The age-related metabolizable energy of cereal grains, oilseed meals, corn gluten meals, and feather meals for broilers

Abstract

A 2 × 3 factorial arrangement of treatments with two ages of broilers (11 to 14 or 25 to 28 d of age) and three samples of feed ingredients was utilized to compare metabolizable energy (ME) and ratio of ME to gross energy (GE) in each group of three cereal grains (CG, including one corn, two wheat flour), three oilseed meals (OM, including one soybean meal, one peanut meal, and one cottonseed meal), three corn gluten meals (CGM A, B, and C), and three feather meals (FM A, B, and C). Each treatment contained six replicates of four Arbor Acre male broilers in energy balance experiments. Trends toward interactions between age and source of CG were observed on the ME and ME/GE of CG (0.05 <P < 0.10). The ME and ME/GE in corn were greater for broilers from 25 to 28 than for 11 to 14 d of age (P < 0.05). However, the ME and ME/GE in wheat flour A and B were not affected by the age of the broilers. The ME and ME/GE of OM were not affected by the age of broilers but differed across sources (P < 0.01). Conversely, the ME and ME/GE of FM were not different across sources of FM, but the ME and ME/GE of FM were less for broilers from 11 to 14 compared to 25 to 28 d of age (P < 0.01). Significant interactions between age and sources of CGM affected the ME and ME/GE of CGM (P < 0.05). The ME and ME/GE of CGM A were greater than CGM B (P < 0.05) when fed to broilers from 25 to 28 d of age but there was no effect from 11 to 14 d of age. The ME and ME/GE of CGM were less in broilers from 11 to 14 compared to 25 to 28 d of age (P < 0.05). These results indicate that the energy value of wheat flour and OM are similar regardless of age, but the ME in starter diets with corn, CGM, and FM may be overestimated if the ME values are obtained from growing broilers.

The metabolizable energy of corn, corn gluten meals, and feather meals may be overestimated for broilers at the starter phase if their metabolizable energy values are obtained from growing broilers.

Introduction

An accurate assessment of the metabolizable energy (ME) for feed ingredients is essential to estimate effective energy for poultry growth. Nutritionists need to understand the effect of age on the ME value of ingredients for broilers (Yang et al., 2020; Khalil et al., 2021), but there is a dearth of information on ME values of feed ingredients for broilers across phases in the databases of NRC (1994), INRA (INRA-AFZ-INAPG, 2004) and CVB (2021). The digestive tract of starter broilers is less mature compared to grower broilers, and the secretion of digestive juice and bile is insufficient to efficiently digest some ingredients (Noy and Sklan, 2002; Juanchich et al., 2021). These different conditions suggest that the ME of feed should be greater for grower vs. starter broilers. However, Khalil et al. (2021) reported that the ME of wheat (3,219 vs. 3,195 kcal/kg for nitrogen-corrected apparent metabolizable energy (AMEn)) and sorghum (3,614 vs. 3,633 kcal/kg for AMEn) were not affected by age (8 to 14 vs. 22 to 28 d of age), but the ME of barley (2,988 vs. 3,090 kcal/kg for AMEn) and corn (3,542 vs. 3,659 kcal/kg for AMEn) were affected by age. Several studies also described age-related effects on the ME for soybean meal (Bertechini et al., 2019), meat and bone meal (Adeola et al., 2018), and fish meal (Yaghobfar, 2003). These findings suggest there may be an interactive effect between the age of broilers and cereal grain or protein ingredients on ME values. In total, the difference in ME of cereal grains determined with broilers during the starter and grower phases is less than 3.3% of ME (Olukosi and Bedford, 2019; Khalil et al., 2021), which is numerically similar to the reproducible error of determination of ME (2.92% of ME, Bourdillon et al., 1990). However, in contrast to cereal grains, the ME of protein ingredients was affected by age with greater variability (Yaghobfar, 2003; Bertechini et al., 2019). There is a dearth of information on ME values of feed ingredients for broilers across phases, especially protein ingredients in China. Understanding the effect of age on the ME of different sources of protein ingredients is critical to provide accurate effective energy for broilers, especially at the starter phase because diets commonly contain >30% protein ingredients. The objective of the current study was to understand the effect of age and source on the ME of 12 feed ingredients (three cereal grains (CG), three oilseed meals (OM), three corn gluten meals (CGM), and three feather meals (FM)) for broilers during starter and grower phases.

Materials and Methods

All experimental procedures related to the use of live broilers were approved by the animal care and welfare committee of the Institute of Animal Sciences of Chinese Academy of Agricultural Sciences (Beijing, China). The code of ethical inspection was IAS 2021-104.

Feed ingredients and experimental diets

Three CG: one corn and two sources of wheat flours (WF); three OM: one soybean meal (SBM), one peanut meal (PNM), and one cottonseed meal (CSM); three sources of CGM with variable CP content, and three sources of FM: one enzymatically hydrolyzed FM, one expanded FM, and one hydrolyzed FM were sampled from Shandong New Hope Liuhe Group. (Qingdao, China). The nutrient compositions of all feed ingredients are shown in Table 1. A starter-grower diet was formulated to exceed the nutrient requirement recommended by China Agricultural Industry Standard (NY/T 33-2004) for broilers when not in the energy balance experiment (Table 2). Thirteen experimental diets included 1 corn-soybean meal basal diet and 12 test diets (Table 2). Each test diet consisted of a basal diet and test feed ingredient, with dietary CP less than 25.0% according to the technical regulation of feed evaluation recommended by Ministry of Agriculture and Rural Affairs of the People’s Republic of China (2020). The chemical compositions of all diets are presented in Table 2.

