Abstract
The photoperiod is an important factor during rearing and laying period that affects age and body weight at sexual maturation and reproductive performance in poultry; however relevant research on this factor in pigeons is still lacking. Thus, this study investigated the effects of different photoperiodic programs on the reproductive performance and hormonal profile in White King pigeons. From 101 d of age, the pigeons in the control group were exposed to a natural photoperiod until 160 d, and then to a photoperiod of 16 h (16 light [L]: 8 dark [D]) and lasted for 200 d. Pigeons in the 3 experimental groups were exposed to a short photoperiod of 8L: 16D until 160 d, and then to 14L: 10D, 16L: 8D, and 18L: 6D, respectively. The results showed that light-restriction (8L: 16D) during the rearing period and then 14L: 10D or 16L: 8D photostimulation delayed the age at first egg laying in pigeons. However, 16L: 8D after an 8L: 16D photoperiod during the breeding period ensured maximum photosensitivity, and significantly improved the reproductive performance (egg production and fertility rates) in pigeons. Moreover, the highest reproductive performance in group under16L: 8D after 8L: 16D photoperiodic program was accompanied by improved follicle-stimulating hormone and estradiol levels and reduced prolactin hormone levels. The results indicated that photoperiodic programs from rearing to laying period are closely related to the reproductive performance of White King pigeons. The results provide information that 8L: 16D during rearing period and 16L: 8D during laying period can be used to enhance reproductive performance in the pigeon industry.
Key words: pigeon, photoperiod, egg production, steroid hormone, sexual maturity
INTRODUCTION
The domestic pigeon (Columba livia) is one of the earliest domesticated birds. It has important economic, ornamental, and racing value, and is used for its squabs. Due to its low-cholesterol, high-protein meat source with a unique flavor and aroma, pigeon meat is a high-quality nutritional food (Pomianowski et al., 2009). Currently, domestic pigeons are the fourth common poultry species in China after chickens, ducks, and geese. In addition, the stock of breeding pigeons and sales of squabs in China are the highest in the world. Pigeons currently account for less than 1% of the global poultry population and production of squab is increasing. However, the increasing squab's production is mainly due to the expansion of the breeding scale of breeding pigeons rather than the improvement of production efficiency.
Due to their inherent reproductive characteristics of “monogamous” system, natural mating, and parental feeding, pigeons have an average clutch interval of approximately 47.44 d (Khargharia et al., 2003), with paired pigeons only laying 2 eggs in a laying period. Compared to hens laying eggs almost every day, this low reproductive performance is a bottleneck that restricts the development of the pigeon industry.
Poultry are very sensitive to light and light systems directly or indirectly affect production, health status, behavior, and reproductive performance (Lewis and Morris, 2000). As a breeding animal that requires prolonged exposure to light, natural light cannot fully meet the needs of pigeons for growth and reproduction. However, research on lighting systems during the production process of meat pigeons in-sufficiently. Light has several main characteristics: photoperiod (duration and distribution over 24 h), intensity, wavelength and light color. Appropriate light intensity has a positive effect on egg production and the number of squabs raised (Cooper, 1976). Different light colors also affect the reproductive performance of White King pigeons (Wang et al., 2015).
To date, efficient and complete artificial lighting systems have not been widely adopted in the pigeon breeding industry. Thus, the pigeon breeding industry often relies on the acquired knowledge of other poultry, limiting its efficient development. In addition, the sexual maturation and productivity of pigeons can be modulated by photoperiods during the rearing period (61–180d) or pre-lay period (puberty-sexual maturation); however, there have been no studies on the application of artificial light during this period in pigeons. Therefore, this study aimed to evaluate the effects of a 3-phase photoperiodic programs during the rearing and laying periods on reproductive parameters, and plasma hormone levels in laying pigeons.
MATERIALS AND METHODS
All procedures used in this study were approved by the Research Committee of Jiangsu Academy of Agricultural Sciences (IACUC number: NKYVET 2014-63). All methods and management procedures were complied with the Regulations for the Administration of Affairs Concerning Experimental Animals, approved by the State Council of the People's Republic of China.
