1. Introduction
Whole grain (WG) inclusion has gained prominence as a feeding strategy, especially in free-range farming for organic poultry production [
1]. Evidence has indicate that WG feeding could decrease the incidence of coccidiosis and
Salmonella enteritidis infection [
2,
3], improve the gut microflora ecology [
4,
5], increase the relative gizzard weight, and promote the apparent metabolizable energy and starch digestibility [
6,
7]. In addition, further reduction of cost can be achieved due to the simplified handling and processing steps [
8]. Free-choice feeding (FCF) is one WG feeding strategy [
9]. Since individual birds could have different nutrient requirements for maintenance and production, the ability to self-select feeds to reach their own nutrient targets may not be realized when only one formulated diet is given [
1].
In Asian countries, raising pigeons for meat has gained popularity in recent years. However, pigeon squabs are reared by their parents for nearly 28 d from hatching, and the whole breeding cycle of pigeon often lasts 2 months, which includes nonbreeding, laying, hatching, and feeding period [
10]. The problem is that birds in the same flock are probably in different breeding periods and should have distinct dietary requirements in response to each period. However, a diet formulated to meet all requirements of an average bird during the whole breeding cycle will contain either excessive or inadequate levels of nutrients for individual pigeons above or below the mean. Therefore, FCF system of WG feeding is widely used in the meat-type pigeon production of China, which has been proven to enhance growth performance [
11].
Pigeon meat consumption has become popular in more and more countries [
12]. Compared with broilers, the muscle of meat-type pigeons is mainly in the breast, and the proportion of thigh is relative lower [
11]. The high concentration of protein and the much lower cholesterol found in pigeon muscle make it an ideal candidate for human food resource [
13]. Meat quality of animals can be affected by the breed, nutritional level, and feeding management. Positive effects of whole grain feeding on the meat quality in poultry have been reported, which includes improvement of the meat color [
14], decreasing the lipid deposition [
15], and increasing of trace elements’ content [
16]. Commercial organic poultry meat produced by WG feeding is attractive and more expensive for customers in the Chinese market. People also thought that this feeding mode can change the meat flavor because of the improved animal welfare, but the relative knowledge was highly limited. Therefore, the experiment was designed to test the influence of five different feeding strategies (four free-choice feeding systems and one compound feeding system) on meat quality and intestinal development of 28-day-old pigeon squabs.
3. Results
Whole grain feeding can be well accepted by the birds (
Table 3).
Table 4 showed the influence of five different feeding strategies on meat quality of pigeon breast muscle at 28 days-of-age. The values of pH, L*, water-holding capacity, and shear force were not influenced by feeding strategies (
p > 0.05). a* and b* values in T4 were highest among the five treatments (
p = 0.038;
p < 0.001).
As shown in
Table 5, no effects of different feeding strategies on the contents of moisture, CP, and ash in pigeon meat were found (
p > 0.05). The content of CF in breast muscle in T2 was higher than that in T5 (
p = 0.032).
There was no significant difference in the activity of GSH-Px among different feeding groups (
p = 0.262) (
Table 6). The T-SOD activity of pigeon breast meat in T2 and T4 was higher than that in T5 (
p = 0.046), and CAT activity in the T5 group was also the lowest (
p = 0.025). MDA content in pigeon breast meat of T5 tended to increase, but it was not significant (
p = 0.058).
As shown in
Table 7, higher values of the nonessential amino acids, glycine (1.09%), and tyrosine (0.84%), and the essential amino acids, lysine (1.97%), threonine (1.10%), valine (1.09%), histidine (0.67%), and arginine (1.54%) were observed in T1 (
p < 0.05). The contents of glutamic acid (3.26%), glycine (1.16%), alanine (1.49%), and aspartic acid (2.07%) were also higher in T2. The proline (0.41%) content of pigeon breast meat was higher in T3 (
p = 0.035). However, complete pelleted feeding resulted in lower levels of the majority of essential amino acids in pigeon breast muscle.
Organ index of pigeon duodenum, jejunum, and ileum showed no changes under different feeding strategies (
p > 0.05) (
Table 8). However, different feeding systems have significant effects on intestinal histomorphology in 28-day-old squabs (
p < 0.05) (
Table 9). Villus height and surface area of duodenum and jejunum in T2 group were the highest among the treatments and squabs in the group while T5 received complete pelleted diet and had the lowest villus height (
p < 0.05). Surface area of pigeon jejunum in T1 was lower than other groups (
p < 0.05). Crypt depth of three intestinal segments had no changes under the different feeding strategies (
p > 0.05).
As shown in
Table 10, AKP activity in duodenum and jejunum was the highest in 28-day-old squabs reared by parental pigeons fed corn, wheat, and pelleted feed, and it decreased significantly in the pigeon group fed complete pelleted feed (
p < 0.05). Different feeding strategies showed no significant effects on activity of MLA and LAP in three intestinal segments (
p > 0.05).
4. Discussion
A theory was put forth that the nutrient requirement can be achieved by self-selection of the birds themselves [
1]. Only one completed study may not satisfy every specific nutrient requirement of breeding pigeons during different physiological period [
11]. Food preference (corn > pea, wheat) of pigeons was reported by Sales and Janssen [
24]. Therefore, choice feeding based on unground corn and high-protein pellets gained popularity for a long time. Until now, both WG feeding and complete feeding are applied in pigeon production, but different combinations of corn, pea, wheat, and pelleted feed in the WG feeding strategy were used by different producers. Our previous study found that choice feeding of corn, wheat, and pelleted feed can enhance the growth performance of pigeons and was thought to be commercially available [
11]. However, the acceptance of a type of whole grain by birds is mainly attributed to its shape, color, size, and nutrients concentration or, probably, the involvement of all these factors [
5]. In the present study, wheat in WG feeding groups seemed to be well-received due to its higher relative intake. Smaller size and convenience for pecking may be the major reason, while corn and pea are large seeds and are not easy to ingest by poultry [
25].