Table 1.

Nutrient content of feed ingredients (DM basis, %)

Feed ingredients	DM	CP	EE	Ash	CF	NDF	ADF	GE, kcal/kg
Corn	87.20	8.55	4.14	1.40	2.92	9.60	1.72	4,434
Wheat flour A	86.41	17.54	2.08	1.31	1.23	3.56	1.08	4,449
Wheat flour B	87.80	17.96	2.87	1.90	2.14	7.97	0.59	4,466
Soybean meal	88.05	53.48	0.90	6.91	4.35	8.82	5.06	4,663
Peanut meal	89.78	51.98	0.86	6.32	6.78	15.58	8.19	4,597
Cottonseed meal	89.90	56.73	1.66	8.21	9.51	18.17	11.76	4,676
Corn gluten meal A	91.56	61.25	0.98	2.81	2.05	8.39	0.79	5,352
Corn gluten meal B	93.25	63.06	1.07	2.26	2.23	10.17	2.81	5,442
Corn gluten meal C	91.39	67.06	0.94	2.45	1.32	7.30	0.78	5,463
Feather meal A	92.18	91.58	5.71	3.31	--	--	--	5,716
Feather meal B	88.71	90.21	5.47	2.17	--	--	--	5,788
Feather meal C	91.29	93.88	2.16	3.83	--	--	--	5,599

Abbreviations: Feather meal A, enzymatic hydrolysis feather meal; Feather meal B, hydrolyzed feather meal; Feather meal C, expanded feather meal

Table 2.

The composition of the experimental diets (air-dry basis, %)

Items	Starter-grower diet	Experimental diets
		1	2	3	4	5	6	7	8	9	10	11	12	13
Corn	53.40	69.78	41.87	41.87	41.87	55.83	55.83	55.83	59.31	59.31	59.31	62.80	62.80	62.80
Soybean meal	35.38	25.74	15.44	15.44	15.44	20.59	20.59	20.59	21.88	21.88	21.88	23.17	23.17	23.17
Test ingredient
Corn			40.00
Wheat flour A				40.00
Wheat flour B					40.00
Soybean meal						20.00
Peanut meal							20.00
Cottonseed meal								20.00
Corn gluten meal A									15.00
Corn gluten meal B										15.00
Corn gluten meal C											15.00
Feather meal A												10.00
Feather meal B													10.00
Feather meal C														10.00
Soybean oil	4.51
Corn gluten meal	2.00
Dicalcium phosphate	1.73	1.75	1.05	1.05	1.05	1.40	1.40	1.40	1.49	1.49	1.49	1.57	1.57	1.57
Limestone	1.07	1.14	0.68	0.68	0.68	0.91	0.91	0.91	0.97	0.97	0.97	1.03	1.03	1.03
Premix1	0.50	0.50	0.30	0.30	0.30	0.40	0.40	0.40	0.42	0.42	0.42	0.45	0.45	0.45
Sodium chloride	0.30	0.30	0.18	0.18	0.18	0.24	0.24	0.24	0.25	0.25	0.25	0.27	0.27	0.27
L-lysine	0.50	0.35	0.21	0.21	0.21	0.28	0.28	0.28	0.30	0.30	0.30	0.31	0.31	0.31
DL-methionine	0.23	0.21	0.13	0.13	0.13	0.17	0.17	0.17	0.18	0.18	0.18	0.19	0.19	0.19
L-threonine	0.19	0.15	0.09	0.09	0.09	0.12	0.12	0.12	0.13	0.13	0.13	0.14	0.14	0.14
L-valine	0.14	0.08	0.05	0.05	0.05	0.06	0.06	0.06	0.07	0.07	0.07	0.07	0.07	0.07
Broiler complex enzyme	0.03
Phytase	0.02
Total, %	100.00	100.00	100.00	100.00	100.00	100.00	100.00	100.00	100.00	100.00	100.00	100.00	100.00	100.00
Nutrient content, %2
DM	91.75	90.97	90.25	89.89	90.19	90.72	90.94	90.97	90.82	91.04	90.92	90.85	90.63	90.88
GE, kcal/kg	4,325	3,963	3,965	3,952	3,972	4,008	4,005	4,018	4,093	4,112	4,115	4,087	4,078	4,068
CP	22.54	17.85	13.77	17.01	17.46	24.05	23.97	24.94	23.86	24.18	24.82	24.79	24.45	25.04
EE	7.53	3.15	3.19	2.45	2.70	2.45	2.48	2.49	2.77	2.74	2.77	3.22	3.20	2.76

Abbreviations: 1, Basal diet; 2, Corn diet; 3, Wheat flour A diet; 4, Wheat flour B diet; 5, Soybean meal diet; 6, Peanut meal diet; 7, Cottonseed meal diet; 8, Corn gluten meal A diet; 9, Corn gluten meal B diet; 10, Corn gluten meal C diet; 11, Feather meal A diet; 12, Feather meal B diet; 13, Feather meal C diet; CP, crude protein; DM, dry matter; EE, ether extract; GE, gross energy.

