animal Z. G. Wen 1,2a, Y. Jiang 1,3a, J. Tang 1,3, M. Xie 1, P. L. Yang 2 and S. S. Hou 1

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1 Animal (2016), 10:9, pp The Animal Consortium 2016 doi: /s x animal Effect of feed consumption levels on growth performance and carcass composition during the force-feeding period in foie gras production of male Mule ducks Z. G. Wen 1,2a, Y. Jiang 1,3a, J. Tang 1,3, M. Xie 1, P. L. Yang 2 and S. S. Hou 1 1 Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing , China; 2 Feed Research Institute, Chinese Academy of Agricultural Sciences, Beijing , China; 3 College of Animal Science and Technology, China Agricultural University, Beijing , China (Received 4 June 2013; Accepted 26 January 2016; First published online 7 March 2016) In order to avoid excess feed consumption during the force-feeding period in foie gras production, a dose-response experiment with seven feed consumption levels (450, 540, 630, 720, 810, 900, 990 g/day per bird) was conducted to evaluate the effects of feed consumption levels on growth performance and carcass composition of male Mule ducks from 91 to 102 days of age. One-day-old Mule ducklings (sterile and artificial hybrid of male Albatre Muscovy duck and female Pekin duck were fed a two-phase commercial diets for ad libitum intake from hatching to 91 days of age, followed by graded feeding levels of a corn diet by force-feeding from 91 to 102 days of age. Fifty-six 91-day-old male Mule ducks with similar BW were randomly assigned to seven treatments, with eight birds per treatment. Birds were housed in individual pens. At 102 days of age, final BW was measured and BW gain and feed conversion ratio of ducks from each treatment were calculated from day 91 to 102, and then all ducks were slaughtered to evaluate the yields of skin with subcutaneous fat, abdominal fat, breast meat (including pectoralis major and pectoralis minor), leg meat (including thigh and drum stick), and liver. Significant differences in BW gain, total liver weight and liver relative weight were observed among the treatments ( P < 0.001). According to the broken-line regression analysis, the optimal feed consumption levels of male Mule ducks from 91 to 102 days of age for maximum BW gain, total liver weight and liver relative weight were 217, 227 and 216 g feed/kg BW 0.75 per day, respectively. Keywords: ducks, feed consumption level, force-feeding, production performance, foie gras Implications Mule ducks have a high capacity for foie gras production. Overfeeding can induce a strong accumulation of lipids in the liver. In foie gras production, high level of corn-based feed is force-fed into the esophagus of Mule ducks. However, the optimum amount of feed consumption that should be supplied to maximize growth performance and foie gras yield is not clear. Therefore, this study helps to know optimum feed consumption level that should be supplied not only to maximize the growth performance and total liver yield, but also to minimize the adverse effects of excessive feed intake on nutrient digestibility and utilization resulting in high nutrient excretion. Introduction In waterfowl, a carbohydrate-rich corn-based diet for two weeks is commercially used to increase hepatic fatty acid a These two authors contributed equally to this work. houss@263.net synthesis in foie gras production (Hermier et al., 1991), because liver in avian species is considered as the major lipogenic organ. Overfeeding increases significantly lipid levels in duck meat and liver (Zanusso et al., 2003; Molee et al., 2005; Chartrin et al., 2006a). It is generally accepted that the net balance between de novo lipogenesis, fatty acid uptake and fatty acid oxidation can explain fat deposition in overfed waterfowl (Hermier et al., 1991; Hansen and Walzem, 1993; Fournier et al., 1997). Mule duck (a sterile hybrid of male Albatre Muscovy duck and female Pekin duck) has high ability for foie gras production (André et al., 2007). In a study conducted to compare the response of Pekin ducks and Mule ducks to overfeeding, Chartrin et al. (2006b) found that Mule ducks showed a higher production of foie gras than Pekin ducks. By comparison with Pekin ducks, liver weight was increased eight-fold from Mule ducks in 2 weeks of overfeeding (Chartrin et al., 2006a). Mule ducks provide the major part of duck foie gras produced in China and France (Pingel, 2009). Feeding levels affect BW, liver yield, and fat deposition during the force-feeding period in Mule ducks 1417

