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Effects and interactions of dietary lysine and apparent nitrogen corrected metabolizable energy on yellow-feathered broiler breeder hens
Journal of Animal Science and Biotechnology volume 15, Article number: 143 (2024)
Abstract
Background
Dietary lysine and apparent nitrogen-corrected metabolizable energy (AMEn) are two key variables affecting the production of breeder hens. In this study, the effects and interactions of lysine and AMEn on yellow-feathered broiler breeder hens were investigated. A total of 720 30-week-old breeder hens were fed in a 5 (lysine: 0.56%, 0.68%, 0.80%, 0.92%, and 1.04%) × 2 (AMEn: 11.50 and 11.10 MJ/kg) factorial arrangement for 12 weeks. The productive performance, reproductive traits, biochemical variables of breeder hens, the amino acid concentration and quality of eggs, and the growth performance of offspring broilers were determined.
Result
(1) Dietary lysine had quadratic effects (P < 0.05) on laying rate, average daily egg mass and feed intake/egg mass of breeder hens; birds with 11.50 MJ/kg AMEn (high AMEn) had higher (P < 0.05) BW than those with 11.10 MJ/kg AMEn (low AMEn); (2) dietary lysine significantly affected on the relative ovarian weight (quadratic and linear), and numbers of large yellow follicles (LYF, quadratic); birds with high AMEn had longer fallopian tube and more LYF than those with low AMEn (P < 0.05); (3) dietary lysine had significant effects (linear and quadratic) on eggshell thickness and shell strength of eggs from breeder hens; birds with high AMEn had thinner eggshells and deeper yolk color than those with low AMEn (P < 0.05); (4) there were higher (P < 0.05) contents of protein and concentrations of all measured animo acids (AAs) in eggs from birds fed low AMEn; (5) supplementation with high AMEn to breeder hens significantly increased the hatchability of fertilized eggs; (6) neither dietary lysine level or AMEn affected growth performance of offspring broilers; (7) both dietary lysine level and AMEn significantly affected gonadotropin concentrations and biochemical variables of breeder hens.
Conclusions
Dietary lysine had significant influences on productive performance, reproductive traits, and egg quality of yellow-feathered breeder hens. Based on productive performance, the optimal levels of dietary lysine were 0.81% to 0.83%, while 0.71% to 72% lysine was enough to obtain the best quality of breeding eggs. High AMEn was more beneficial to breeder hens for reproductive traits and hatchability of the fertilized eggs, while it showed detrimental effects on eggshell thickness and AA concentrations of breeding eggs.
Introduction
In commercial diets (corn-soybean meal based) for broilers, lysine is one of the most limiting essential amino acids (AAs) and necessary for proper growth and development of chickens [1, 2], especially for the turnover of muscle protein where it produces a marked effect in modulating protein biosynthesis and turnover [3]. Energy, is required for the maintenance of body temperature, and synthesis of organic tissues of broilers [4]. Studies have shown the importance of lysine for reproduction, as it promoted the development of reproductive organs and improved production performance of Ross 308 breeder hens [5] and layer hens [6]. Energy is also critical for egg production of layer hens [4, 7] and higher energy improved productive traits in Ross 308 breeder hens [8]. However, so far, research only showed the effects of lysine or AMEn on productive performance of commercial white-feathered broiler breeder hens, with a lack of studies on yellow-feathered broiler breeder hens. The effects of lysine or AMEn on egg quality of layers were also studied, while there is few study exploring the effects on the hatching performance of eggs from breeder hens, and the growth performance of offspring broilers.
Yellow-feathered broilers provide consumers with high-quality meat products and play an important role in poultry production worldwide [9]. In China, the annual sales of yellow-feathered broilers are approximately four billion birds, comparable to white-feathered broilers [10]. Based on Nutrient Requirements of Yellow Chickens (2020) [11], the recommended dietary lysine for broiler breeder hens was 0.68% to 0.78%. There was 0.56% lysine in the basal diet used in this research (without L-lysine supplementation), so 5 levels of lysine (0.56%, 0.68%, 0.80%, 0.92%, and 1.04%) were used. Dietary energy is closely related to the development of sexual organs, and higher energy increased weight of sexual organs, thus improved the productive performance of broiler breeder pullets [8], so the recommended AMEn (11.10Â MJ/kg, 2,650Â kcal/kg) from Nutrient Requirements of Yellow Chickens [11] and a higher one (11.50Â MJ/kg, 2,750Â kcal/kg) were used in this research. The productive performance, reproductive traits, biochemical variables of breeder hens, the concentrations of amino acid, quality, and hatching performance of eggs, and the growth performance of offspring broilers were determined to clear explain the effects of lysine and AMEn on breeder hens, and to obtain the optimal nutrient levels for yellow-feathered breeder hens. The results will provide guidance for practical production of yellow-feathered breeder hens.
Materials and methods
Experimental design and chicken husbandry
The present study used a 5 × 2 factorial arrangement of treatments to assess main effects and interaction of dietary lysine (0.56%, 0.68%, 0.80%, 0.92%, and 1.04%) and AMEn (11.50 and 11.10 MJ/kg) in yellow-feathered breeder hens (Table 1). A total of 720 30-week-old breeder hens (2.55 ± 0.18 kg) with similar laying rates were used. Birds were randomly allocated to the 10 treatments and received diets supplemented with incremental levels of lysine and AMEn for 12 weeks. Each treatment contained 6 replicates with 12 birds per replicate. The breeders were housed in laying cages (325 mm × 450 mm × 410 mm, 2 birds/cage), and provided with 120 g/d of feed per bird, and access to fresh water ad libitum. Birds were exposed to 16 h light daily.
