The brooding behavior and physiological differences of Wanxi white geese in different stages of the brooding periodABSTRACT
In this study, a total of 115 geese were selected and raised in 23 separate pens. We found that the average frequency of brooding was 2.18 times during the whole reproduction period. The duration of broodiness of early, middle, and later stage of the brooding period were 2.96 d, 9.93 d, and 4.27 d, respectively. The daily brooding time of early, middle, and later stage of the brooding period were 13.59 h/day, 21.62 h/day, and 5.26 h/day, respectively. The egg production was negatively correlated with the duration of broodiness in early, middle, and later stage of the brooding period and the daily brooding time of early and middle stage of the brooding period. In addition, the LH, FSH, E2, and P4 levels of laying stage were significantly higher than that of early, middle, and later brooding stage. The E2 level of middle stage was significantly lower than early and later stages. Taken together, we demonstrated that annual egg production of geese can be increased through waking up the brooding geese in the early or middle stage of brooding period. And E2 may be a marker hormone for laying stage of Wanxi white geese.
Keywords:
brooding behavior; geese; physiological differences; hormones
RESUMO
Neste estudo, um total de 115 gansos foram selecionados e criados em 23 baias separadas. Descobrimos que a frequência média de cria foi de 2,18 vezes durante todo o período de reprodução. A duração da choca nos estágios inicial, intermediário e final do período de choca foi de 2,96 d, 9,93 d e 4,27 d, respectivamente. O tempo diário de choco nos estágios inicial, intermediário e final do período de choco foi de 13,59 h/dia, 21,62 h/dia e 5,26 h/dia, respectivamente. A produção de ovos foi negativamente correlacionada com a duração da choca nos estágios inicial, intermediário e final do período de choca e com o tempo diário de choca nos estágios inicial e intermediário do período de choca. Além disso, os níveis de LH, FSH, E2 e P4 do estágio de postura foram significativamente mais altos do que os do estágio inicial, intermediário e posterior de choco. O nível de E2 no estágio intermediário foi significativamente menor do que nos estágios inicial e posterior. Em conjunto, demonstramos que a produção anual de ovos de gansos pode ser aumentada com o despertar dos gansos chocos no estágio inicial ou intermediário do período de choco. E o E2 pode ser um hormônio marcador para o estágio de postura dos gansos brancos Wanxi.
Palavras-chave:
comportamento de choco; gansos; diferenças fisiológicas; hormônios
INTRODUCTION
Brooding behavior, a common reproduction trait of most domestic geese, consists of increasing frequency of nest visits, defense of the nest, turning and retrieval of eggs, and sit on a clutch of eggs to incubate them (Romanov et al., 2002). When the female geese show brooding behavior, it indicates the beginning of the transition from laying stage to brooding stage. During the brooding stage, the ovaries of poultry degenerate, which eventually leads to the decline of egg production and feed egg ratio (Ding et al., 2014). China is an important exporter of goose products in the world goose consumption market. However, almost over 90% Chinese goose breeds (Yao et al., 2019), such as Xupu goose (Qin et al., 2021), Zhedong goose (Yu et al., 2016a), and Wanxi white goose, have brooding behavior, which leads to low egg production of these breeds. Therefore, brooding behavior is one of the most important traits that restrict the development of modern goose industry (Yu et al., 2016b).
