Amino acid digestibility in housefly and black soldier fly prepupae by growing pigs

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Amino acid digestibility in housefly and black soldier fly prepupae by growing pigs X. Tana,c, H.S. Yanga,b,c,*, M. Wanga,c, Z.F. Yia,c, F.J. Jia,c, J.Z. Lia,c, Y.L. Yina,b,c a Hunan International Joint Laboratory of Animal Intestinal Ecology and Health, Animal Nutrition and Human Health Laboratory, School of Life Sciences, Hunan Normal University, Changsha City, Hunan, 410081, China b Chinese Academy of Science, Institute of Subtropical Agriculture, Research Center for Healthy Breeding of Livestock and Poultry, Hunan Engineering and Research Center of Animal and Poultry Science and Key Laboratory for Agroecological Processes in Subtropical Region, Scientific Observation and Experimental Station of Animal Nutrition and Feed Science in South-Central, Ministry of Agriculture, Changsha City, Hunan, 410125, China c State Key Laboratory of Developmental Biology of Freshwater Fish, College of Life Science, Hunan Normal University, Changsha 410081, People’s Republic of China

A R T IC LE I N F O

ABS TRA CT

Keywords: Amino acid Ileal standardized digestibility Housefly Black soldier fly Swine

An experiment was conducted with the objectives of determining the coefficient of ileal apparent digestibility (CIAD) and the coefficient of ileal standardized digestibility (CISD) of amino acids (AA) in housefly (HF) and black soldier fly (BSF) prepupae meal by growing pigs. Ten pigs fitted with a T-cannula in the distal ileum with an average initial body weight of 25.05 kg were housed individually in metabolism cages equipped with a feeder and a nipple drinker. The pigs were randomly assigned each to one of two diets formulated to contain 976.7 g/kg of HF or BSF as the sole source of nitrogen. A nitrogen-free (N-free) diet was also formulated to estimate the basal ileal endogenous loss (BEL) of AA. All experimental diets contained 2 g/kg titanium dioxide as an indigestible marker. The daily feed allowance was offered in three equal meals that were fed at 0830, 1400 and 1930 h. Each experimental period lasted for 7 days, the initial 4 d for diet acclimation, followed by 3 d for ileal digesta collection and the digesta samples were collected continuously for 12 h. The CIAD of all AA for HF and BSF are more than 0.726 and 0.641, respectively. The values for the CISD of all AA range from 0.870 to 1.608 and from 0.767 to 1.177 for HF and BSF, respectively. Moreover, the values for the CIAD of all AA in HF are greater (P < 0.05) than in BSF. The dispensable AA account for the most proportion of the endogenous fraction and the BEL of proline is the greatest. The values for the CISD of all AA except methionine and cysteine in HF are also greater (P < 0.05) than in BSF. It is concluded that the digestibility of all AA in HF is greater than in BSF in pig.

1. Introduction The adequate amino acids (AA) content in diet is one of the most significant factors in formulating swine diets. Therefore,

Abbreviations: AA, amino acids; BEL, basal ileal endogenous loss; BSF, black soldier fly; N-free, nitrogen-free; BW, body weight; CIAD, coefficient of ileal apparent digestibility; CISD, coefficient of ileal standardized digestibility; CP, crude protein; DM, dry matter; EE, ether extract; GE, gross energy; HF, housefly; N, nitrogen; SID, standardized ileal digestibility; Ti, Titanium ⁎ Corresponding author at: Hunan International Joint Laboratory of Animal Intestinal Ecology and Health, Animal Nutrition and Human Health Laboratory, School of Life Sciences, Hunan Normal University, Changsha City, Hunan, 410081, China. E-mail address: [email protected] (H.S. Yang). https://doi.org/10.1016/j.anifeedsci.2020.114446 Received 14 December 2017; Received in revised form 3 February 2020; Accepted 10 February 2020 0377-8401/ © 2020 Elsevier B.V. All rights reserved.