During the last 2 weeks, each breeder received artificial insemination every 3 d (25 μL, pooled semen). At the end of the trial, 20 eggs per replicate were incubated [12]. Fifteen hatched chicks per replicate were raised with the same diets for 84 d. The rearing and husbandry of offspring broilers was as already described [13].
Experimental diets
The basal diets were formulated according to the recommended nutrition of breeder hens and nutritive values of feedstuffs in Nutrient Requirements of Yellow Chickens [11]. The details of basal diets for breeder hens and offspring broilers are provided in Tables 2 and 3, respectively. The crude protein of diets was determined according to the Association of Official Analytical Chemists [14]. Lysine level in diets was determined using the hydrolysis and extraction method [15]. In brief, proteins in feed were hydrolyzed into AAs in hydrochloric acid solution at 110 °C, separated by ion exchange chromatography and derivatized by ninhydrin column, and then determined at a wavelength of 570 nm with AA analyzer (L-8900, Hitachi High-Technologies, Tokyo, Japan).
Measurement of reproductive performance
At the end of the trial, the body weight (BW) of breeder hens was recorded. Eggs were counted and weighed every day, and daily egg mass per replicate was calculated. The unqualified eggs (excessively large or small, misshapen, dirty, with sand shell or without a shell) were recorded. The variables of reproductive performance were calculated using the formulas:
Sample collection
Two breeder hens of each replicate were chosen at the end of the trial and blood was collected in evacuated EDTA-K2 tubes from the wing vein. Plasma was then obtained by centrifuging (1,000 × g, 15 min, 4 °C). These 2 birds were then electrically stunned and exsanguinated. The carcass was dissected. The ovaries and oviducts including the infundibulum, enlargement, isthmus, and uterus were removed. The ovarian stroma, remaining after dissection of large and small yellow follicles, was collected and snap-frozen in liquid nitrogen. When used for the determination of biochemical variables, the ovarian stroma was homogenized with ice-cold PBS (1:10, v/v), and clarified supernatant was obtained after centrifuging (2,000 × g, 10 min).
Analysis of reproductive traits
The weight of oviduct was measured. The large yellow follicles (LYF, > 8 mm) and small yellow follicles (SYF, 3–8 mm) were identified and counted by measuring the diameter with a Vernier caliper. The ovarian stroma, oviduct, LYF, and SYF were weighed, respectively. The relative weight of these organs or tissues relative to BW was calculated as follows:
Determinations of egg quality
At 10th week of the study, 3 eggs/replicate (close to the average egg weight) were chosen to determine the egg quality. The major and minor axises were measured with a micrometer. An automatic egg analyzer (EMT-5200 Robotmation Co., Ltd., Tokyo, Japan) was used to determine the yolk color, albumen height, and Haugh unit. An eggshell strength tester (FGV-10XY, Orka Food Technology, Ramat HaSharon, Israel) was used to measure eggshell strength. The yolk was weighed, and eggshell thickness was measured with a micrometer. The relative yolk weight to egg weight and the shape index of egg was calculated using the formulas:
Measurement of hatching quality
At hatch, the weight of chicks was recorded, and the hatching weight of chick/egg weight was calculated.
Determinations of amino acid concentrations in eggs
At the end of the trial, for birds treated with 0.56%, 0.80%, and 1.04% lysine (treatments I, III, V, VI, VIII, and X), one egg per replicate was selected to determine concentrations of AAs. After removing eggshell, the yolk and albumen were together weighed and freeze-dried. Crude protein and dry matter were analyzed according to the Association of Official Analytical Chemists [14]. Quantitative analysis of AAs in eggs was performed using the hydrolysis and extraction method, with subsequent readings via HPLC by Guangzhou KingMed Diagnostics Group Co., Ltd. (Guangzhou, China).
Measurement of growth performance of offspring broilers
The growth performance of the offspring from each replicate was determined. Birds were weighed at 1 and 84 days of age. Dead birds were recorded. The final BW, average daily feed intake, average daily gain, feed to gain ratio, and mortality were calculated.
Determinations of biochemical variables and gonadotropin concentration in breeders
The activities of alkaline phosphatase (AKP), total antioxidant capacity (T-AOC), total superoxidase dismutase (T-SOD), glutamic oxaloacetic transaminase (GOT) and glutamic pyruvic transaminase (GPT), and the concentration of uric acid (UA), malondialdehyde (MDA), total protein (TP), and albumin (ALB) in the plasma, along with the activities of T-AOC and T-SOD and the concentration of MDA in ovarian stroma were analyzed spectrophotometrically using commercial kits (A059-1-1, A015-1-2, A001-1-2, C010-1-1, C009-1-1, C012-1-1, A003-1-2, A045-2-2 and A028-1-1, Nanjing Jiancheng Bioengineering Institute, Nanjing, China) and a spectrophotometer (Biomate 5, Thermo Electron Corporation, Rochester, NY, USA). The level of follicle stimulating hormone (FSH) in plasma was determined with ELISA kits (Jiangsu Meimian Industrial Co., Ltd., Jiangsu, China) and the above spectrophotometer.