Animals, Diets, and Housing
The experiment was carried out at Nanjing city (118° 61′ E, 31° 87′ N), Jiangsu Province, starting on the August 26, 2021. A total of 400 young White King pigeons aged 60 d with similar body weights (510.5 ± 0.39 g) were bred in a commercial pigeon farm (Jiangsu Cuigu Pigeon Industry Co., Ltd., Nanjing, China). Subsequently, all pigeons were subjected to either a 2-phase (natural-long photoperiod) or 3-phase (natural-short-long) photoperiodic program. The detailed procedure is as follows, from 61 to 100 d of age, the pigeons received natural light, and the duration of the photoperiod was 13.8 to 12.5 h, calculated using data from Nanjing Meteorological Bureau, Nanjing City, China. To avoid premature pairing of young pigeons, they were raised separately according to gender in 2 online flat cages in a same barn, by conducting gender identification of young pigeons and labeling their feet with gender tags. Each flat cage contained 200 male or 200 female pigeons. From 101 d, the pigeons were randomly divided into four groups in 4 barns. Each group have 50 male pigeons and 50 female pigeons bred in 10 big cages (5 cages with male pigeons and 5 cages with female pigeons) in the barn, and every cage contained 10 male or 10 female pigeons. One cage with male pigeons and another cage with female pigeons being treated as 1 replicate, therefore there were 5 replicates per group and 20 squabs per replicate. The control group was continuously exposed to a natural photoperiod until 160 d (duration of the photoperiod was 12.5–11.1 h) and then gradually increased to a photoperiod of 16 h (N-16 light [L]:8 dark [D]). The remaining 3 groups were initially exposed to a short photoperiod of 8 h (8L:16D) for 60 d, which was achieved by covering the windows of the pigeon barns with opaque sheets from 4 to 8: am and from 16 to 20 pm. From 161d, the photoperiods were gradually increased to of 14 h (S-14L:10D), 16 h (S-16L:8D) and 18 h (S-18L: 6D), respectively. The total daily photoperiods in four groups were both supplementary artificial lighting period in conjunction with natural light.
From the age of 161 d, the pigeons in the same replicate attempted to pair off in the pattern of one female and one male. Once paired successfully, each pair of pigeons was kept on the former replicate and housed in a 3-layer, 3-dimensional cage equipped with a perch and nest. Artificial light was provided using LED strips to achieve an illuminating intensity at a bird head height of 10 lx during rearing (From 61 to 160 d) and 15 to 25 lx during the pairing and laying phase (From 161d). The ambient temperature (10–30°C) and humidity in four barns were similar during the more than 1 year experimental periods.
Pigeons were fed a corn- and pea-based grower diet (11.2 MJ/kg and 12.0% CP) from 61 to 160 d. Thereafter, the feed was changed to a diet for breeding pigeons (12.2 MJ/kg and 15.0% CP). Pigeons were fed twice a day (at 7 am and 3 pm); and water was provided ad libitum throughout the study. Each pair of parent pigeons raised 2 squabs, and crop milk secreted by the parent pigeons was used to feed the squabs.
Reproductive Performances
The age at first egg (AFE) in the different groups was recorded. For each group, productive performance was recorded for 200 d after the first egg laid. Data on egg production by paired pigeons, egg weight, and rate of broken eggs were collected daily. Egg weight was measured using an electronic scale with an accuracy of 0.1 g. After laying, eggs were hatched by both male and female breeding pigeons. Fertility rate = (number of fertile eggs at 4 d of hatching/ number of hatching eggs) × 100. Hatchability = (number of newly squabs/number of fertile eggs) × 100.
Determination of Hormone Concentrations
At the end of the 200 d period after the first egg laid in each group and 12 h after feed withdrawal, 2 female pigeons with similar physiological periods (7–10 d after the 2 eggs were laid) were chosen from the 5 replicates of each group. Blood samples were collected from the wing vein into a heparinized syringe and then centrifuged at 1,320 g at 4°C for 10 min to harvest the plasma samples.