¹Supplied per kilogram of diet: vitamin A, 8,000 IU; vitamin D₃, 1,000 IU; vitamin E, 20.0 IU; vitamin K₃, 0.80 mg; thiamine, 3.0 mg; riboflavin, 8.0 mg; vitamin B_6, 5.0 mg; vitamin B₁₂, 20.0 µg; pantothenic acid, 10.0 mg; nicotinic acid, 40.0 mg; folic acid, 0.60 mg; biotin, 0.20 mg; Cu (as copper sulfate), 8.0 mg; Fe (as ferrous sulfate), 100 mg; Mn (as manganese sulfate), 120 mg; Zn (as zinc sulfate), 100 mg; I (as calcium iodate), 0.70 mg; Se (as sodium selenite), 0.30 mg.

²The DM, GE, CP, and EE were determined values (air-dry basis).

Experimental design

In each of four groups of feed ingredients including three CG, three OM, three CGM, and three FM, a 2 × 3 factorial arrangement of treatments was utilized with two ages of broilers (days 11 to 14 or days 25 to 28) and three samples of feed ingredients. A total of 800 one-day-old Arbor Acre (AA) male broilers were obtained from a local hatchery and provided free access to a starter-grower diet and water in three-tier cages when not participating in an energy balance experiment. A group of 312 AA male broilers on day 8 (BW = 231 ± 1 g) and another group of 312 AA male broilers on day 22 (BW = 1,169 ± 6 g) were selected for the energy balance experiment and randomly divided into 13 dietary treatments with six replicates of four broilers in each experimental diet.

ME bioassay

The AME and AMEn of experimental diets were determined by the total collection of feces and urine according to the European reference method of in vivo ME bioassay (Bourdillon et al., 1990) and the technical regulation recommended by the Ministry of Agriculture and Rural Affairs of the People’s Republic of China (2020). The procedures were outlined as follows: 6 d for energy balance experiment, including an adaptation period of 55 hours from 09:00 on day 1 to 16:00 on day 3 (free access to the experimental diets), a fast of 17 hours from 16:00 on day 3 to 09:00 on day 4, 55 hours of free access to the experimental diets starting at 09:00 on day 4 to 16:00 on day 6, and another fast of 17 hours from 16:00 on day 6 to 09:00 on day 7. During the fasting period, broilers were free access to glucose saline solution (5% of glucose and 0.9% of sodium chloride). Excreta from each replicated cage were collected three times per day through plastic trays from 09:00 on day 4 to 09:00 on day 7 of the energy balance experiment. Meanwhile, the excreta were transferred to a forced air-drying oven at 65 °C. The AME values of experimental diets were determined in two 6 d energy balance experiments with broilers from 11 to 14 and 25 to 28 d of age, respectively.

Chemical analysis

The dry matter (DM) of the sample was determined using the standard method of the Association of Official Analytical Chemists (AOAC, 1990); the gross energy (GE) of diets and excreta was measured according to the method of ISO 9831:1998 using a Parr 6400 automatic adiabatic calorimeter (Parr instrument company, Moline, IL); the nitrogen (N) of diets and excreta were determined by the method of AOAC (1990) using a Kjeldahl nitrogen analyzer and the equation CP = N × 6.25 (model KDY-9820, Shandong Haineng Scientific Instruments Co., Ltd., Dezhou, China); the ether extract (EE) content of ingredients was determined according to the method of AOAC (1990) using an automatic fat analyzer (model SOX-406, Shandong Haineng Scientific Instruments Co., Ltd., Dezhou, Shandong); the crude fiber (CF) and acid detergent fiber (ADF) of ingredients were determined by the method of AOAC (1990). The neutral detergent fiber (NDF) was determined according to the procedure described by Van Soest et al. (1991).

Calculations

All data were expressed on a DM basis. The ME of the experimental diets was calculated using the following formula:

$${\displaystyle \begin{array}{l}{\displaystyle \mathrm{A}\mathrm{M}\mathrm{E}\left(\mathrm{k}\mathrm{c}\mathrm{a}\mathrm{l}/\mathrm{k}\mathrm{g}\right)=(\mathrm{d}\mathrm{i}\mathrm{e}\mathrm{t}\mathrm{i}\mathrm{n}\mathrm{t}\mathrm{a}\mathrm{k}\mathrm{e}\times \mathrm{G}\mathrm{E}\mathrm{c}\mathrm{o}\mathrm{n}\mathrm{t}\mathrm{e}\mathrm{n}\mathrm{t}\mathrm{o}\mathrm{f}\mathrm{d}\mathrm{i}\mathrm{e}\mathrm{t}\text{-}\mathrm{e}\mathrm{x}\mathrm{c}\mathrm{r}\mathrm{e}\mathrm{t}\mathrm{a}\times }\\ \mathrm{G}\mathrm{E}\mathrm{c}\mathrm{o}\mathrm{n}\mathrm{t}\mathrm{e}\mathrm{n}\mathrm{t}\mathrm{o}\mathrm{f}\mathrm{e}\mathrm{x}\mathrm{c}\mathrm{r}\mathrm{e}\mathrm{t}\mathrm{a})/\mathrm{d}\mathrm{i}\mathrm{e}\mathrm{t}\mathrm{i}\mathrm{n}\mathrm{t}\mathrm{a}\mathrm{k}\mathrm{e}\end{array}}$$

$${\displaystyle \begin{array}{l}{\displaystyle \mathrm{A}\mathrm{M}\mathrm{E}\mathrm{n}\left(\mathrm{k}\mathrm{c}\mathrm{a}\mathrm{l}/\mathrm{k}\mathrm{g}\right)=\mathrm{A}\mathrm{M}\mathrm{E}-(\mathrm{R}\mathrm{N}\times 8.22)/\mathrm{F}\mathrm{I}}\end{array}}$$

in which RN (retained nitrogen, g) = diet intake (g) × N content of diet (%) − excreta (g) × N content of excreta (%); FI is the feed intake (kg); 8.22 is the nitrogen correction factor (kcal/g).