Statistical analysis
The main effects (lysine and AMEn) and interactions between them were examined by multivariate analysis of variance using SPSS 17.0 for Windows. Means were compared by Duncan multiple range tests at P < 0.05 significance levels. Furthermore, in the case of a significant effect (P < 0.05) of lysine × AMEn interaction, the linear and quadratic effect of lysine × AMEn were also analyzed to better describe the cause of the interaction (SAS 8.1) [16].
Where appropriate, polynomial regressions were fitted to test for linear and quadratic effects in response to lysine. When a significant quadratic component was demonstrated (P < 0.05), optimal dietary lysine was estimated as the lower level achieving 95% of the maximal or minimal response. When an interaction is significant, analysis of polynomial regressions was conducted separately for two AMEn levels.
Results
Productive performance
As shown in Table 4, dietary lysine had quadratic effects (P < 0.05) on laying rate, average daily egg mass and feed intake/egg mass of yellow-feathered breeder hens. The optimal levels of dietary lysine estimated from the quadratic regressions were 0.83%, 0.82%, and 0.81% for laying rate, average daily egg mass, and feed intake/egg mass, respectively.
Dietary AMEn had a significant effect on final BW of breeder hens, and birds with 11.50 MJ/kg AMEn had higher body weight than those with 11.10 MJ/kg AMEn (P < 0.05). Furthermore, there was no interaction (P > 0.05) between dietary lysine and AMEn on variables of productive performance.
Reproductive traits
As presented in Table 5, dietary lysine had significant effect on the relative weight of ovarian stroma (quadratic and linear), and numbers of LYF (quadratic). Dietary AMEn had significant influence on the numbers of LYF, and birds with 11.50 MJ/kg AMEn had more LYF than those with 11.10 MJ/kg AMEn (P < 0.05).
Interactions existed between dietary lysine and AMEn for the relative ovarian weight and numbers of LYF. The optimal levels of dietary lysine estimated. For numbers of LYF, the optimal lysine level was 0.76% when AMEn was 11.50 MJ/kg, and 0.92% when AMEn was 11.10 MJ/kg, respectively.
Egg quality
Dietary lysine had both linear and quadratic effects (P < 0.05) on eggshell thickness and shell strength of eggs from breeder hens (Table 6). Dietary AMEn significantly affected on eggshell thickness and yolk color (P < 0.05), and birds with 11.50 MJ/kg AMEn had thinner eggshell and deeper yolk color than those fed 11.10 MJ/kg AMEn (P < 0.05).
Interactions were found between lysine and AMEn for eggshell strength (P < 0.05) and yolk color (P < 0.05). The optimal levels of dietary lysine from the quadratic regressions were 0.71% for eggshell strength (when AMEn was 11.50 MJ/kg), and 0.72% for eggshell thickness.
Concentrations of amino acids in eggs
As shown in Table 7, there were higher (P < 0.05) levels of DM, CP, and concentrations of all measured AAs in eggs from birds fed 11.10 compared to 11.5 MJ/kg AMEn. Dietary lysine only affected concentrations of proline in eggs, where those in eggs from birds fed 0.80% and 1.02% lysine were increased over birds fed 0.56% lysine.
Interactions existed (P < 0.05) between dietary lysine and AMEn for the concentrations of total AAs, alanine, arginine, aspartic acid, glycine, isoleucine, leucine, proline, serine, threonine, tyrosine, and valine.
Hatching performance
Table 8 shows that dietary lysine did not affect the hatching performance of yellow-feathered breeder hens (P > 0.05). Dietary AMEn had significant effect on hatchability of fertilized eggs, where birds given 11.50 MJ/kg AMEn out-performed (P < 0.05) those fed 11.10 MJ/kg AMEn. Significant interactions (P < 0.05) between lysine and AMEn existed for hatchability of fertilized eggs.
Growth performance of offspring broilers
Table 9 shows that, neither main effect of dietary lysine level or AMEn, nor interactions between them affected growth performance of offspring broilers (P > 0.05).
Concentration of gonadotrophins in plasma and biochemical variables in plasma and ovarian stroma
Table 10 shows that dietary lysine affected the concentration of FSH (linear and quadratic, P < 0.05) in the plasma of breeder hens. The level of FSH was decreased in birds with 11.10 rather than 11.50 MJ/kg AMEn (P < 0.05). In the case of plasmal FSH, significant interactions (P < 0.05) existed between dietary lysine and AMEn.
Lysine significantly affected on the levels of TP (quadratic and linea), ALB (quadratic and linear), UA, the T-AOC activity (linear) in plasma, and the MDA level (quadratic) and T-SOD activity (quadratic and linear) in ovarian stroma. The levels of ALB, MDA and the activity of AKP in plasma, the level of MDA and the activity of T-AOC in ovarian stroma were increased. The level of UA and the activity of T-AOC in plasma were decreased in birds with 11.50 MJ/kg AMEn rather than those with 11.10 MJ/kg AMEn (P < 0.05). Interactions existed (P < 0.05) between lysine and AMEn for the levels of ALB and MDA in plasma, and the level of MDA and the activity of T-SOD in ovarian stroma.