Please cite this article as: X. Tan, et al., Animal Feed Science and Technology, https://doi.org/10.1016/j.anifeedsci.2020.114446

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determining the digestibility of AA is important for accurate formulation to meet AA requirement of pigs. Generally, the AA digestibility is measured by the ileal digestibility assay (Gabert et al., 2001) and the standardized ileal digestibility (SID) assay is the most frequently used way to determine AA availability in feeding stuff in swine diets (Stein et al., 2007). In addition, researchers have reported that formulating swine diets using digestible AA is more efficient rather than total AA (Lee et al., 2017). Index method is used to measure the AA digestibility because it is very difficult to collect all of ileal digesta (Adeola, 2001). Housefly (HF; Musaca domestica) can effectively be used as an alternative protein source for livestock such as poultry and fish (Zuidhof et al., 2003; Ogunji et al., 2007). Inaoka et al. (1999) reported that AA composition of HF was similar to fish meal and HF can partially replace the fish meal in broiler chicken feed. Hwangbo et al. (2009) also showed that HF maggots can effectively be used as feeding diets for broiler chickens. The larvae of black soldier fly (BSF; Hermetia illucens) can grow on very dense populations on organic wastes and transform organic wastes into valuable biomass (van Huis, 2013; Nguyen et al., 2015). There are some studies showed that BSF can be used as an alternative protein source for broiler quails, broilers, and European sea bass (De Marco et al., 2015; Cullere et al., 2016; Mwaniki et al., 2018; Mwaniki and Kiarie, 2019). The HF and BSF meal may also be a good feed resource for swine. It is important to determine the AA digestibility of protein source for using in feed formulation. To our knowledge, there is only one non-peer review report about AA digestibility of BSF for pigs (Kortelainen et al., 2014), and studies on the AA digestibility of HF for pigs have not been reported. Therefore, the purpose of the current study was to determine digestibility coefficients of AA in HF and BSF fed to growing pigs. 2. Materials and methods 2.1. Animals and housing Ten Duroc × Landrace × Yorkshire pigs (average initial body weight of 25.05 ± 0.93 kg) were used in this study to determine the coefficient of ileal apparent digestibility (CIAD) and coefficient of ileal standardized digestibility (CISD) of AA in HF and BSF. The pigs were surgically equipped with a simple T-cannulas in the distal ileum using procedures as described by Nyachoti et al. (2002). Following the surgery, pigs were housed individually in metabolism cages during the experiment period. Each cage was equipped with a feeder and a nipple drinker which allowed the pigs to have unrestricted access to water all the time. The experimental design and procedures in this study were reviewed and approved by the Animal Care and Use Committee of Hunan Normal University, Changsha City, Hunan, China. 2.2. Diets and feeding Three experimental diets were prepared. A nitrogen-free (N-free) diet was formulated to contain sucrose and cornstarch mainly to estimate the basal ileal endogenous losses (BEL) of AA (Table 1). Two diets were formulated to contain either HF or BSF meal at concentration of 976.7 g/kg as the sole source of nitrogen (Table 1). The HF and BSF that were used in the current study were grown Table 1 Ingredient and analyzed nutrient composition of experimental diets (as-fed basis). Item

Ingredient (g/kg) HFa BSFb Corn starch Sucrose Vitamin-mineral premixc Salt Choline chloride Dicalcium phosphate Limestone Titanium dioxide Analyzed compositiond GE (MJ/kg) DM (g/kg) CP (g/kg) EE (g/kg)

Diet HFa

BSFb

Nitrogen-free

976.7 – – – 1.8 3 0.5 8 10 2

– 976.7 – – 1.8 3 0.5 8 10 2

– – 876.7 100 1.8 3 0.5 8 10 2

24.7 897.2 529.9 227.7

27.7 938.9 431.6 354.8

16.8 895.4 6.0 21.9

a

HF = housefly. BSF = black soldier fly. c Provided the following quantities per kg of complete diet: 10,000 IU of Vitamin A, 1000 IU of Vitamin D3, 80 IU of Vitamin E, 2.0 mg of Vitamin K3, 0.03 mg of Vitamin B12, 12 mg of riboflavin, 40 mg of niacin, 25 mg d-pantothenic acid, 0.25 mg of biotin, 1.6 mg of folic acid, 3.0 mg of thiamine, 2.25 mg of pyridoxine,10 mg of Cu (CuSO4), 120 mg of Zn (ZnSO4), 45 mg of Mn (MnSO4), 150 mg of Fe (FeSO4), 0.18 mg of Se (Na2SeO3),1.0 mg of I (Ca(IO3)2). d GE = gross energy; DM = dry matter; CP = crude protein; EE = ether extract. b