The ME of feed ingredients was calculated according to the formula of Kong and Adeola (2014):

$${\displaystyle \begin{array}{l}{\displaystyle \mathrm{A}\mathrm{M}{\mathrm{E}}_{\mathrm{t}}\left(\mathrm{k}\mathrm{c}\mathrm{a}\mathrm{l}/\mathrm{k}\mathrm{g}\right)=\mathrm{A}\mathrm{M}{\mathrm{E}}_{\mathrm{b}\mathrm{d}}+[(\mathrm{A}\mathrm{M}{\mathrm{E}}_{\mathrm{e}\mathrm{d}}-\mathrm{A}\mathrm{M}{\mathrm{E}}_{\mathrm{b}\mathrm{d}})/{\mathrm{P}}_{\mathrm{i}}]}\end{array}}$$

$${\displaystyle \begin{array}{l}{\displaystyle \mathrm{A}\mathrm{M}\mathrm{E}{\mathrm{n}}_{\mathrm{t}}\left(\mathrm{k}\mathrm{c}\mathrm{a}\mathrm{l}/\mathrm{k}\mathrm{g}\right)=\mathrm{A}\mathrm{M}\mathrm{E}{\mathrm{n}}_{\mathrm{b}\mathrm{d}}+[(\mathrm{A}\mathrm{M}\mathrm{E}{\mathrm{n}}_{\mathrm{e}\mathrm{d}}-\mathrm{A}\mathrm{M}\mathrm{E}{\mathrm{n}}_{\mathrm{b}\mathrm{d}})/{\mathrm{P}}_{\mathrm{i}}]}\end{array}}$$

in which AME_bd, AME_ed, or AME_t is the AME of basal diet, experimental diet, or test ingredient; AMEn_bd, AMEn_ed, or AMEn_t is the AMEn of basal diet, experimental diet, or test ingredient; P_i (%) is the proportion of DM from the test ingredient in the experimental diet.

Statistical analysis

Summary statistics were calculated using the MEANS procedure of SAS 9.4 (SAS Inst. Inc., Cary, NC). The GLM procedure of SAS 9.4 (SAS Inst. Inc., Cary, NC) was used to analyze the ME or ME/GE among experimental diets or feed ingredients within the two ages (days 11 to 14; days 25 to 28), and their interactions. Means were separated by the Tukey-Honest significant difference. The CONTRAST statement in the GLM procedure of SAS 9.4 (SAS Inst. Inc., Cary, NC) was performed to compare the different levels of age on the ME or ME/GE of the same experimental diets or feed ingredients. The REG procedure of SAS 9.4 (SAS Inst. Inc.) was used to regress ME of experimental diets or ingredients in broilers from 25 to 28 against 11 to 14 d of age. Differences were significant at P < 0.05, whereas 0.05 ≤ P ≤ 0.10 was considered a trend.

Results

Metabolizable energy and ME/GE of CG diets or CG fed to broilers

Trends toward interactions between age and source of CG were observed on the AME, AMEn, AME/GE, and AMEn/GE of diets (0.05 < P < 0.10; Table 3). The AME, AME/GE, AMEn, and AMEn/GE in diets of corn were greater for broilers from 25 to 28 than 11 to 14 d of age (P < 0.05). However, the AME, AME/GE, AMEn, and AMEn/GE in diets of WF A and WF B were not affected by the age of the broilers. The AME, AME/GE, AMEn, and AMEn/GE in the diets of corn and WF A were not different but greater than those in the diet of WF B (P < 0.05).

Table 3.

Metabolizable energy and ME/GE of CG diets or CG fed to AA broilers from 11 to 14 and 25 to 28 d of age

Item		CG diet				CG
		AME, kcal/kg DM	AMEn, kcal/kg DM	AME/GE, %	AMEn/GE, %	AME, kcal/kg DM	AMEn, kcal/kg DM	AME/GE, %	AMEn/GE, %
Days 11–14	Corn	3,497	3,367	79.60	76.64	3,682	3,611	83.03	81.44
	WF A	3,523	3,377	80.12	76.81	3,750	3,642	84.29	81.85
	WF B	3,416	3,265	77.56	74.15	3,477	3,356	77.84	75.14
Days 25–28	Corn	3,580	3,453	81.47	78.58	3,879	3,814	87.49	86.01
	WF A	3,550	3,406	80.74	77.48	3,810	3,705	85.64	83.27
	WF B	3,404	3,253	77.29	73.87	3,439	3,314	76.99	74.19
SEM		21	20	0.48	0.44	53	49	1.19	1.11
Age	Days 11–14	3,479	3,337b	79.09	75.87b	3,636	3,536	81.72	79.48
	Days 25–28	3,511	3,371a	79.83	76.64a	3,709	3,611	83.37	81.16
CG	Corn	3,539a	3,410a	80.54a	77.61a	3,780a	3,712a	85.26a	83.72a
	WF A	3,536a	3,392a	80.43a	77.15a	3,780a	3,673a	84.96a	82.56a
	WF B	3,410b	3,259b	77.42b	74.01b	3,458b	3,335b	77.42b	74.67b
Variance of sources, P-value
	Age	0.065	0.041	0.068	0.040	0.100	0.074	0.098	0.073
	CG	<0.001	<0.001	<0.001	<0.001	<0.001	<0.001	<0.001	<0.001
	Age×CG	0.095	0.057	0.095	0.056	0.098	0.059	0.096	0.058
Days 11–14 contrast to days 25–28, P-value
	Corn	0.009	0.004	0.009	0.004	0.013	0.007	0.012	0.007
	WF A	0.366	0.299	0.370	0.296	0.427	0.371	0.427	0.371
	WF B	0.700	0.658	0.691	0.659	0.614	0.547	0.615	0.548

^a,b Within an age or CG group, means without a common superscript differ significantly (P < 0.05).