2 Wen, Jiang, Tang, Xie, Yang and Hou Table 1 Composition and main characteristics of starter, grower and force-feeding diets Composition (%) Commercial starter diet (0 to 21 days of age) Commercial grower diet (21 to 91 days of age) Force-feeding diet (91 to 102 days of age) Corn Soybean meal Dicalcium phosphate Limestone fine Premix Sodium chloride DL-Methionine Total Characteristics 2 (%) Metabolizable energy 3 (MJ/kg) CP Calcium Available phosphorus Crude fat Total methionine Total lysine Premix provided the following per kg of diets: Cu as CuSO 4 5H 2 O 10 mg; Fe as FeSO 4 7H 2 O 60 mg; Zn as ZnO 60 mg; Mn as MnSO 4 H 2 O 80 mg; Se as NaSeO mg; I as KI 0.2 mg; Choline chloride 1000 mg; vitamin A IU; vitamin D IU; vitamin E 20 IU; vitamin K 3 2 mg; thiamin 2 mg; riboflavin 8 mg; vitamin B 6 4 mg; vitamin B mg; pantothenic acid 20 mg; nicotinic acid 50 mg; folic acid 1 mg; biotin 0.2 mg. 2 Calculated values. 3 Values were calculated according to the ME n of feedstuffs for poultry provided by NRC (1994). 4 The numbers were analyzed values. (Chartrin et al., 2007). In practice, the optimum amount of feed supply that should be recommended to maximize growth performance and fatty liver yield is not clear. Excessive feed consumption in ducks negatively affected digestibility and utilization of nutrients (Zhang et al., 2007), which resulted in a large amount of manure and litter, which cause pollution problems (Yokota, 1976; Yokota and Ueda, 1981). In addition, reduced utilization of nutrients will increase costs of production per gram foie gras. In fact, the focus of force-feeding ducks should be on maximizing duck production with minimum feed cost. Quantification of feed consumption during the force-feeding period is important to improve economic benefit through better feed utilization and less feed cost. At present, the optimal amount of feed consumption is not clear in force-fed Mule ducks and experimental data for the optimal feed supply level during the force-feeding period is limited. Therefore, in order to avoid excess feed consumption in foie gras production of Mule ducks, the objective of this study was to investigate the effects of feed supply levels on growth performance and carcass composition to determine the optimum amount of feed supply that should be recommended not only to maximize the growth performance and total liver yield, but also to minimize the accumulation of wastes that are produced by duck industry. Material and methods All procedures of the present study were approved by welfare committee of the Institute of Animal Science of Chinese Academy of Agricultural Sciences. Animals and diets Male Mule ducklings (sterile and artificial hybrid of male Albatre Muscovy duck and female Pekin duck) hatched on the same day were obtained from waterfowl breeding center of Chinese Academy of Agricultural Sciences. They were fed a commercial starter diet containing 205 g/kg CP and MJ ME/kg from hatching to 21 days of age, and a grower diet containing 168 g/kg CP and MJ ME/kg from 22 to 91 days of age. Then the birds were fed a corn diet by force-feeding from 91 to 102 days of age. The corn diet was prepared in mash form and was analyzed containing 83 g/kg CP and 3.3 g/kg crude fat. The calculated ME value was MJ/kg. During the force-feeding period, the corn diet for each duck was first weighed and mixed with tap water (1 : 1, 20 C water temperature) for 2 h before feeding, and then it was quantificationally introduced into the enlargement of the ducks esophagus. Composition and main characteristics of starter and grower diets and force-feeding diet are shown in Table 1. Experimental design and rearing management A total of 80 male Mule ducklings were conventionally reared on the floor from hatching to 91 days. During this period, the birds had free access to water and feed and lighting was continuous. The temperature was kept at 33 C (at floor level) from 1 to 3 days of age, at 30 C from 4 to 7 days of age, at 27 C from 8 to 15 days of age, and then it was reduced gradually to 20~24 C. The humidity was 20% from 1 to 3 days of age and then gradually increased to 65%. At 91 days of age, all ducks were weighed 1418

3 The optimal feed consumption level of Mule ducks Table 2 Effects of feed consumption levels from 91 to 102 days of age on growth performance of male Mule ducks Feed consumption levels (g/day per bird) Final BW 1 (g) BW gain 1 (g/bird per day) FCR d 54.8 d d 62.9 c c 69.4 c b 81.1 b a 92.9 a a 99.5 a a 98.3 a 9.02 SEM P-value < < FCR = feed conversion ratio 1 Data were based on all ducks (n = 8 birds/ treatment); the force-feeding period lasted 12 days from 91 to 102 days of age. 2 SEM: pooled standard error of the mean. a,b,c,d Mean values in the same column with no common superscript differ significantly (P < 0.05). individually, and 56 birds with similar weights were randomly allotted to raised wire-floor pens (1 2 m) with one bird per pen. There were seven dietary treatments, each containing eight replicate birds. The treatment groups were quantitatively force-fed. Feed intake in the first 2 days was the same 330 g/bird on day 91 and 390 g/bird on day 92, respectively, and then the amount of feed intake provided to the ducks in each treatment remained unchanged during the other 10 days and was 450, 540, 630, 720, 810, 900 and 990 g/day per bird for each treatment group, respectively. Force-feeding was performed three times a day at 0600, 1300 and 2000 h, supplying one third of the daily among of