2

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on chicken manure and provided by Hunan Shanhemei Bio Environmental Protection Co., Ltd (Changsha, China). Titanium dioxide (2 g/kg) was included in all experimental diets as an indigestible marker. Vitamins and minerals were adequate to meet the NRC (2012) recommendations. Feed was provided in a daily amount equal to 3 times the energy requirement for maintenance (i.e., 197 kcal metabolizable energy per kg BW0.60; NRC, 2012). The daily feed allowance was offered in three equal meals that were fed at 0830, 1400 and 1930 h. Representative samples of each diet were kept at 4 ℃ until required for analysis. 2.3. Experimental design and sample collection The trial consisted of two periods, each of which lasted for 7 days. A total of 10 pigs were randomly divided into two groups. In the first period, both of the two groups were fed a N-free diet. In the second period, one group was fed a HF meal, and the other group was fed a BSF meal. The experimental period lasted for 7 days consisting of a 4-d period for diet acclimation while the remaining 3-d was used for digesta collections. The ileal digesta samples were collected continuously for 12 h from each pig from 0830 to 2030 h on each day of sampling (d 5, 6, and 7). A plastic bag with a tie was attached to the T-cannula and digesta flowing into the bag were collected. Bags were removed at least every 30 min or if they were filled with ileal digesta. Collected ileal digesta samples were stored frozen at −20 ℃ immediately for later analysis and prevent bacterial degradation of the digesta proteins. 2.4. Sample preparation and chemical analyses At the end of the experiment, digesta samples were thawed, pooled for each pig and each day, homogenized, sub-sampled and lyophilized. Samples of experimental diets and freeze-dried ileal digesta were finely ground prior to chemical analyses. Amino acids were liberated from the protein by hydrolysis with 6 M HCl for 24 h at 110 ℃ and analyzed using an AA analyzer (Hitachi L-8900, Tokyo, Japan). Methionine and cysteine were analysed in samples that had been oxidized with performic acid before hydrolysis (Procedure 994.12; Association of Analytical Chemists, 2000). Tryptophan was not analyzed. Dry matter (DM) by oven-drying at 105 ℃ for 9 h (Ahn et al., 2014). Ether extract (EE) was determined using petroleum ether as the solvent in an automatic soxhlet extractor (SOX 416, Gerhardt, Germany). Gross energy (GE) can be measured using benzoic acid as the calibration standard in an isothermal auto-calorimeter (5E-AC8018, Changsha, China). Crude protein (CP) was measured with AA3 flow injection analyzer (Seal, Shanghai, China). Titanium (Ti) concentrations of feed and ileal digesta samples were measured by using UV/vis spectrophotometer (Lambda 25, PerkinElmer, Shanghai, China). Phosphorus was also determined by using UV/vis spectrophotometer (Lambda 25, PerkinElmer, Shanghai, China). Calcium was measured by using flame atomic absorption spectrometer (novAA350, Jena, Germany). 2.5. Calculations and statistical analysis The digestibility of AA was calculated based on AA and Ti concentrations of diets and ileal digesta. The CIAD of AA were calculated according to the following equation (Baker et al., 2010):

CIADAA =1-(

AAileal Ti )×( diet ) AA diet Tiileal

where CIADAA is the CIAD of AA, AAileal and AA diet is the concentration of AA in the ileal digesta and diet, respectively. Ti diet and Tiileal is the concentration of Ti in the diet and ileal digesta, respectively. The BEL at the distal ileum of AA were calculated from the pigs fed nitrogen-free diet using the following equation (Baker et al., 2010):

IAA end = AAileal ×(

Ti diet ) Tiileal

where IAA end (g/kg of dry matter intake) is the BEL of AA. The values for the CISD of AA were calculated by correcting the BEL of AA. The CISD for AA were calculated using the following equation (Baker et al., 2010):

CISDAA =CIAD+(

IAA end ) AA diet

where the CISDAA is the CISD of AA. The data were subjected to a t-test using SAS software version 9.2 (SAS Inst. Inc., Cary, NC, USA). Data are presented as as means and SEM. The experimental unit was a pig, and probability values < 0.05 were taken to indicate statistical significance. 3. Results and discussion The contents of DM, CP, EE and GE in HF and BSF diets are presented in Table 1. The HF has greater contents of CP than BSF, while BSF has greater contents of GE and EE than HF. The contents of AA in HF and BSF are presented in Table 2. The lysine, methionine and threonine in HF meal are 38.3, 14.4 and 23.2 g/kg, respectively. The contents of lysine, methionine and threonine in BSF are 25.4, 7.0 and 16.0 g/kg, respectively. The methione and cysteine are the least abundant AA in both HF and BSF. The most abundant indispensable AA in HF are lysine, phenylalanie and leucine. In BSF, leucine, lysine and valine are the most abundant 3