Trends toward interactions between age and source of CG were observed on the AME, AMEn, AME/GE, and AMEn/GE of CG (0.05 < P < 0.10). The AME, AME/GE, AMEn, and AMEn/GE in corn were greater for broilers from 25 to 28 than 11 to 14 d of age (P < 0.05). However, the AME, AME/GE, AMEn, and AMEn/GE in WF A and WF B were not affected by the age of broilers. The AME, AMEn, AME/GE, and AMEn/GE in corn and WF A were not different but greater than those in WF B (P < 0.05).

Metabolizable energy and ME/GE of OM diets or OM fed to broilers

No interactions between age and source of OM were observed on the AME, AMEn, AME/GE, and AMEn/GE of diets (Table 4). The AME, AMEn, AME/GE, and AMEn/GE of OM diets were not affected by the age of broilers, but the AME, AMEn, AME/GE, and AMEn/GE in diets of SBM and PNM were greater than those in diet with CSM (P < 0.05).

Table 4.

Metabolizable energy and ME/GE of OM diets or OM fed to AA broilers from 11 to 14 and 25 to 28 d of age

Item		OM diet				OM
		AME, kcal/kg DM	AMEn, kcal/kg DM	AME/GE, %	AMEn/GE, %	AME, kcal/kg DM	AMEn, kcal/kg DM	AME/GE, %	AMEn/GE, %
Days 11–14	SBM	3,238	3,033	73.28	68.64	2,683	2,335	57.53	50.07
	PNM	3,198	3,010	72.61	68.36	2,497	2,241	54.33	48.75
	CSM	3,147	2,949	71.26	66.77	2,242	1,931	47.94	41.29
Days 25–28	SBM	3,233	3,035	73.16	68.69	2,634	2,315	56.48	49.66
	PNM	3,239	3,049	73.56	69.24	2,682	2,402	58.34	52.25
	CSM	3,163	2,968	71.62	67.21	2,301	1,997	49.20	42.71
SEM		22	19	0.50	0.44	111	97	2.38	2.08
Age	Days 11–14	3,194	2,997	72.38	67.92	2,474	2,169	53.27	46.70
	Days 25–28	3,212	3,017	72.78	68.38	2,539	2,238	54.67	48.21
OM	SBM	3,235a	3,034a	73.22a	68.67a	2,658a	2,325a	57.01a	49.87a
	PNM	3,218a	3,030a	73.09a	68.80a	2,589a	2,321a	56.33a	50.50a
	CSM	3,155b	2,958b	71.44b	66.99b	2,271b	1,964b	48.57b	42.00b
Variance of sources, P-value
	Age	0.338	0.213	0.340	0.213	0.481	0.386	0.475	0.383
	OM	0.003	0.001	0.002	< 0.001	0.003	0.001	0.002	<0.001
	Age×OM	0.577	0.645	0.575	0.643	0.579	0.651	0.572	0.645
Days 11–14 contrast to days 25–28, P-value
	SBM	0.870	0.932	0.868	0.938	0.755	0.890	0.757	0.889
	PNM	0.194	0.166	0.193	0.167	0.249	0.247	0.242	0.243
	CSM	0.605	0.487	0.611	0.485	0.710	0.632	0.712	0.633

^a,b Within an OM group, means without a common superscript differ significantly (P < 0.05).

No interactions between age and source of OM were observed on the AME, AMEn, AME/GE, and AMEn/GE of OM. The AME, AMEn, AME/GE, and AMEn/GE of OM were not affected by the age of broilers, but the AME, AMEn, AME/GE, and AMEn/GE in SBM and PNM were greater than those in CSM (P < 0.05).

Metabolizable energy and ME/GE of CGM diets or CGM fed to broilers

Significant interaction between age and sources of CGM was observed on the AME, AMEn, AME/GE, and AMEn/GE of diets (P < 0.05; Table 5). The AME and AMEn of CGM A diet were not different from those with CGM B but numerically less than those on CGM C diet fed to broilers from 11 to 14 d of age. However, the AME and AMEn of diet with CGM A were greater than those with CGM B (P < 0.05) and numerically greater than those on CGM C diet when fed to broilers from 25 to 28 d of age. The AME/GE or AMEn/GE of diet with CGM A was numerically less than those with CGM C fed to broilers from 11 to 14 d of age. However, those in diet with CGM A was numerically greater than those on CGM C diet fed to broilers from 25 to 28 d of age. The AME, AMEn, AME/GE, and AMEn/GE of CGM diets were less for broilers from 11 to 14 than 25 to 28 d of age (P < 0.05).

Table 5.