Discussion
Effect and interaction of dietary lysine and AMEn on productive performance and reproductive traits of yellow-feathered breeder hens
Lysine is required for protein synthesis [17], thus is essential for the growth and reproduction of chickens. Our research showed that dietary lysine had quadratic effects on laying rate, average daily egg mass and feed intake/egg mass of breeder hens. Previous study showed that, to a certain extent, high dietary lysine increased laying rate, and settable egg production of Ross 308 breeder hens [4]. There was not much research on breeder hens, but for Lohmann Brown layer hens, egg production and egg mass were decreased and FCR was increased when dietary lysine levels were higher than 0.9% [6]. In research with laying ducks, egg production and egg weight were increased linearly and quadratically as dietary lysine levels increased [18]. These together with the current study suggested that excessive or insufficient lysine has adverse effects on productive performance of breeder hens. For yellow-feathered breeder hens, the optimal lysine levels for productive performance were estimated to be 0.81% to 0.83%, which were higher than the requirement for egg production of white-feathered breeder hens [5] (0.71% to 0.77%, Ross 308), and also higher than the recommendation of Nutrient Requirements of Yellow Chickens (0.68% to 0.78%) [11].
In the current study, different lysine levels affected the egg production with no influence on BW of breeder hens, the same with research on Ross 308 breeder hens [5]. Joseph et al. [19] founded that there was no difference on BW of Cobb 500 broiler breeders, but egg production in responses to crude protein level was observed, and Mohiti-Asli et al. [20] suggested that the BW of matured hens might be more susceptible to energy intake. Part of the energy received is directedly used for fat deposition and BW gain [21], thus dietary AMEn has a significant effect on final BW of breeder hens. The current research suggested that birds given high AMEn (11.50 MJ/kg) had higher BW than those provided with low AMEn (11.10 MJ/kg). Similarly, Lu et al. [7] found that the BW of laying breeders decreased linearly with increasing energy restriction; geese received a high ME diet caused an increased weight in liver and abdominal fat [12]. It is worth noting that, in diets with low AMEn, there was more wheat bran used (as Table 2 shown), indicating that fiber might partly contributed to the difference in BW, as Mohiti-Asli et al. [20] found that dietary fiber decreased the BW gain and abdominal fat weight of broiler breeder hens.
Dietary energy is closely related to the development of sexual organs. Previous research found that energy-restricted feeding delayed development of sexual organs, including the number of LYF, oviductal length, and relative weight of ovarian stroma and fallopian tube, and delayed sexual maturity [7, 22]. Feed restriction slowed the growth rate of the follicle and fallopian tube, thereby constrained development of sexual organs of breeder hens [23]. Higher energy increased ovarian weight of Ross 308 broiler breeder pullets, presumably because it partitioned extra nutrients for ovarian development [8]. In the present research, high AMEn increased the numbers of LYF. Birds with high AMEn also had heavier ovarian stroma, but the impact was not significant, and the difference between the current and previous result of white-feathered breeders [8] might be due to the difference in the breed or age of birds (the birds used in the current research were in higher level of sexual maturity, which might lead to less sensitive of sexual development to nutrition). Overall, high energy promoted the development of sexual organs of yellow-feathered breeder hens, and the possible mechanism was higher energy advanced activation of the hypothalamo–pituitary–gonadal axis and stimulated reproductive gonadotropin levels [8].
Research showed that diets with lower lysine had detrimental nutritional consequences resulting from imbalanced dietary AAs and impaired growth of the reproductive organs, the relative weight of fallopian tube and ovary were lower in Ross 308 parent stock hens given 0.59% lysine compared to hens with higher lysine (0.63% to 0.79%) [4]. However, the highest lysine level (0.79%) used in this research was close to the calculated lysine requirement based on linear- and quadratic-plateau models (0.71% to 0.77%), so it was unable to know whether there were adverse effects of excessive lysine on reproductive performance. In the current manuscript, dietary lysine significantly affected the relative weight of ovarian stroma, and numbers of LYF in a quadratic manner, suggesting that excessive or insufficient lysine had adverse effects on reproductive traits of breeder hens. Tian et al. [24] showed that excessive lysine reduced the expression of lipid metabolism genes (FABP1, ACC, ME, SREBP-1c, and PPARα) in the liver, thus inhibited lipogenesis and eventually led to the reduced abdominal fat deposition in broilers. Lipid synthesis and metabolism are related to energy, which might be the mechanism by which excessive lysine affected reproductive traits of breeder hens. In the current research, interactions existed between dietary lysine and AMEn for the reproductive traits, and the optimal lysine level was higher (0.92%) when birds were given lower energy than those given higher energy (0.76%).
Effect and interaction of dietary lysine and AMEn on egg quality and their concentrations of amino acids
Dietary lysine had both linear and quadratic effects on eggshell thickness and strength of eggs from breeder hens. Similarly, eggshell strength increased with increases in the dietary lysine for laying hens [25], consistent with other earlier results [26, 27]. The shell matrix containing 70% protein [25], might be affected by protein synthesis and optimal AA composition. For yellow-feathered breeder hens, the optimal level of dietary lysine for eggshell quality was estimated as being 0.71% to 0.72%.