Animal meat quality was closely related to the feed ingredients [
26]. Bright flesh color can stimulate customers’ desire to buy. The values of redness and yellowness in T4 were higher than that in other treatments in our study, and more relative intake of corn ingested by pigeons in T4 may be an important reason. Since corn was found to be a major contributor of dietary natural pigments (zeaxanthin and lutein) [
27], the redness of meat is closely related to the oxymyoglobin content [
28]. Supplementation of the protein-xanthophylls concentrate of alfalfa made the muscle redder and of a higher oxymyoglobin content [
29]. Lutein-supplemented chickens also had greater yellowness in breast meat [
30]. Introducing only wheat grain in the diet of fattening turkeys gained the opposition results [
31] which can be attributed to the lower intake of natural pigments.
Vandeputte-Poma [
32] reported that the content of grains in crop milk increased steadily after 12 days of age. The inclusion of WG in poultry diet was shown to improve the nutrient uptake and utilization [
8,
33]. Whole grains in crop milk brought by parent pigeons probably affected the energy utilization of squabs, but different combinations of whole grains (corn, pea, and wheat) may have different feeding effects, which could be attributed to the size or nutritive value of grains. Ye et al. [
34] reported that the shear force of breast meat was correlated with intramuscular fat in pigeon squabs, which is similar to that in mammals [
35]. However, there was no significant difference in shear force among the five treatments.
Lipid-derived free radicals can damage the structure of cells through oxidation due to their highly unstable characteristics [
36]. Lipids oxidation in meat can lead to a decrease in nutritional and sensory value [
37]. Therefore, the antioxidant status, which can be reflected by the activities of antioxidant enzymes (GSH-Px, CAT, and SOD) and the concentration of the end product of lipid oxidation (MDA), is closely linked to meat quality [
38]. Previous studies found that free radicals produced by lipid oxidation of meat can get into the cytoplasm, and the reaction with oxymyoglobin and metmyoglobin accumulation can be accelerated, which in turn decreases the value of a* and causes meat discoloration [
39,
40,
41]. These findings can explain the relatively lower value of redness and yellowness of breast meat in T5. Lutein and zeaxanthin in corn are important antioxidant carotenoids [
42]. The inclusion of whole grain of corn in the treatments, especially in T4, can bring more content of carotenoids, which can decrease oxidative damage in poultry [
30,
43].
Amino acids are important sources of aroma flavor, which are involved in the Maillard reaction and Strecker degradation [
44]. Different amino acids elicit different tastes; for example, phenylalanine, histidine, tyrosine, methionine, valine, and arginine are bitter in taste, whereas glutamic acid is sour and umami in taste, and proline elicits both sweet and bitter tastes [
45]. Glutamic acid, alanine, glycine, and arginine are also important precursors of meat flavor volatiles [
46]. It was reported that duck muscle under the whole wheat feeding system contained more glutamic acid, alanine, and arginine [
47], especially glutamic acid, which may be due to its higher content in dietary wheat compared to that in corn. Digestibility of ileal protein and concentrations of alanine, asparagine, and cysteine in systemic plasma can be effectively increased by WG feeding [
48,
49]. The whole grains appeared in crop milk probably affected amino acid deposition in squabs’ breast meat. In the present study, both essential amino acids (lysine, threonine, valine, histidine, and arginine) and nonessential amino acids (glutamic acid, glycine, alanine, and tyrosine) measured in breast muscle in T1 were higher than in T5, possibly indicating the greater nutritive value in meat. However, different grain types or combinations in diets may exert different effects on the same animal species, and further research is warranted.
Other than the hyperplasia of the gizzard organ, relative weight of intestinal segments in birds fed a diet with whole grains inclusion commonly shows no changes in most studies [
2,
33,
50]. This is consistent with our present study results. Although the research investigating the effect of WG feeding on animal gastrointestinal morphology were limited, controversial results were reported. Gabriel et al. [
51] found that villus surface area and the length of villus to crypt increased significantly in the duodenum of whole wheat-fed broilers at 23 days of age. Meanwhile, no influence of whole grain feeding on intestinal morphology was also reported [
33]. Generally, the longer and larger intestinal villi are beneficial for the digestion and absorption of nutrients [
52]. The form and composition of diet would change from the upper part to the lower part of the intestine. The morphology of the upper small intestine was expected to improve when poultry was fed a diet with whole grains inclusion [
53]. The present study found that the choice feeding of corn, wheat, and pelleted feed increased villus length and surface area of the upper small intestine in squabs compared with that in the complete pelleted feed group, which showed small intestines structurally more oriented to digestion. Interestingly, not all whole grains feeding treatments showed such a positive effect. Previous studies reported that histological changes are more likely to be induced by the content and physicochemical properties of dietary fiber other than the protein intake [
54,
55,
56]. Therefore, different combinations of whole grains may bring a different intake of dietary fiber, which in turn affected the pigeon intestinal morphology.
Studies investigating the effect of whole grain feeding on digestive enzyme activity were also scarce. AKP is considered to be a marker for enterocyte maturity, which can account for the migration of epithelial cells, and finally affecting animal villus morphology [
57]. In pigeon duodenum and jejunum and the higher villus height of WG feeding treatment was associated with a higher AKP activity in the present study, which further confirmed the above viewpoint. MLS and LAP are responsible for nutrient digestion [
58], and they were also thought to be enterocyte maturation marker for digestive function in growing pigeons [
59]. However, activities of these two enzymes in our study showed no changes under the different feeding strategies. It indicated that choice feeding of whole grains probably had little effect on intestinal digestive function.