Metabolizable energy and ME/GE of CGM diets or CGM fed to AA broilers from 11 to 14 and 25 to 28 d of age

Item		CGM diet				CGM
		AME, kcal/kg DM	AMEn, kcal/kg DM	AME/GE, %	AMEn/GE, %	AME, kcal/kg DM	AMEn, kcal/kg DM	AME/GE, %	AMEn/GE, %
Days 11–14	CGM A	3,438bc	3,256bc	76.30b	72.25b	3,786bc	3,535bc	70.73b	66.05b
	CGM B	3,394c	3,217c	75.14c	71.22c	3,494c	3,277c	64.20c	60.21c
	CGM C	3,484b	3,298b	76.98b	72.87b	4,082b	3,805b	74.72b	69.66b
Days 25–28	CGM A	3,562a	3,368a	79.05a	74.74a	4,561a	4,222a	85.22a	78.88a
	CGM B	3,482b	3,299b	77.10b	73.04b	4,021b	3,755b	73.89b	69.00b
	CGM C	3,548a	3,356a	78.39a	74.14a	4,464a	4,137a	81.71a	75.74a
SEM		12	10	0.26	0.23	74	66	1.37	1.22
Age	Days 11–14	3,439	3,257	76.14	72.11	3,787	3,539	69.89	65.31
	Days 25–28	3,531	3,341	78.18	73.98	4,349	4,038	80.28	74.54
CGM	CGM A	3,500	3,312	77.67	73.50	4,174	3,879	77.98	72.47
	CGM B	3,438	3,258	76.12	72.13	3,758	3,516	69.05	64.60
	CGM C	3,516	3,327	77.69	73.51	4,273	3,971	78.22	72.70
Variance of sources, P-value
	Age	<0.001	<0.001	< 0.001	<0.001	<0.001	<0.001	<0.001	<0.001
	CGM	<0.001	<0.001	<0.001	<0.001	<0.001	<0.001	<0.001	<0.001
	Age×CGM	0.045	0.042	0.042	0.040	0.040	0.038	0.032	0.031
Days 11–14 contrast to days 25–28, P-value
	CGM A	<0.001	<0.001	<0.001	<0.001	<0.001	<0.001	<0.001	<0.001
	CGM B	<0.001	<0.001	<0.001	<0.001	<0.001	<0.001	<0.001	<0.001
	CGM C	<0.001	<0.001	<0.001	<0.001	0.001	0.001	0.001	0.001

^a-c Within an age × CGM group, means without a common superscript differ significantly (P <0.05).

Significant interactions between age and source of CGM were observed on the AME, AMEn, AME/GE, and AMEn/GE of CGM (P < 0.05). The AME and AMEn of CGM A were not different from those of CGM B but numerically less than those of CGM C in broilers from 11 to 14 d of age. However, the AME and AMEn of CGM A were greater than those of CGM B (P < 0.05) and numerically greater than those of CGM C in broilers from 25 to 28 d of age. The AME/GE or AMEn/GE of CGM A was numerically less than those of CGM C in broilers from 11 to 14 d of age. However, those of CGM A was numerically greater than those of CGM C in broilers from 25 to 28 d of age. The AME, AMEn, AME/GE, and AMEn/GE of CGM were less for broilers from 11 to 14 than 25 to 28 d of age (P < 0.05).

Metabolizable energy and ME/GE of FM diets or FM fed to broilers

No interactions between age and source of FM were observed on the AME, AMEn, AME/GE, and AMEn/GE of diets (Table 6). The AME, AMEn, AME/GE, and AMEn/GE of FM diets were not affected by the sources of FM but were less for broilers from 11 to 14 compared to 25 to 28 d of age (P < 0.01).

Table 6.

Metabolizable energy and ME/GE of FM diets or FM fed to AA broilers from 11 to 14 and 25 to 28 d of age

Item		FM diet				FM
		AME, kcal/kg DM	AMEn, kcal/kg DM	AME/GE, %	AMEn/GE, %	AME, kcal/kg DM	AMEn, kcal/kg DM	AME/GE, %	AMEn/GE, %
Days 11–14	FM A	3,196	3,016	71.04	67.03	1,656	1,382	28.96	24.17
	FM B	3,240	3,063	72.02	68.09	2,024	1,782	34.97	30.78
	FM C	3,197	3,022	71.42	67.52	1,641	1,423	29.31	25.42
Days 25–28	FM A	3,375	3,179	75.02	70.67	3,328	2,891	58.21	50.58
	FM B	3,363	3,174	74.74	70.54	3,203	2,819	55.34	48.71
	FM C	3,331	3,142	74.41	70.19	2,896	2,522	51.72	45.03
SEM		18	16	0.39	0.35	172	153	3.09	2.67
Age	Days 11–14	3,211b	3,034b	71.49b	67.54b	1,774b	1,529b	31.08b	26.79b
	Days 25–28	3,356a	3,165a	74.72a	70.46a	3,142a	2,744a	55.09a	48.11a
FM	FM A	3,286	3,098	73.03	68.85	2,492	2,136	43.59	37.37
	FM B	3,302	3,119	73.38	69.31	2,613	2,300	45.15	39.75
	FM C	3,264	3,082	72.91	68.85	2,269	1,972	40.52	35.23
Variance of sources, P-value
	Age	<0.001	<0.001	<0.001	<0.001	<0.001	<0.001	<0.001	<0.001
	FM	0.119	0.080	0.466	0.318	0.146	0.117	0.307	0.253
	Age×FM	0.256	0.200	0.259	0.204	0.320	0.259	0.317	0.258
Days 11–14 contrast to days 25–28, P-value
	FM A	<0.001	<0.001	<0.001	<0.001	<0.001	<0.001	<0.001	<0.001
	FM B	<0.001	<0.001	<0.001	<0.001	<0.001	<0.001	<0.001	<0.001
	FM C	<0.001	<0.001	<0.001	<0.001	<0.001	<0.001	<0.001	<0.001

^a,b Within an age group, means without a common superscript differ significantly (P < 0.05).