feed every time. The temperature of force-feeding room was 20~24 C and humidity 65~70%. Measurements At the end of the 12-day force-feeding period, BW gain and feed conversion ratio (FCR) of ducks from each pen were calculated. After being deprived of feed for 12 h, all ducks from each pen were euthanized by CO 2 inhalation and bled. Birds were then immersed into hot water at 60 C for 2 min, scalded, picked, and eviscerated manually. Skin with subcutaneous fat, abdominal fat, breast meat (including pectoralis major and pectoralis minor), leg meat (including thigh and drum stick) and liver were removed from carcasses manually and weighed. Breast meat and leg meat were all skinless and boneless. All weights, including skin with subcutaneous fat, abdominal fat, breast meat, leg meat and liver were expressed as a percentage relative to eviscerated carcass weight at processing. Statistical analysis Data were analyzed as a completely randomized design by one-way ANOVA procedure of SAS software (SAS Institute, 2003). When dietary treatment was significant (P < 0.05), means were compared using Duncan s multiple comparison procedure of SAS software (SAS Institute, 2003). In the study, broken-line regression model analysis (Robbins et al., 2006) was used to estimate the optimum feed consumption level of Mule ducks based on BW gain and total liver yield data using the NLIN procedure of Body weight gain (g/d) Y= (884-X) R 2 =0.992 P< Y=98.91 when X > 884 Xoptimum= Feed consumption level (g/d) Figure 1 Relationship between BW gain and feed consumption levels using a broken-line regression model analysis. The break point is labeled with an arrow. It indicates the optimum feed consumption level. SAS software (SAS Institute, 2003). The model was as following: y = l + uðr xþ where y is the BW gain and total or relative liver weight, x the feed consumption levels, r the abscissa of the breakpoint and r is taken as the estimated optimal feed consumption level, l growth index response to optimal feed consumption level and u the slope of model. In this model, y = l when x > r. Results and discussion The main purpose of overfeeding of ducks and geese is to increase fat deposition to produce foie gras. The effect of overfeeding on production performance has been well discussedinwaterfowl(fournieret al., 1997; Davail et al., 2000; Su et al., 2009). In the present study, initial live BWs for different treatments were similar (P > 0.05) and varied from 4031 ± 49.4 to 4071 ± 86.8 g. At the end of the study, some ducks at 990 g/day group showed leg paralysis and crippled. When these ducks were slaughtered, a lot of undigested feed was observed in the enlargement of the ducks esophagus. It indicated force-feeding 990 g/day feed had over-achieved 1419

4 Wen, Jiang, Tang, Xie, Yang and Hou Table 3 Effects of feed consumption levels at 102 days of age on total liver weight and carcass composition of male Mule ducks 1 Skin with subcutaneous fat Abdominal fat Breast meat Leg meat Liver Feed consumption levels (g/day per bird) g % BW g % BW g % BW g % BW g % BW c 2.81 c bc 3.20 bc bc 3.17 bc b 3.82 b a 4.97 a a 5.05 a a 4.88 a SEM P-value < < Data were based on all ducks (n = 8 birds/treatment). 2 SEM: pooled standard error of the mean. a,b,c Mean values in the same column with no common superscript differ significantly (P < 0.05). Total liver weight (g) Y= (920-X) R 2 =0.928 P= Y=205.3 when X > 920 Xoptimum= Feed consumption level (g/d) Figure 2 Relationship between total liver weight and feed consumption levels using a broken-line regression model analysis. The break point is labeled with an arrow. It indicates the optimum feed consumption level. Liver relative weight (%) Y= (880-X) R 2 =0.916 P= Y=4.97 when X > Xoptimu= Feed consumption level (g/d) Figure 3 Relationship between liver relative weight and feed consumption levels using a broken-line regression model analysis. The break point is labeled with an arrow. It indicates the optimum feed consumption level. maximum digestion capacity of male Mule ducks. As showed in Table 2, feed consumption levels affected the final BW and BW gain significantly (P < 0.05) but not FCR. The results showed that force-feeding higher amounts of feed resulted in an improvement in BWs, which was in agreement with other reports (Zanusso et al., 2003; Chartrin et al., 2005). However, there was no further increase in BW gain when feed intake exceeded 900 g/day (Table 2), which suggested that BW gain of Mule ducks had reached its maximum. We applied the regression model analysis that has been widely used for determining quantitative nutrient requirements in animal nutrition (Luo et al., 2006; Yuan et al., 2010; Zhu et al., 2012) to estimate the optimum feed consumption level for Mule ducks. In this trial, based on the broken-line regression model analysis with the BW gain data, the optimum feed consumption level for Mule ducks was 884 g/day (Figure 1). The values are very different from previous data in Pekin ducks by Wen et al. (2015), who