In the current study, high AMEn positively influenced yolk color. The same result was shown in the research of Han et al. [28] in laying hens, likely associated with inclusion of specific feed ingredients for producing different dietary AMEn concentrations. The color of egg yolk directly reflects concentrations of carotenoids in diet that are contained at high amounts in corn or corn-derived ingredients [28,29,30]. In the current experiment, more corn was used to produce the high-AME diet. Granghelli et al. [4] showed that increasing dietary ME levels increased the eggshell thickness, and Han et al. [28] suggested that normal-energy diet increased eggshell thickness compared with low-energy diet. Interestingly, the current research showed different results. Eggshell biomineralization was regulated by calcium homeostasis in hens, in turn affected by vitamin D metabolites [31] and human researches indicated that the vitamin D deficiency was associated with obesity [32, 33]. Thus, the decline in eggshell thickness might be the consequence of vitamin D decline, which was related to the more energy intake. More researches are needed to explore the specific mechanism how energy regulates the eggshell.
The nutritional needs for embryonic development of birds are obtained from predetermined nutrients in the eggs [34], but there have been only few studies on the deposition of AAs in the egg yolk from breeder hens. Dietary lysine quadratically increased the concentrations of proline, probably because higher proline was associated to increased protein synthesis [35], and the reduced concentration of proline caused by the lysine-restricted diet might suggest reduced protein anabolism [36]. High dietary AMEn decreased the concentrations of all AAs in eggs, which might be related with the reduced total protein. This finding might be the consequence of the increased fat in egg caused by high dietary AMEn, as more energy would be used for fat deposition of breeder hens [21], and maternal fat might affect the deposition of fat in eggs.
Effect and interaction of dietary lysine and AMEn on hatching performance of eggs and growth performance of offspring
There is increasing awareness of the importance of maternal diet to offspring health [37]. During the formation of eggs, maternal nutrients are deposited in the eggs and subsequently used by the embryo [38]. There is hence an important connection between maternal nutrition and the growth, development, and normal metabolism of embryos and offspring chickens [13, 39]. In the current study, dietary AMEn had a significant effect on hatchability of the fertilized eggs. Similarly, Enting et al. [40] also found breeder hens that received more energy showed higher hatchability of their fertilized eggs. Firman et al. [41] also found that providing with creatine (a naturally occurring energy source) in ovo also increased the hatchability of eggs, with potentially higher energy reserved available for embryonic growth and hatching.
Maternal dietary lysine level or AMEn and their interactions did not affect any variables related to growth performance of offspring broilers, concurred with previous work that did not find any influence of maternal diet on feed conversion ratio of the offspring [37], that might because numerous environmental and nutritional factors such as egg storage, hatching conditions, rearing conditions, feed quality, and pathogen exposure might additively or synergistically mask the effect of maternal nutrition on the broiler [37].
Effect and interaction of dietary lysine and AMEn on biochemical variables of yellow-feathered breeder hens
In the present study, dietary lysine increased the activities of T-AOC in plasma and T-SOD in ovarian stroma. Previous studies showed the influence of lysine on strengthening antioxidant capacity in animals, as it markedly improved the activities of antioxidant enzymes such as catalase and glutathione peroxidase in serum and renal tissue of rats [42] and intestine of grass carp [43] via activating the target of rapamycin (TOR) signaling pathway, and suppressing the p38 mitogen-activated protein kinase (p38-MAPK) signaling pathway [43]. The current research also suggested that low lysine increased the TP and ALB in plasma of breeder hens, which probably resulted from lysine restriction leading to altered protein metabolism, mainly increased catabolism [2, 36].
High AMEn decreased the plasmal concentration of MDA and ovarian stroma and increased the activities of AKP and T-AOC. The decline in antioxidant capacity might be related to the weight gain of breeder hens, because diets with high energy caused increased weight of liver and abdominal fat [21, 22] as already discussed. Moreover, high AMEn led to the enhancement of FSH secretion of breeder hens, an important regulator of ovarian function, especially in the recruitment of follicles [44]. Research on mammals showed that the expression level of FSHR (follicle stimulating hormone receptor) in sheep with high energy was higher than those with low energy [45]. Higher energy advances the activation of the hypothalamo–pituitary–gonadal axis, stimulated reproductive gonadotropin levels, and upregulated the expression of their receptor genes.
Conclusion
Dietary lysine had significant influences on productive performance, reproductive traits, and egg quality of yellow-feathered breeder hens. Based on laying rate, average daily egg mass, and feed intake/egg mass, the optimal levels of dietary lysine, estimated from the quadratic regressions, were 0.81% to 0.83%, which were higher than the requirement for white-feathered breeder hens, and also higher than the recommendation of Nutrient Requirements of Yellow Chickens. Levels of 0.71% to 72% was enough obtain the best quality of breeding eggs. In this experiment, compared with low AMEn (11.10Â MJ/kg), high AMEn (11.50Â MJ/kg) was more beneficial to breeder hens for reproductive traits and hatchability of the fertilized eggs, while it showed detrimental effects on antioxidant capacity of hens and eggshell thickness and AA concentrations of breeding eggs. Furthermore, interactions existed between dietary lysine and AMEn for reproductive traits and egg quality, indicating that lysine requirements should be conducted for different levels of AMEn.
Data availability
All data generated or analyzed during this study are available from the corresponding author on request.