A number of studies have suggested that broodiness is a quantitative trait controlled by multiple genes (Zhou et al., 2010; Yuan et al., 2020), and its generation is regulated by complex molecular mechanisms (Wu et al., 2021). Female geese not only have conspicuous brooding behavior during brooding stage, but also have significant changes in some physiological state of the brooding geese, including body weight (Begli et al., 2019), body temperature (Yao et al., 2019), and endocrine hormone (Liu et al., 2018; Wang et al., 2021). Previous researchers believed that the hypothalamic-pituitary-gonadal axis plays a decisive role in regulating broodiness (Liu et al., 2018; Gumułka et al., 2020). By its very nature, the coordinated activity of the hypothalamic-pituitary-gonad axis initiates, maintains, and terminates laying and brooding through a variety of reproductive endocrine hormones, including luteinizing hormone (LH), follicle stimulating prolactin (PRL), hormone (FSH), estradiol (E2), progesterone (P4), and Anti-Mullerian hormone (AMH) (Yu et al., 2016a); Onagbesan et al., 2006). In particular, PRL is regarded as a marker endocrine hormone for broodiness (15). The high level of PRL affects the ovary and hypothalamic thermoregulatory center through the blood circulation, thus inhibiting ovarian development and regulating body temperature, and reducing the secretion of LH, FSH, E2, and P4 (Porter et al., 1991).
China has a range of local goose breed with a variety of excellent characteristics. Wanxi white goose, an excellent breed from the west of anhui province in China, is famous for its high quality feather and meat (Chen et al., 2012). However, the large-scale development of Wanxi white geese is restricted by its characteristics of seasonal breeding, long brooding period and low egg production. Generally, Wanxi White geese have 1-3 egg laying cycles (laying-brooding-recovery) every year. The whole reproductive period is from January to May each year. The annual egg production of Wanxi white goose is only 25, compared with that of Sichuan goose (80 eggs/year) (Yao et al., 2019) and Huoyan goose (120 eggs/year) (Qin et al., 2021). In this study, Wanxi white geese were considered to have a relatively stable laying-brooding cycle and a long reproductive cycle, so it became an ideal model to study the brooding behavior and physiological changes of geese.
Taken together, the brooding behavior of geese is one of the key factors restricting the further improvement of goose egg production. It is important to understand the brooding behavior and physiological changes of goose to improve egg production (Yao et al., 2019). However, due to the underdeveloped monitoring technology in the past, the actual observation of the brooding behavior was fixed point observation (Jiang et al., 2010) or timed observation (Yao et al., 2019), which greatly weakened the authenticity and reliability of the brooding behavior research results. A new commercial monitoring system was used in this study, including infrared night vision, which enabled day and night monitoring of brooding behavior. Moreover, there are few literatures on the brooding behavior and physiology of geese, especially the long-term observation data on the brooding behavior and physiology. In the current study, the reproduction period of Wanxi white geese was observed for a long time (December 20, 2020 to May 20, 2021), and a large number of original information were collected, which laid a foundation for further research on the regulation mechanism of broodiness.
MATERIALS AND METHODS
All animal procedures were performed according to guidelines provided by the China Council on Animal Care. All animal experiments were approved by the Animal Care and Use Committee of West Anhui University (SYXK, Wan 2021-009).
A total of 115 Wanxi white geese, including 23 male geese (600 day old) and 92 female geese (300 day old), were selected and raised in 23 separate pens (1♂ and 4♀ per pen). All geese were kept at the standard light level of 14 h (14L:10D) during the laying period. In this experiment, all geese were provided the same diet (Table 1) and fed ad libitum. The geese were raised in pens equipped with playground fields. The egg-laying area, covered with rice husks, is large enough (2.5m x 1m) to comfortably accommodate four standing geese and allow the geese to easily turn around.
The automatic video acquisition system (Dahua, Hangzhou, China) was set up above egg-laying area in the pen of each group. Colored paint on the neck or/ wing of each female geese was used as a marker for behavior observation. Based on the preliminary experiment and previous literature (Yao et al., 2019), when geese had laid a batch of eggs, some geese began to display the brooding behavior, and this behavior persisted for more than 3 days, we classified it as the beginning of the brooding. At this point, the brooding behavior mainly includes starting to incubate the egg (even if the egg is not produced by this goose), turning and retrieval of eggs, brooding in the egg-laying area for a long time after removing the egg, feeding frequency and time gradually reduced.
