the HP (C-N balance in our study) and CH4 (respiratory chamber in our study) will permit the comparison of the discrepancies of km with published studies (0.64, Galvani et al. 2010; 0.69, Deng et al. 2012; 0.67, Xu et al. 2012). Compared with other C-N balance studies, our HP of non-pregnant ewes was lower than the estimations in Muzaffarnagari sheep (398.32–445.18 kJ kg–1 BW0.75 d) (Chandramoni et al. 1999) and in Manchega sheep (407 kJ kg–1 BW0.75 d) (Fernández et al. 2012). Uniformly, the km was also lower than in the calculations in Muzaffarnagari sheep (0.66–0.69; Chandramoni et al. 1999) and in cattle (0.70–0.72; Hales et al. 2012).

3.5. Energy requirements for the growth of non-pregnant ewes Because of the limitation of the C-N balance method, we could not determine the empty body weight (EBW). From the regression relationship between the ADG and MEI, the

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MEg requirement of non-pregnant ewes was 31.28 MJ kg–1 ADG. Deng et al. (2012), from the allometric relationships between the body energy and EBW to estimate the retained energy in the body, the MEg requirement was 28.97 MJ kg–1 ADG 50 kg–1 BW in ram lambs as calculated by NEg/kg and was slightly lower than our value above. Cannas (2004) stated the MEg of AFRC, CSIRO and INRA were 39.81, 40.64 and 63.42 MJ kg–1 ADG, which were much greater than that in our study.

4. Conclusion In conclusion, the NEm were 215.5, 253.1, 247.7 and 244.7 kJ kg–1 BW0.75 d, the corresponding MEm were 372.4, 327.1, 320.9 and 362.0 kJ kg–1 BW0.75 d, and the km were 0.58, 0.77, 0.77 and 0.68 during the periods of non-pregnancy and early, middle and late lactation, respectively. The MEg requirement of the non-pregnant ewes was 31.3 MJ kg–1 ADG.

5. Materials and methods This study was conducted from October 2012 to January 2013 at the Experimental Station of the Chinese Academy of Agricultural Sciences (CAAS) in Nankou, Beijing, China. The animals were kept in an enclosed facility that was equipped with heating radiators, and the mean maximum and minimum temperatures inside the facility during the experimental period were 27.4 and 11.5°C, respectively. The experimental procedures were approved by the Animal Ethics Committee of CAAS, and humane animal care and handling procedures were followed throughout the experiment.

5.1. Digestibility and respirometry trials Fifteen 14-mon-old Dorper×thin-tailed Han crossbred ewes ((51.19±3.70) kg) were synchronized of oestrus with intravaginal sponges containing progesterone for 12 d. A total of 48 h after sponge removal, the ewes were treated with transcervical artificial insemination. 40 d later, the ewes were examined by ultrasonography for pregnancy. The lactating ewes were assigned randomly into three levels of feed intake: ad libitum and 80 and 60% ad libitum with five ewes in each level. According to the NRC (2007), the experimental diets were formulated as a pelleted mixture (Table 5). The ewes were dewormed via the administration of ivermectin (0.2 mg kg–1 BW) before the trial, were fed once daily at 08:00 and had free access to clean water at all times. Three digestion trials were conducted at 20, 50, and 80 d of lactation, which lasted 10 d after the 7-d adaptation period. In addition, another nine healthy non-pregnant ewes were grouped randomly into the above three intake levels to perform the digestibility and respirometry experiments.

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Table 5 Ingredients and nutritional composition of the diets (% DM) Items Ingredients Chinese wildrye hay Corn Soybean meal CaHPO4 CaCO3 NaCl Mineral/Vitamin premix1) Total Nutritional composition2) GE (MJ kg–1) DM (% as fed) Ash CP EE NDF ADF Ca P 1)

2)

Content (%) Non-pregnant

Early lactation

Mid lactation

Late lactation

60.0 25.7 12.4 0.40 0.70 0.50 0.30 100

40.0 33.1 25.0 0.68 0.47 0.50 0.30 100

50.0 28.1 19.8 0.78 0.57 0.50 0.30 100

55.0 28.9 17.0 0.78 0.57 0.50 0.30 100

19.06 84.7 3.21 11.1 7.72 40.1 23.5 0.48 0.36

18.33 84.7 1.27 18.3 7.67 33.2 17.6 0.46 0.44

18.07 86.5 2.63 17.3 7.83 37.8 20.1 0.51 0.48

17.96 86.0 3.66 15.5 8.54 38.1 20.9 0.51 0.48

The premix provided the following per kg of diet: VA 30 000 IU, VD 10 000 IU, VE 100 mg, Fe 90 mg, Cu 12.5 mg, Mn 50 mg, Zn 100 mg, Se 0.3 mg, I 0.8 mg, and Co 0.5 mg. GE, gross energy; DM, dry matter; CP, crude protein; EE, ether extract; NDF, neutral detergent fibre; ADF, acid detergent fibre. The data are determined values.