Abbreviations
- AA:
-
Amino acid
- AKP:
-
Alkaline phosphatase
- ALB:
-
Albumin
- AMEn:
-
Apparent nitrogen-corrected metabolizable energy
- BW:
-
Body weight
- FSH:
-
Follicle stimulating hormone
- GOT:
-
Glutamic oxaloacetic transaminase
- GPT:
-
Glutamic pyruvic transaminase
- LYF:
-
The large yellow follicles (> 8 mm)
- MDA:
-
Malondialdehyde
- SYF:
-
Small yellow follicles (3−8 mm)
- T-AOC:
-
Total antioxidant capacity
- TP:
-
Total protein
- T-SOD:
-
Total superoxidase dismutase
- UA:
-
Concentration of uric acid
References
El-Bahr SM, Shousha S, Alfattah MA, Al-Sultan S, Khattab W, Sabeq II, et al. Enrichment of broiler chickens’ meat with dietary linseed oil and lysine mixtures: influence on nutritional value, carcass characteristics and oxidative stress biomarkers. Foods. 2021;10(3):618. https://doiorg.publicaciones.saludcastillayleon.es/10.3390/foods10030618.
Watanabe G, Kobayashi H, Shibata M, Kubota M, Kadowaki M, Fujimura S. Reduction in dietary lysine increases muscle free amino acids through changes in protein metabolism in chickens. Poult Sci. 2020;99(6):3102–10. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/j.psj.2019.11.025.
Leclercq B. Lysine: specific effects of lysine on broiler production: comparison with threonine and valine. Poult Sci. 1998;77(1):118–23. https://doiorg.publicaciones.saludcastillayleon.es/10.1093/ps/77.1.118.
Granghelli CA, Burbarelli M, Lelis KD, Pelissari PH, Utimi N, Leite B, et al. Effects of dietary metabolizable energy levels and beak trimming on the performance, egg quality, and economic viability of layers. Poult Sci. 2019;98(11):5831–9. https://doiorg.publicaciones.saludcastillayleon.es/10.3382/ps/pez145.
Kim E, Wickramasuriya SS, Shin TK, Cho HM, Kim HB, Heo JM. Estimating total lysine requirement for optimised egg production of broiler breeder hens during the early-laying period. J Anim Sci Technol. 2020;62(4):521–32. https://doiorg.publicaciones.saludcastillayleon.es/10.5187/jast.2020.62.4.521.
Onimisi PA, Orunmuyi M, Musa AA, Bale S, Bawa GS. Effects of feed lysine content on laying performance and egg quality of late laying hens. Int J Res Appl Technol. 2012;1(5):104–10.
Lu J, Li YF, Qu L, Ma M, Yang XD, Shen MM, et al. Effects of energy-restricted feeding during rearing on sexual maturation and reproductive performance of rugao layer breeders. Poult Sci. 2021;100(8):101225. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/j.psj.2021.101225.
Hadinia SH, Carneiro P, Fitzsimmons CJ, Bedecarrats GY, Zuidhof MJ. Post-photostimulation energy intake accelerated pubertal development in broiler breeder pullets. Poult Sci. 2020;99(4):2215–29. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/j.psj.2019.11.065.
Wang Y, Wang W, Li L, Gou Z, Lin X, Jiang S. Effects and interaction of dietary calcium and nonphytate phosphorus for slow-growing yellow-feathered broilers between 56 and 84 d of age. Poult Sci. 2021;100(5):101024. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/j.psj.2021.101024.
Wang YB, Wang WW, Fan QL, Ye JL, Zhang S, Jiang SQ. Effects and interaction of dietary calcium and non-phytate phosphorus for slow-growing yellow-feathered broilers during the starter phase. Animal. 2021;15(5):100201. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/j.animal.2021.100201.
Ministry of Agriculture and Rural Affairs of the People's Republic of China. Nutrient requirements of yellow chicken: NY/T3645-2020. Beijing: China Agricultural Press; 2020.
Chen F, Jiang Z, Jiang S, Li L, Lin X, Gou Z, et al. Dietary vitamin A supplementation improved reproductive performance by regulating ovarian expression of hormone receptors, caspase-3 and Fas in broiler breeders. Poult Sci. 2016;95(1):30–40. https://doiorg.publicaciones.saludcastillayleon.es/10.3382/ps/pev305.
Wang Y, Li L, Gou Z, Chen F, Fan Q, Lin X, et al. Effects of maternal and dietary vitamin A on growth performance, meat quality, antioxidant status, and immune function of offspring broilers. Poult Sci. 2020;99(8):3930–40. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/j.psj.2020.03.044.
AOAC International. International Association of Official Analytical Chemists. Official methods of analysis. In: Chemists. Gaithersburg:Â AOAC International; 2007.
National Feed Industry Standardization Technical Committee of the People's Republic of China. Determination of animo acids in feed: GB/T 18246–2019. Beijing: China Agricultural Press; 2019.
Świerk S, Przybyło M, Flaga J, Szczepanik K, Garus-Piętak A, Biernat W, et al. Effect of increased intake of concentrates and sodium butyrate supplementation on ruminal epithelium structure and function in growing rams. Animal. 2023;17(11):100898. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/j.animal.2023.100898.