The concentrations of steroid hormones were determined using enzyme-linked immunosorbent assay (ELISA) according to t the manufacturer's instructions. The ELISA kits for follicle stimulating hormone (FSH), luteinizing hormone (LH), and estradiol (E2) were purchased from Shanghai Enzyme-Linked Biotechnology Co., Ltd. (Shanghai, China). The prolactin (PRL) hormone content was determined using a sandwich ELISA developed by our lab (Chen et al., 2019). The optical density was measured at 450 nm using an Infinite F50 microplate reader (Tecan Group Ltd., Männedorf, Switzerland) within 15 min.
The intra- and inter-assay coefficients of variation for FSH, LH, and E2 were less than 10% and the intra- and inter-assay coefficients of variation for PRL were less than 12%. Standard curves were used to determine the hormone concentration. The standard ranges were 0 to 8 mIU/mL for FSH, 0 to 160 ng/mL for LH, 0–64 pmol/L for E2, and 0–12.5 ng/mL for PRL.
Statistical Analysis
The results are expressed as arithmetic mean and standard error of mean (Mean ± SEM) of samples in each treatment group. Differences in plasma concentrations of steroid hormones among the 4 photoperiodic programs were analyzed using one-way analysis of variance (ANOVA). Statistical analyses were performed using the IBM SPSS software (ver.17.0; IBM SPSS, Armonk, NY). Differences were considered highly significant at P ≤ 0.05.
RESULTS AND DISCUSSION
The reproductive performance of pigeons exposed to different photoperiodic programs during the rearing and laying periods is shown in Figure 1. The average AFE of the four groups were 175.5, 181.7, 178.8, and 177.7 d, respectively. Pigeons in the short photoperiod followed by 14L:10D (S-14L:10D) or 16L:8D (S-16L:8D groups started laying later than those in the N-16L:8 D group (P < 0.01) (Figure 1A). This indicates that exposure to a short 8L:16D photoperiod during the rearing period inhibited sexual maturity and delayed the AFE. The AFE in the S-14L: 10D group was significantly greater than those in the S-16L:8D and S-18L:6D groups (P < 0.01), indicating that exposure to 14L:10D light before sexual maturity also delayed AFE.
Figure 1.
The reproductive performance of White King pigeons exposed to different photoperiods (A, B, C, D, E and F: AFE, egg production, rate of broken eggs, egg weight, fertility rate and hatchability, respectively). Consecutive letters (eg, a, b) on the bars indicate significant differences (P < 0.05), and discrete letters (eg, a, c) indicate highly significant differences (P < 0.01), the same as below. Abbreviations: AFE, age at first egg; N-16L:8D, a natural photoperiod followed by a photoperiod of 16 h light (L):8 h dark (D); S-14L:10D, S-16L:8D and S-18L: 6D, a short photoperiod of 8 h followed by photoperiods of 14, 16, and 18 h.
Age at first egg in poultry is associated with photostimulation, in which photoperiod, light source, spectra, and intensity have been considered as factors regulating chicken reproductive performance. A study on female broiler breeders observed the greatest advance in mean AFE (200.4–182.0 d) with an increasing photoperiod from 8 to 13 h, with no further advantages (the steeper rises in rate of lay during the initial 20 d of egg production and peak rate of lay) occurring for photostimulation than 13 h (saturation day length) (Lewis et al., 2008). In addition, research on geese reported that changes in the photoperiod during the rearing period alter the AFE (Wang et al., 2002). There was no significant difference in AFE between the S-16L:8D and S-18L:6D groups, suggesting that the 18 h photoperiod is the saturation day length for breeding pigeons. Usually, it is disadvantageous to increase the age at maturity because the initial egg size is too small and the fertilization rate is too low for successful hatching.
Compared to the control N-16L:8D group, egg production in the S-16L:8D group was significantly improved (P < 0.01) and the number of eggs laid by paired pigeons increased from 10.6 to 13.6 (Figure 1B). Although sexual maturity was delayed in pigeons reared on a shorted 8L:16D photoperiod during the rearing period, egg production increased in the pigeons under 18L: 6D photoperiod during the laying period. The natural or 8L:16D photoperiods did not stimulate for sexual maturity of young pigeons and thus the attainment of sexual maturity could be hastened by providing an appropriate lighting stimulus. Furthermore, light restriction during the rearing and pre-lay periods may prevent pigeons from responding photosexually and ensure that they are maximally photosensitive.