During the trials, the animals were confined in individual metabolism cages (1.2 m×0.6 m). The amount of feed intake in the ad libitum group was based on that from the previous day and adjusted dynamically to ensure approximately 10% remaining from the total. During the digestion trials, lambs were not allowed to stay with ewes except on the time of suckling. The times for single lamb artificial suckling were at 09:00, 15:00 and 21:00 daily. All of the lambs were weighed at the beginning and end of suckling to measure the milk production of the ewes. In parallel with the digestibility trial, a respirometry experiment was conducted to determine the methane (CH4) and carbon dioxide (CO2) production with an open-circuit respirometry system simultaneously with the oxygen (O2) consumption (Sable Systems International, Las Vegas, NV, USA). The system was equipped with 3 polycarbonate respiratory chambers; therefore, the 15 ewes were taken turns to measure the CH4 production on days 1, 3, 5, 7, and 9 of the 10-d digestibility period. After a 24-h adaption period for each group, the CH4 production was determined over a 24-h period (Deng et al. 2012). When being moved in and out of the respiratory chamber, each ewe was weighed, and the average of these weights was calculated as the calorimetry weight.

that energy is retained in the forms of protein and fat is the presupposition of the carbon and nitrogen balance method (C-N balance) (McDonald 2002). The quantities of protein and fat that are stored can be estimated by carrying out digestion and respirometry trials to determine the difference between the amounts of C and N entering and leaving the body. The source of C and N entering the body is feed, and the main excretion routes are faeces and urine. However, C also leaves the body of ruminants as CH4 and CO2. The quantity of protein stored is calculated by multiplying the retained N by 6.25, as body protein is assumed to contain 0.16 kg N kg–1. Body protein also contains 0.52 kg C kg–1; therefore, the amount of C that is stored as protein can be calculated. The remaining C is stored as fat, which contains 0.767 kg C kg–1. Fat storage is calculated by dividing the C balance, less that stored as protein, by 0.767. The caloric values were 39.75 MJ kg–1 for fat and 23.85 MJ kg–1 for protein. The calculation of the retained energy (RE, kJ) refers to the formula of Fernández et al. (2012). The calculation process is illustrated in Fig. 6. And the heat production (HP, kJ) was calculated as the difference between metabolizable energy intake and RE.

5.2. Carbon and nitrogen balance

The daily feed intake and orts were recorded and sampled to measure the dry matter (DM), organic matter (OM), gross energy (GE), crude protein (CP), ether extract (EE), neutral

As carbohydrate storage in the body is relatively constant,

5.3. Measurements

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Respirometry trials

Digestion trials

Fecal N–(Fecal N+Urinary N)

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Fecal C–(Fecal C+Urinary C)

CH4-C, CO2-C

Retained C (g)

Retained N (g) ×6.25 Protein retention (g)

×0.52

Retained C in protein (kJ)

×23.85

Retained C in fat (g)

Retained energy in protein (kJ)

×100/76.7×39.75 Retained energy in fat (kJ)

Energy retetntion (kJ)

Fig. 6 The calculation process of the carbon and nitrogen balance method.

detergent fibre (NDF), acid detergent fibre (ADF), Ca and P (Deng et al. 2013). The faeces were weighed daily, and a sample of 10% was collected to analyse the DM, OM, GE, CP, NDF, and ADF. Urine was also collected daily in a bucket containing 100 mL of 10% (v/v) H2SO4. The total volume was measured and then diluted to 5 L with water, and then 30 mL was collected as a sample, stored at –20°C to analyse the GE and CP after gathering. The samples of feed, orts and faeces for each ewe were pooled to a composite sample, dried at 65°C, and ground through a 1-mm sieve for analysis. Before the lamb sucked milk, 10 mL of milk was sampled daily at 09:00, 15:00, and 21:00. After one trial, the milk sample was pooled and lyophilised (LGJ12B vacuum freeze drier, Song Yuan Hua Xing Technology Co. Ltd., Beijing, China) before being stored at –4°C). The milk production of each lactating ewe was determined as the weight difference of the lambs between starting and ending sucking milk.

5.4. Chemical analyses According to the procedure of AOAC (1990), the DM was measured in an oven at 105°C for at least 8 h. The ash was determined via combustion in a muffle furnace at 600°C for 8 h, and the OM was calculated as the difference between the DM and ash. The analyses of the NDF and ADF were performed according to Van Soest et al. (1991). The Kjeldahl method was used to measure the total nitrogen (KDY-9830 automatic Kjeldahl analyser, Tongrunyuan Co. Ltd., Beijing,

China); then, the CP was multiplied by the coefficient 6.25. The GE was measured using a bomb calorimeter (6400, PARR Instrument Company, Moline, USA). Before the energy determination, 8 mL of urine was absorbed by 3 pieces of filter papers and dried in an oven at 65°C. The calorie content of the filter paper was also measured. The carbon was determined using an elemental analyser (2400 series II CHNS/O analyser, Perkin Elmer Co., Shelton, USA).

5.5. Calculations and statistical analyses The metabolic energy parameters were determined through digestion and respirometry trials during non-pregnancy and lactation. The digested energy (DE) of the diet was calculated as the difference between the GE intake and faecal energy (FE). The metabolizable energy (ME) was equal to the DE less the urinary energy (UE) and methane energy (CH4-E). The heat production (HP) was calculated as the difference between the metabolizable energy intake (MEI) and the RE, which was calculated as the sum of energy that was deposited in the forms of adipose and protein by the carbon-nitrogen balance method. The data were analysed as a completely randomised design using SAS (ver. 9.2, SYSTAT Institute, Inc. Evanston, IL, USA). All of the analyses were performed using PROC ANOVA, and the means were compared using the Duncan’s test when a significant difference (P<0.05) was detected. The linear regression analyses were conducted with PROC REG.

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Acknowledgements This study was funded by the Ministry of Agriculture of China and was conducted as part of the National Technology Program of the Meat Sheep Industry of China (CARS-39). We thank Ms. Nie Mingfei, Dr. Li Yanling, Ms. Chen Xiaolin, Ms. Cui Xiang, Ms. Zhang Lixia and Ms. Qi Minli from the Feed Research Institute of Chinese Academy of Agricultural Sciences, and Ms. Jia Jingwen and Ms. Wang Meng from Beijing University of Agriculture, China, for their technical assistance.

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