Khwatenge CN, Kimathi BM, Nahashon SN. Transcriptome analysis and expression of selected cationic amino acid transporters in the liver of broiler chicken fed diets with varying concentrations of lysine. Int J Mol Sci. 2020;21(16):594. https://doiorg.publicaciones.saludcastillayleon.es/10.3390/ijms21165594.
Ruan D, Fouad AM, Zhang YN, Wang S, Chen W, Xia WG, et al. Effects of dietary lysine on productivity, reproductive performance, protein and lipid metabolism-related gene expression in laying duck breeders. Poult Sci. 2019;98(11):5734–45. https://doiorg.publicaciones.saludcastillayleon.es/10.3382/ps/pez361.
Joseph NS, Robinson FE, Korver DR, Renema RA. Effect of dietary protein intake during the pullet-to-breeder transition period on early egg weight and production in broiler breeders. Poult Sci. 2000;79(12):1790–6. https://doiorg.publicaciones.saludcastillayleon.es/10.1093/ps/79.12.1790.
Mohiti-Asli M, Shivazad M, Zaghari M, Rezaian M, Aminzadeh S, Mateos GG. Effects of feeding regimen, fiber inclusion, and crude protein content of the diet on performance and egg quality and hatchability of eggs of broiler breeder hens. Poult Sci. 2012;91(12):3097–106. https://doiorg.publicaciones.saludcastillayleon.es/10.3382/ps.2012-02282.
Scappaticcio R, Garcia J, Fondevila G, de Juan AF, Camara L, Mateos GG. Influence of the energy and digestible lysine contents of the diet on performance and egg quality traits of brown-egg laying hens from 19 to 59 weeks of age. Poult Sci. 2021;100(7):101211. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/j.psj.2021.101211.
Chen X, Yu T, Dou Y, Ji Q, Guo L, Geng Z. High dietary energy decreased reproductive performance through increasing lipid deposition in Yangzhou geese at late laying stage. Poult Sci. 2023;102(10):102915. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/j.psj.2023.102915.
Bruggeman V, Onagbesan O, D’Hondt E, Buys N, Safi M, Vanmontfort D, et al. Effects of timing and duration of feed restriction during rearing on reproductive characteristics in broiler breeder females. Poult Sci. 1999;78(10):1424–34. https://doiorg.publicaciones.saludcastillayleon.es/10.1093/ps/78.10.1424.
Tian DL, Guo RJ, Li YM, Chen PP, Zi BB, Wang JJ, et al. Effects of lysine deficiency or excess on growth and the expression of lipid metabolism genes in slow-growing broilers. Poult Sci. 2019;98(7):2927–32. https://doiorg.publicaciones.saludcastillayleon.es/10.3382/ps/pez041.
Scappaticcio R, Camara L, Herrera J, Mateos GG, de Juan AF, Fondevila G. Influence of the energy concentration and the standardized ileal digestible lysine content of the diet on performance and egg quality of brown-egg laying hens from 18 to 41 weeks of age. Poult Sci. 2022;101(12):102197. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/j.psj.2022.102197.
Keshavarz K, Nakajima S. The effect of dietary manipulations of energy, protein, and fat during the growing and laying periods on early egg weight and egg components. Poult Sci. 1995;74(1):50–61. https://doiorg.publicaciones.saludcastillayleon.es/10.3382/ps.0740050.
Leeson S, Caston LJ. A problem with characteristics of the thin albumen in laying hens. Poult Sci. 1997;76(10):1332–6. https://doiorg.publicaciones.saludcastillayleon.es/10.1093/ps/76.10.1332.
Han GP, Kim DY, Kim KH, Kim JH, Kil DY. Effect of dietary concentrations of metabolizable energy and neutral detergent fiber on productive performance, egg quality, fatty liver incidence, and hepatic fatty acid metabolism in aged laying hens. Poult Sci. 2023;102(4):102497. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/j.psj.2023.102497.
Grashorn M. Feed additives for influencing chicken meat and egg yolk color. In: Carle R, Schweigert RM, editors. Handbook on natural pigments in food and beverages. Sawston: Woodhead Publishing; 2016. p. 283–302.
Shin HS, Kim JW, Lee DG, Lee S, Kil DY. Bioavailability of lutein in corn distillers dried grains with solubles relative to lutein in corn gluten meal based on lutein retention in egg yolk. J Sci Food Agric. 2016;96(10):3401–6. https://doiorg.publicaciones.saludcastillayleon.es/10.1002/jsfa.7520.
Zhang Y, Deng Y, Jin Y, Wang S, Huang X, Li K, et al. Age-related changes in eggshell physical properties, ultrastructure, calcium metabolism-related serum indices, and gene expression in eggshell gland during eggshell formation in commercial laying ducks. Poult Sci. 2022;101(2):101573. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/j.psj.2021.101573.
Fiamenghi VI, Mello ED. Vitamin D deficiency in children and adolescents with obesity: a meta-analysis. J Pediatr (Rio J). 2021;97(3):273–9. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/j.jped.2020.08.006.
Pereira-Santos M, Costa PR, Assis AM, Santos CA, Santos DB. Obesity and vitamin D deficiency: a systematic review and meta-analysis. Obes Rev. 2015;16(4):341–9. https://doiorg.publicaciones.saludcastillayleon.es/10.1111/obr.12239.