The number of broken eggs was higher in the S-18L:6D group than in the other 3 groups (P < 0.01, Figure 1C). The 18L: 6D photoperiod during the laying period may have increased the activity of the pigeons and probability of egg crushing. A longer photoperiod increases calcium intake from feed and provides sufficient time to consume calcium for eggshell formation. However, it is unknown whether exposure to an 18L: 6D photoperiod affected the quality of eggshells. Further studies are needed to explore the optimal photoperiod for breeding pigeons from the perspective of eggshell quality.
Egg weight did not differ among pigeons in the 4 photoperiodic programs (Figure 1D). No effects of different photoperiods during rearing period on the pigeon's egg weight have been previously reported. Different lighting programs also affected the fertility rates of pigeon eggs. The fertility rate of S-16L: 8D and S- 14L:10D groups were significant higher than the other 2 groups (P < 0.05, Figure 1E). There were no significant differences in the hatchability of fertilized eggs among the 4 groups. Our previous study in geese found that increasing the daily photoperiod from 8 h to 11 h results in a significantly higher fertility rate than increasing it to 14 h (Zhu et al., 2019). Therefore, exposure to a short 8 h period during the rearing period and a 16L:8D photoperiod during the laying period enhanced the reproductive performance of pigeons.
The plasma concentrations of FSH, LH, E2, and PRL in the 4 photoperiodic programs are shown in Figure 2. The plasma FSH and E2 levels in the female breeding pigeons of the S-16L:8D group were significantly higher than those in the other 3 groups (P < 0.05, Figure 2A and 2C). There were no significant differences in plasma LH levels among the pigeons under the 4 photoperiodic programs (Figure 2B). However, plasma PRL levels in the S-18L:6D group were significantly lower than those in the other 3 groups (P < 0.05, Figure 2D).
Figure 2.
Plasma concentration of FSH, LH, E2, and PRL hormones after exposed to different photoperiods during rearing and laying period in White King pigeons (A, B, C and D: FSH, LH, E2 and PRL, respectively). Abbreviations: FSH, follicle stimulating hormone; LH, luteinizing hormone; E2, estradiol; PRL, prolactin.
The reproductive behavior of poultry is mainly regulated by the hypothalamic-pituitary-gonadal axis. In avian species, external photoperiodic stimuli are transferred to the hypothalamus, where they lead to the synthesis and release of gonadotropin-releasing hormones (GnRH). GnRH is transported to the anterior pituitary gland and translated into hormonal signals such as FSH and LH. FSH and LH subsequently reach the ovary and regulate the secretion of steroid hormones (mainly E2) and follicular development. In addition, the secretion of PRL is sensitive to the photoperiod and contributes to the inhibition of GnRH and LH secretion (Shi et al., 2007), resulting in high levels of PRL and contributing to the regression of the reproductive system.
In the present study, a short 8 h photoperiod during rearing period and 16 h photoperiod during the laying period were more effective in improving the plasma FSH and E2 levels and decreasing plasma PRL levels in pigeons, which were the main reasons for the best reproductive performance among the 4 photoperiodic programs. Studies on Magang geese showed that different photoperiods can promote or inhibit the expression and secretion of pituitary PRL and LH (Shi et al., 2007). These results suggest that the photoperiod alters hormone concentrations to stimulate or inhibit follicular development and egg laying.
In summary, a light-restricted photoperiod (8 h) during rearing period delayed AFE, but ensured that the pigeons were maximally photosensitive as a subsequent 16 h photostimulation during the laying period significantly improved the reproductive performance of pigeons, accompanied by improved plasma FSH and E2 levels and reduced plasma PRL hormone levels in female pigeons. The results of this study are of interest to the pigeon breeding industry as this study provides information that 8L: 16D during rearing period and 16L: 8D during laying period can be used to enhance reproductive performances.
ACKNOWLEDGMENTS
The author would like to thank the Jiangsu Agricultural Science and Technology Innovation Fund (JASTIF) (CX (21) 2013) and Jiangsu Provincial Key R&D Program–Modern Agriculture (BE2022315) for financial support of this study.
DISCLOSURES
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
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