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Table 2 Analyzed amino acid composition of housefly (HF) and black soldier fly (BSF) (g/kg, asfed basis). Item

Ingredient

Indispensable amino acids Arginine Histidine Isoleucine Leucine Lysine Methionine Phenylalanine Threonine Valine Dispensable amino acids Alanine Aspatic acid Cysteine Glutamic acid Glycine Proline Serine Tyrosine

HF

BSF

27.2 16.1 26.2 35.3 38.3 14.4 36.0 23.2 27.1

19.5 12.6 21.4 28.8 25.4 7.0 18.7 16.0 24.6

28.3 54.9 3.9 76.6 22.8 22.6 21.5 34.0

27.6 40.7 2.7 50.0 25.2 24.0 15.7 23.7

indispensable AA. The contents of all AA except glycine and proline in HF are higher than in BSF. However, the AA contents in HF are lower than the values for fish meal published in NRC (2012) except histidine, isoleucine, phenylalanie and tyrosine. In contrast, the AA contents in HF investigated here are greater than the values for soybean meal reported by Kim et al. (2009) except arginine, leucine, cysteine, glutamic acid and serine. Animals stayed healthy, readily ate their diets and grew normally during the experimental period. Data on AA digestibility in HF and BSF fed to pigs are scarce thus making it difficult to make comparisons with the present data. The CIAD of AA are presented in Table 3. The CIAD of indispensable AA for HF and BSF are more than 0.844 and 0.735, respectively. The CIAD of dispensable AA for HF and BSF are more than 0.726 and 0.641, respectively. The HF has greater (P < 0.05) CIAD of all AA estimated in this study than in BSF. Compared to plant based protein sources, the values for the CIAD of all indispensable AA in HF except arginine, histidine and isoleucine are greater than the values of soybean meal (Petersen et al., 2005). In addition, of the dispensable AA, the CIAD except cysteine and glutamic acid for HF are also greater than for soybean meal (Petersen et al., 2005). The CIAD of all AA in HF are higher than the values of fish meal (NRC, 2012). The CIAD of all AA except alanine and Table 3 Coefficients of ileal apparent digestibility (CIAD) of amino acids in housefly (HF) and black soldier fly (BSF) fed to growing pigsa. Item

Indispensable amino acids Arginine Histidine Isoleucine Leucine Lysine Methionine Phenylalanine Threonine Valine Dispensable amino acids Alanine Aspatic acid Cysteine Glutamic acid Glycine Proline Serine Tyrosine a b

Diet

SEMb

P-value

HF

BSF

0.926 0.876 0.844 0.884 0.904 0.915 0.894 0.873 0.873

0.821 0.755 0.735 0.774 0.757 0.812 0.745 0.739 0.773

0.005 0.011 0.013 0.009 0.008 0.014 0.009 0.011 0.010

< 0.001 < 0.001 < 0.001 < 0.001 < 0.001 0.001 < 0.001 < 0.001 < 0.001

0.874 0.885 0.726 0.874 0.807 0.837 0.881 0.920

0.793 0.749 0.641 0.780 0.733 0.745 0.776 0.814

0.009 0.010 0.025 0.011 0.019 0.024 0.009 0.006

< 0.001 < 0.001 0.042 < 0.001 0.023 0.029 < 0.001 < 0.001

Each least squares mean represents 5 observations. SEM = standard error of the means. 4

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Table 4 Basal endogenous losses (g/kg of dry matter) of CP and amino acids at the terminal ileuma. Item

Mean

S.D.b

CP Indispensable amino acids Arginine Histidine Isoleucine Leucine Lysine Methionine Phenylalanine Threonine Valine Mean, indispensable AA Dispensable amino acids Alanine Aspatic acid Cysteine Glutamic acid Glycine Proline Serine Tyrosine Mean, dispensable AA Mean, total AA

22.46

8.69

1.005 0.288 0.838 1.087 0.494 0.825 0.423 0.980 0.923 0.763

0.420 0.057 0.142 0.179 0.090 0.189 0.084 0.162 0.166 0.165

1.452 1.430 0.497 1.563 2.825 13.374 0.981 0.214 2.792 1.777

0.424 0.229 0.102 0.266 0.862 6.100 0.190 0.053 1.028 0.597

a b

Each least squares mean represents 10 observations. Standard deviation.