Santos JS, Araujo I, Martins PC, Royer A, Cafe MB, Andrade MA, et al. The transfer of amino acids and minerals to the egg yolk and to the yolk sac of their progeny is affected by breeder age. J Anim Physiol Anim Nutr (Berl). 2022;106(1):139–46. https://doiorg.publicaciones.saludcastillayleon.es/10.1111/jpn.13569.
Wu G, Bazer FW, Burghardt RC, Johnson GA, Kim SW, Knabe DA, et al. Proline and hydroxyproline metabolism: implications for animal and human nutrition. Amino Acids. 2011;40(4):1053–63. https://doiorg.publicaciones.saludcastillayleon.es/10.1007/s00726-010-0715-z.
Soglia F, Zampiga M, Baldi G, Malila Y, Thanatsang KV, Srimarut Y, et al. Lysine depletion during different feeding phases: effects on growth performances and meat quality of broiler chickens. Animals (Basel). 2021;11(6):1499. https://doiorg.publicaciones.saludcastillayleon.es/10.3390/ani11061499.
Moraes T, Pishnamazi A, Wenger II, Renema RA, Zuidhof MJ. Energy and protein dilution in broiler breeder pullet diets reduced offspring body weight and yield. Poult Sci. 2019;98(6):2555–61. https://doiorg.publicaciones.saludcastillayleon.es/10.3382/ps/pey603.
Yuan J, Roshdy AR, Guo Y, Wang Y, Guo S. Effect of dietary vitamin A on reproductive performance and immune response of broiler breeders. PLoS One. 2014;9(8):e105677. https://doiorg.publicaciones.saludcastillayleon.es/10.1371/journal.pone.0105677.
Wu H, Sun H, Ma C, Lian L, Lu L, Xu L, et al. Effects of maternal dietary energy restriction on breast muscle fibre development in the offspring of broiler breeders. Anim Biosci. 2021;34(11):1829–38. https://doiorg.publicaciones.saludcastillayleon.es/10.5713/ab.20.0712.
Enting H, Kruip TA, Verstegen MW, van der Aar PJ. The effect of low-density diets on broiler breeder performance during the laying period and on embryonic development of their offspring. Poult Sci. 2007;86(5):850–6. https://doiorg.publicaciones.saludcastillayleon.es/10.1093/ps/86.5.850.
Firman CB, Inhuber V, Cadogan DJ, Van Wettere WHEJ, Forder REA. Effect of in ovo creatine monohydrate on hatchability, post-hatch performance, breast muscle yield and fiber size in chicks from young breeder flocks. Poult Sci. 2023;102(3):102447. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/j.psj.2022.102447.
Jozi F, Kheiripour N, Taheri MA, Ardjmand A, Ghavipanjeh G, Nasehi Z, et al. L-lysine ameliorates diabetic nephropathy in rats with streptozotocin-induced diabetes mellitus. Biomed Res Int. 2022;2022:4547312. https://doiorg.publicaciones.saludcastillayleon.es/10.1155/2022/4547312.
Huang D, Maulu S, Ren M, Liang H, Ge X, Ji K, et al. Dietary lysine levels improved antioxidant capacity and immunity via the TOR and p38 MAPK signaling pathways in grass carp, Ctenopharyngodon idellus Fry. Front Immunol. 2021;12:635015. https://doiorg.publicaciones.saludcastillayleon.es/10.3389/fimmu.2021.635015.
Visser JA, Themmen A. Role of anti-mullerian hormone and bone morphogenetic proteins in the regulation of FSH sensitivity. Mol Cell Endocrinol. 2014;382(1):460–5. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/j.mce.2013.08.012.
Liu B, Li H, Tao W, Huang F, Rui X, Wang J, et al. Effects of different energy diets on DNA methylation and mRNA expression in follicle stimulating hormone receptor gene promoter region of Duolang sheep during estrus. Mol Biol Rep. 2022;49(4):2565–77. https://doiorg.publicaciones.saludcastillayleon.es/10.1007/s11033-021-07058-6.
Acknowledgements
W. Bruce Currie (Emeritus Professor, Cornell University) made suggestions on presentation.
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This work was financially supported by China Agriculture Research System of MOF and MARA (CARS-41), the National Key R&D Project (2021YFD1300404), the Natural Science Foundation from Guangdong Province (2022A1515012069), the Science and Technology Plan Project of Guangzhou (SL2022A04J00940, 2024E04J0562), the Science and Technology Program of Guangdong Academy of Agricultural Sciences (R2023PY-QY012, R2021YJ-YB3012), P. R. China.
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YBW and SQJ designed the experiments. YBW performed animal husbandry. YBW, QW, XTY, QLL, ZYG and XJL performed the animal experiment and analyzed the data. SQJ and YBW provided the resources and financial support. YBW wrote the final article. SQJ and YBW reviewed and edited the article. All authors read and approved the final manuscript.
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Experimental procedures were approved by the Institutional Animal Care and Use Committee, Guangdong Academy of Agricultural Sciences in China (GAASISA-2018-031).
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Wang, Y., Wang, Q., Yao, X. et al. Effects and interactions of dietary lysine and apparent nitrogen corrected metabolizable energy on yellow-feathered broiler breeder hens. J Animal Sci Biotechnol 15, 143 (2024). https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s40104-024-01095-4
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DOI: https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s40104-024-01095-4