No interactions between age and source of FM were observed on the AME, AMEn, AME/GE, and AMEn/GE of FM. The AME, AMEn, AME/GE, and AMEn/GE of FM were not affected by the source of FM but were less for broilers from 11 to 14 compared to 25 to 28 d of age (P < 0.01).

Relationship between ME determined with broilers from 11 to 14 and 25 to 28 D of age

The relationship between ME of experimental diets or feed ingredients determined with broilers from 11 to 14 and 25 to 28 d of age is presented in Fig.1. The slopes of the regressions for AME or AMEn in diets of CG and OM determined with broilers from 25 to 28 d of age (AME_25–28, AMEn_25–28) against 11 to 14 d of age (AME_11–14, AMEn_11–14) were not different from 1 and the intercepts were not different from 0, so the two regression lines overlapped for y = x. However, the positions of diets with CGM and FM distributed on the plots of AME_25–28 vs. AME_11–14 or AMEn_25–28 vs. AMEn_11–14 were above the line y = x. Similarly, the regression lines of AME_25–28 on AME_11–14 and AMEn_25–28 on AME_11–14 for CG and OM overlapped the line for y = x, but the positions of CGM and FM distributed on the plots of AME_25–28 vs. AME_11–14 or AMEn_25–28 vs. AMEn_11–14 were above the line y =x.

Figure 1.

Relationship between metabolizable energy of experimental diets or feed ingredients determined with broilers from 11 to 14 and 25 to 28 d of age. (a) Solid line is the regression line of AME_25–28 on AME_11–14 in diets of corn, WF A, WF B, SBM, PM, and CSM. AME_25–28 = 1.070 × AME_11–14 − 208 (P_regression < 0.001; R² = 0.97; RMSE= 37 kcal/kg DM; P_slope = 0.526, [H₀: slope = 1, H_α: slope ≠ 1]; P_intercept = 0.570, [H₀: intercept = 0, H_α: intercept ≠ 0]). (b) Solid line is the regression line of AMEn_25–28 on AMEn_11–14 in diets of corn, WF A, WF B, SBM, PM, and CSM. AMEn_25–28 = 1.063 × AMEn_11–14 − 173 (P_regression < 0.001; R² = 0.98; RMSE = 36 kcal/kg DM; P_slope = 0.491; P_intercept = 0.549). (c) Solid line is the regression line of AME_25–28 on AME_11–14 in corn, WF A, WF B, SBM, PM, and CSM. AME_25–28 = 1.007 × AME_11–14 + 46 (P_regression < 0.001; R² = 0.98; RMSE = 118 kcal/kg DM; P_slope = 0.930; P_intercept= 0.862). (d) Solid line is the regression line of AMEn_25–28 on AMEn_11–14 in corn, WF A, WF B, SBM, PM, and CSM. AMEn_25–28 = 1.011 × AMEn_11–14 + 39 (P_regression < 0.001; R² = 0.98; RMSE = 108 kcal/kg DM; P_slope = 0.865; P_intercept = 0.842).

Discussion

The intestinal weight at 28 d of age was 1.25 times greater than 14 d of age for fast-growing broilers (Manyelo et al., 2022), and the expression of intestinal transporters and villus surface area changed as broilers age (Li et al., 2020). These findings indicate the digestive tract changes significantly as fast-growing broilers age. As broilers age, some bacterial species can evolve to ferment undigested components of ileal digesta consequently increasing energy utilization (Wronkowska et al., 2017). However, the contribution of fermentation to dietary ME in broilers is less than in other animals (Apajalahti and Vienola, 2016). In addition, the digesta passage time was approximately 20% longer in broilers on day 28 than on day 14 (Ye et al., 2022), which could increase dietary nutrient digestibility with age (Xu et al., 2015). These age-related changes to digestive physiology may result in better digestibility during the grower relative to the starter phase. However, many studies have shown that the effects of broiler age on nutrient digestion vary with feed ingredients (Bertechini et al., 2019; Khalil et al., 2021), suggesting age and source of feed ingredients interact with nutrient digestibility.

In this study, the ME of corn was less in broilers on days 11 to 14 than those on days 25 to 28. However, the ME of WF A or B was not affected by age of broilers. This result was similar to that reported by Khalil et al. (2021) who observed the AME or AMEn of corn was less for broilers from 7 to 14 compared to 21 to 28 d of age (3,587 vs. 3,719 kcal/kg DM for AME; 3,542 vs. 3,659 kcal/kg DM for AMEn), but they found the AME or AMEn of wheat was not affected by age. Zelenka and Čerešňáková (2005) reported that age of broilers had a reduced effect on starch digestibility of the corn-wheat diet. Barua et al. (2021b) and An and Kong (2022) described the standard ileal digestibility of amino acids (SIAAD) in corn was less in broilers from 10 to 14 compared to 21 to 22 d of age. However, Szczurek et al. (2020) observed that the SIAAD in wheat was not affected by age (88% vs. 87% for mean digestibility of 10 essential amino acids on days 14 and 28, respectively). In addition, digestibility of fat for broilers was greater on days 21 to 35 than on day 7 (Tancharoenrat et al., 2013). The fat content in corn is greater than in WF, so effect of broiler age on the ME may relate to differences in digestibility of fat. In the current study, the ME of WF A was close to corn, while the ME of WF B was less than corn. These findings related to a greater removal of husks in the production of WF A than WF B. In fact, the fiber content of WF A was much less than WF B, thereby increasing the relative ME value of WF A. This result is supported by the data from Yegani et al. (2013), who found a negative relationship between fiber content and ME of wheat and by-products in broilers.