glycine in BSF are lower than the values of soybean meal (Kim et al., 2009). The CIAD of all AA in except cystine and glutamic acid are higher in mechanically extracted BSF meal than full fat BSF meal that used in the present study (Kortelainen et al., 2014). However, the CIAD of all AA except isoleucine and phenylalanine in the present study are greater than hexane extracted BSF meal (Kortelainen et al., 2014). These results suggest that the CIAD of BSF meal are affected by processing methods. The value of BEL (g/kg DM intake) of CP and AA determined from pigs fed the nitrogen-free diet are presented in Table 4. In agreement with previous studies, the dispensable AA account for the most proportion of the endogenous fraction measured at the terminal ileum of growing pigs (Furuya and Kaji, 1992; Dilger et al., 2004; Kiarie and Nyachoti, 2007). These AA are likely to be intact proteins rather than free AA because it has been reported that, under protein-free nutrition in growing pigs, protein constitutes the majority of endogenous nitrogen-containing material at the terminal ileum (Moughan and Schuttert, 1991). Proline is the most prominent AA of all measured in ileal digesta from pigs fed the nitrogen-free diet and the BEL of proline is the greatest in our experiment, which is consistent with previous studies (Stein et al., 1999; Dilger et al., 2004; Woyengo et al., 2010; Son et al., 2014). This phenomenon is due to the state of the protein depletion in the pig. The explanation may be that proline is rich in mucin, but mucin has a high degree of resistance to proteolysis so that the mucin can reach the end of the ileum without being hydrolyzed and reabsorbed (Stein et al., 1999). The branched-chain AA (isoleucine, leucine, and valine), as well as threonine and arginine are the indispensable AA present at relatively higher concentrations than other indispensable AA. This observation is in agreement with previous work (Kiarie and Nyachoti, 2007). The CISD of AA for HF and BSF are given in Table 5. The values for the CISD of all AA range from 0.870 to 1.608 and from 0.767 to 1.177 for HF and BSF, respectively. The values for the CISD of all AA except methionine and cysteine in HF are greater (P < 0.05) than in BSF. Of the indispensable AA, the values of CISD (except histidine and isoleucine) in soybean meal are lower than in HF (Petersen et al., 2005). For dispensable AA, the CISD of them that are measured for HF are higher than the values of soybean meal (Petersen et al., 2005; Kim et al., 2009). The CISD of all AA except methionine, alanine, cysteine, glycine and proline in BSF are relatively lower than the values that are previously reported for soybean meal (Kim et al., 2009). The CISD of all AA in HF are higher than the values for fish meal (NRC, 2012). The CISD of all AA except methionine, cystine, glutamic acid, glycine and proline are higher in mechanically extracted BSF meal than full fat BSF meal used in the present study (Kortelainen et al., 2014). However, the CISD of all AA except phenylalanine are higher than hexane extracted BSF meal (Kortelainen et al., 2014). Further studies are needed to test the effects of HF and BSF on growth performance of pigs. There are some studies have been reported that HF and BSF can be effectively used as feeding diets for broiler chicken (Inaoka et al., 1999; Hwangbo et al., 2009; Cullere et al., 2016). The current experiment also indicates that soybean meal or fish meal may be potentially substituted by HF and BSF as alternative protein sources for pigs. In the previous discussion, we have already compared the AA contents or AA digestibility of HF and BSF with soybean meal and fish meal (Petersen et al., 2005；Kim et al., 2009; NRC, 2012). It is obvious that the composition and digestibility of AA in HF and BSF meal are similar to soybean meal or fish meal. The digestibility of AA in HF is even better than that of soybean meal or fish meal. This means that HF and BSF may be used as alternative protein sources to replace the soybean meal or fish meal in pig feed in the future. Besides, we find that the digestibility of HF meal is higher than BSF meal. The reasons may be that the two insect diets differ in crude fat and CP or AA concentration. Previous study 5

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Table 5 Coeffieients of ileal standardized digestibility (CISD) of of amino acids in housefly(HF) and black soldier fly(BSF) fed to growing pigsa. Item

Indispensable amino acids Arginine Histidine Isoleucine Leucine Lysine Methionine Phenylalanine Threonine Valine Dispensable amino acids Alanine Aspatic acid Cysteine Glutamic acid Glycine Proline Serine Tyrosine a b