reported that the optimum feed consumption level for Pekin ducks during the force-feeding period was 414 g/day. Feed consumption levels for Mule ducks was calculated based on BW 0.75, and feed and energy intake for maximum BW gain were 217 g feed/kg BW 0.75 per day and 2.93 MJ ME/kg BW 0.75 per day, respectively (see the last table). Previous studies have shown that optimum consumption levels for feed and energy intake in Pekin ducks were 163g feed/kg BW 0.75 per day and 2.18 MJ ME/kg BW 0.75 per day, respectively (Wen et al., 2015). This discrepancy may be attributed to differences in feed composition, feed energy levels, and maximum growth capacity of ducks between the two experiments. Liver is the most important part in foie gras production of Mule ducks and higher yield of foie gras means higher economic value for duck producers. In this trial, total liver weight increased significantly with increasing feed consumption level up to 810 g/day (P < 0.05) and showed no significant differences above that level (P > 0.05) (Table 3). Feed consumption levels had significant effect on liver relative weight (P < 0.05), and it achieved maximum value at a feed intake of 900 g/day (Table 3). As previously reported in the three genotypes of ducks (Davail et al., 2003), overfeeding induced a significant increase in liver weight. In waterfowl, an intense lipogenesis from dietary carbohydrates 1420

5 The optimal feed consumption level of Mule ducks Table 4 Feed consumption levels for metabolic BW (BW 0.75, kg) Item Response criterion Broken-line model R 2 Requirement 1 Feed consumption 2 (g/kg BW 0.75 per day) Weight gain y = (217 x) ± 5.4 Total liver weight y = (227 x) ± 19.2 Liver relative weight y = (216 x) ± It was expressed as requirement ± SE. 2 Feed consumption was calculated for BW in the liver results in foie gras (Saadoun and Leclercq, 1987). The main reason may be that the de novo synthesized triglyceride are stored into the hepatocytes when the intensity of lipogenesis is higher than the hepatic capacity for very-lowdensity lipoprotein (VLDL) synthesis and secretion (Hermier et al., 1991; Fournier et al., 1997). In foie gras production of Mule ducks, in order to increase liver weight quickly, excess feed was force-fed into the esophagus. However, our study suggested foie gras weight of Mule ducks had no further increase at 900 g/day, and it reached a maximum energy deposition over 900 g/day (Table 3). The reason may be that the 990 g/day of feed consumption had exceeded ducks ingestion potential, caused gradually morphological adaptation of the digestive tract, and had a negative effect on ducks physiological response and growth (Zhou et al., 1990). In addition, when nutrient digestibility of ducks reduced, increased microbial growth resulted in more competition for nutrients with the host. In this way, it might lead to intestinal disorders. According to broken-line regression, the optimum feed consumption levels were 920 g/day for total liver weight (Figure 2) and 880 g/day for liver relative weight (Figure 3), respectively. Based on BW 0.75, broken-line regression analysis of liver relative weight data indicated that optimum consumption levels for feed and energy intake were 216 g feed/kg BW 0.75 per day and 2.92 MJ ME/kg BW 0.75 per day, respectively (Table 4). When feed consumption levels were calculated based on total liver weight, optimum consumption levels for feed and energy intake were 227 g feed/kg BW 0.75 per day and 3.08 MJ ME/kg BW 0.75 per day, respectively (Table 4). In our study, optimum feed consumption levels for total liver weight were higher compared to that for weight gain and liver relative weight. No significant differences in breast and leg meat yield were observed between treatments (P > 0.05), and the yield of skin with subcutaneous fat and abdominal fat increased gradually with increasing feed consumption level (Table 3). Overfeeding of waterfowls can induce a strong fattening of peripheral adipose tissues such as subcutaneous and abdominal adipose tissues (Janan et al., 2000). These could derive from lipids synthesized in the liver and carried by VLDL (Davail et al., 2003). Increasing subcutaneous and abdominal fat yield may also be a reason for increasing BW gain. In conclusion, feed consumption levels had significant effects on growth performance and carcass composition during the force-feeding period in foie gras production of Mule ducks. The optimum feed consumption levels of male Mule ducks from 91 to 102 days of age for maximum BW gain, total liver weight, and liver relative weight were 217, 227 and 216 g feed/kg BW 0.75 per day, respectively. The present study has potential commercial application for foie gras production of male Mule ducks. Acknowledgments This work was supported by the Earmarked fund for the Modern Waterfowl Industry Technology System of China (CARS-43) and the Agricultural Science and Technology Innovation Program (ASTIP-ISS09). 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