The three OM including SBM, PNM, and CSM, generally contained greater CP (>51.9%), ash (>6.3%), and fiber (CF > 4.3%), and less content of ether extract (<1.7%) relative to CG. The three OM had similar ME in broilers of different ages. Huang et al. (2005) reported that the apparent ileal amino acid digestibility (AIAAD) of SBM in broilers on day 28 was 2% greater than that on day 14 (85% vs. 87%), while the AIAAD of CSM was similar in broilers on days 28 and 14 (69% vs. 70%). The endogenous losses of amino acids of broilers on days 10 to 14 were greater than those on days 22 to 24 (Barua et al., 2021a; An and Kong, 2022). According to the data described by Huang et al. (2005), the SIAAD of SBM and CSM in broilers on day 28 was close to those on day 14, resulting in growth phases having no effect on ME in each of SBM and CSM. The present data also indicate the ME of PNM was not affected by age. The true amino acid digestibility (TAAD) of PNM and SBM was similar in cecectomized adult roosters (Leme et al., 2019), indicating the digestibility of protein of PNM and SBM are close. This reason could lead to comparable ME in present PNM and SBM. The ME values of SBM and PNM exceeded that of CSM, which is consistent with the results reported by CVB (2021). The CSM contains greater fiber content and reduced TAAD than SBM and PNM (Huang et al., 2005). Additionally, CSM has free gossypol which directly inhibits the activity of digestive enzymes such as pepsin, and trypsin (Zhang and Adeola, 2017). These factors could reduce ME in CSM compared to SBM and PNM.

Corn gluten meal is a byproduct of corn processing that contains greater protein (CP > 61%), and less ether extract, ash, and fiber relative to other ingredients. A high concentration of zein (ranging from 30.39% to 57.47% in six samples, Guo et al., 2020) is found in CGM, but the mean AIAAD in broilers over 21 d of age was greater than that of SBM (85% vs. 82%, Ravindran et al., 2005). The ME of three CGM was less in broilers from 11 to 14 than in 25 to 28 d of age, which is consistent with results observed by Guo et al. (2020). This finding likely relates to increased amino acid digestibility of CGM with age of broilers and clearly indicates age influence on the ME of CGM for broilers as the gastrointestinal (GI) tract develops. The ME of the current CGM decreased with increasing NDF, in accordance with findings of Rochell et al. (2011) who report the ME and NDF content of corn byproducts are negatively correlated for broilers. Interestingly, the effect of NDF may depend on age. The current work found that the ME of CGM C (NDF = 7.30%) was greater than CGM A (NDF = 8.39%) in broilers on days 11 to 14, but the ME of those two sources was close on days 25 to 28 of age. The diversity of gut microbiota increases with age of broilers and can modulate digestion of fiber (Mohd Shaufi et al., 2015).

Feather meal contains greater CP (>90.2%) and lower amino acid digestibility relative to SBM (Ravindran et al., 2005; Bandegan et al., 2010). Keratin accounts for more than 90% of the total protein in FM (Xu et al., 2022), it contains greater disulfide bonds, smooth surface structure, compact β-sheet structure, and hydrogen bonds. These structures can be resistant to proteolytic enzymes in the gizzard and intestine of the broiler, especially during phases of accelerated growth. The ME of three FM for broilers was reduced on 11 to 14 compared to 25 to 28 d of age in the current study, indicating the improved digestion of FM as the GI tract develops. Therefore, FM supplementation is not recommended in starter diets for broilers. Others employed keratinase-hydrolyzing, steam-hydrolyzing, or expanding processes to treat fresh poultry feathers to improve their digestibility (Eaksuree et al., 2016; Osunbami and Adeola, 2022). However, no difference was observed in ME for the three FM in the current study, which indicates that there was no efficacy of the process on the digestibility improvement in FM. Similarly, Moritz and Latshaw (2001) and Eaksuree et al. (2016) observed no obvious effect of enzymatic treatment and steam-hydrolyzing condition on the ME or nutritive value of FM sources. Thus, the treatment process of improving the digestibility of FM needs further study.

Conclusion

Our study demonstrated no interactive effects between broiler age and source of feed on ME of OM, and FM, but detected interactive effects for CG and CGM. Thus, the effect of age on ME can depend on the type of feed and its chemical composition. In addition, the ME of WF and OM was not affected by age, but the ME of corn, CGM, and FM increased as broilers aged. These results indicate that the ME in starter diets with corn, CGM, and FM may be overestimated if the ME values of feed ingredients are obtained from growing broilers.

Glossary

Abbreviations

AAD

amino acid digestibility

ADF

acid detergent fiber

AME

apparent metabolizable energy

AMEn

nitrogen-corrected apparent metabolizable energy

BW

body weight

CF

crude fiber

CG

cereal grain

CGM

corn gluten meals

CP

crude protein

CSM

cottonseed meal

EE

ether extract

FM

feather meals

GE

gross energy

ME

metabolizable energy

N

nitrogen

NDF

neutral detergent fiber

OM

oilseed meals

PNM

peanut meal

SBM

soybean meal

SEM

standard error of the mean

WF

wheat flour

Conflict of interest statement

The authors declare no conflict of interest in this study.