Diet

SEMb

P-value

HF

BSF

0.973 0.896 0.878 0.918 0.918 0.988 0.906 0.919 0.910

0.862 0.778 0.775 0.810 0.776 0.918 0.767 0.798 0.809

0.007 0.011 0.014 0.010 0.008 0.020 0.010 0.014 0.011

< 0.001 < 0.001 0.001 0.001 < 0.001 0.054 < 0.001 < 0.001 < 0.001

0.936 0.914 0.870 0.896 0.956 1.608 0.932 0.926

0.839 0.783 0.803 0.810 0.830 1.177 0.835 0.824

0.011 0.012 0.031 0.012 0.021 0.106 0.011 0.006

< 0.001 < 0.001 0.173 0.001 0.003 0.034 < 0.001 < 0.001

Each least squares mean represents 5 observations. SEM = standard error of the means.

reported that the ileal digestibility of most of the AA increased linearly with increasing dietary fat levels (Li and Sauer, 1994). Another research also showed that there was an increase in ileal AA digestibility as the dietary CP or AA content increased (Fan et al., 1994; Htoo et al., 2007). In the present study, although the BSF has greater content of crude fat than HF, the contents of CP and most of the AA in HF are greater than BSF. The effect of CP or AA contents on digestibility may be greater than crude fat content. Therefore, the higher ileal AA digestibility of HF may be because of higher CP and AA contents. Moreover, different concentration of chitin in insect meal may also have influence on AA digestibility in larvae meals (Marono et al., 2015). This study did not analyze the chitin contents in the insect meals and further works are needed to study the effect of chitin on BSF and HF digestibility in pigs. 4. Conclusion In conclusion, the present study provides AA digestibility values for HF and BSF. The digestibility of all AA in HF is greater than in BSF. The values for the digestibility of AA in HF and BSF will be valuable in its routine incorporation in swine diets Declaration of Competing Interest The authors declare no conflict of interest. Acknowledgments This study was supported in part by Hunan Province’s Changsha-Zhuzhou-Xiangtan National Independent Innovation Demonstration Zone projects (2017XK2058), Hunan Province’s Strategic and Emerging Industrial Projects (2018GK4035), Natural Science Foundation of Hunan Province (2017JJ1020). References Adeola, O., 2001. Digestion and balance techniques in pigs. In: Lewis, A.J., Southern, L.L. (Eds.), Swine Nutrition. CRC Press, Washington, DC, USA, pp. 903–916. Ahn, J.Y., Kil, D.Y., Kong, C., Kim, B.G., 2014. Comparison of oven-drying methods for determination of moisture content in feed ingredients. Asian-australas. J. Anim. Sci. 27, 1615–1622. Association of Analytical Chemists, 2000. Official Methods of Analysis, 17th ed. AOAC, Arlington, VA, USA. Baker, K.M., Kim, B.G., Stein, H.H., 2010. Amino acid digestibility in conventional, high-protein, or low-oligosaccharide varieties of full-fat soybeans and in soybean meal by weanling pigs. Anim. Feed Sci. Technol. 162, 66–73. Cullere, M., Tasoniero, G., Giaccone, V., Miotti-Scapin, R., Claeys, E., De Smet, S., Dalle Zotte, A., 2016. Black soldier fly as dietary protein source for broiler quails: apparent digestibility, excreta microbial load, feed choice, performance, carcass and meat traits. Animal 10, 1923–1930. De Marco, M., Martinez, S., Hernandez, F., Madrid, J., Gai, F., Rotolo, L., Belforti, M., Bergero, D., Katz, H., Dabbou, S., Kovitvadhi, A., Zoccarato, I., Gasco, L., Schiavone, A., 2015. Nutritional value of two insect larval meals (Tenebrio molitor and Hermetia illucens) for broiler chickens: apparent nutrient digestibility, apparent ileal amino acid digestibility and apparent metabolizable energy. Anim. Feed Sci. Technol. 209, 211–218. Dilger, R.N., Sands, J.S., Ragland, D., Adeola, O., 2004. Digestibility of nitrogen and amino acids in soybean meal with added soyhulls. J. Anim. Sci. 82, 715–724. Fan, M.Z., Sauer, W.C., Hardin, R.T., Lien, K.A., 1994. Determination of apparent ileal amino acid digestibility in pigs: effect of dietary amino acid level. J. Anim. Sci. 72, 2851–2859.

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