According to the characteristics of brooding behavior, the brooding period of geese can be divided into three stages: (1) The early stage of the brooding period, geese begin to engage in nest-seeking behavior, including frequent visits to the nest, walk around the egg-laying area, and looking for a suitable nest. Once they find a suitable site, the geese build their nest out of scattered straw, shells, or feathers. At this stage, the geese brooding time gradually increased, but not continuous, each brooding lasted 2-6 hours. (2) The middle stage of the brooding period, geese brooding for more than 21 hours a day during this period. During the non-brooding time of the day, the geese only did feeding, drinking and standing activities, but did not play, it can be observed that geese are slow walking and depressed in every activity. At the same time, the frequency of feeding and drinking decreased significantly. (3) The later stage of the brooding period, compared to geese in the middle of the brooding period, the brooding time of geese in this stage was gradually decreased, and the frequency of drinking and feeding gradually increased. Coincidentally, the feather color of geese in this stage get dim (Yao et al., 2019).
The brooding behaviors of 92 female were recorded daily in the annual reproductive cycle, the observation period from December 20, 2020 to May 20, 2021. In the brooding period, the duration of broodiness, daily brooding time, feeding frequency, and drinking frequency were recorded. And then, the number of brooding geese, the percent of broodiness, the maximum brooding days, and the brooding frequency of each goose were calculated and analyzed.
In the laying stage, the individual egg production was identified and recorded daily using the automatic video acquisition system. When at night or in a dark environment, the infrared function is used to identify the geese by the depth and position of the animal markers to record data. The average egg production of each goose during the annual reproductive cycle was calculated and analyzed.
The body weight of 92 female geese were determined in laying stage and early/middle/later stage of the brooding period. As the procedure of the measuring body temperature is stressful to the goose of reproduction period, 30 geese of laying stage were randomly selected for measuring body temperature through the cloaca (rectal temperature) with a digital thermometer (Braun, model Prt1000). 30 geese from other stages were also randomly selected for temperature measurement.
Eight female geese in the laying stage as well as the early, middle, and later stage of brooding period, respectively, were selected. And the blood samples were immediately collected from wing vein using heparinized tubes and centrifuged at 3000 rpm for 10 min to collect plasma for the detection of reproductive hormones. The concentrations of PRL, LH, FSH, E2, P4, and AMH were analyzed by using commercial goose ELISA kit (Nanjing Jiancheng Bioengineering Institute, Nanjing, China). The minimal detectable doses of PRL, LH, FSH, E2, P4, and AMH were 1 mIU/L, 1ng/mL, 0.1mIU/mL, 40pg/mL, 0.2ng/mL, 1ng/mL, respectively.
All data were analyzed using SPSS software (SPSS, Ver. 20.0). Differences in body behavior, egg production, body weight, body temperature, and concentrations of reproduction endocrine hormone were analyzed by one-way ANOVA with the LSD test for multiple comparisons. Correlation of egg production and brooding time were calculated by Pearson correlation coefficients. The mean ± standard deviation (SD) was used to represent the results. Differences between means were considered significant at P < 0.05.
RESULTS
The statistical analysis of brooding behavior of all geese were presented in Table 2. In the current study, a total of 92 geese were observed for nearly five months (From December 20, 2020 to May 20, 2021), we found that about 97.83% of the geese had the brooding behavior. Only 2 geese did not have the brooding behavior during the entire observation period. In the final statistical analysis, 12 geese had only one brooding period during the observation period, 45 geese had two brooding period during the observation period, 33 geese had three brooding period during the observation period. The average frequency of brooding of Wanxi white goose was 2.18 times. Among the brooding geese, the maximum brooding days was 55 days.
The statistical analysis of brooding behavior of goose in different stage of the brooding period were showed in Table 3. The duration of broodiness of early, middle, and later stage of the brooding period were 2.96 d, 9.93 d, and 4.27 d, respectively. The duration of broodiness of middle stage of the brooding period was significantly longer than that of early and later stage (P < 0.05), the duration of broodiness of later stage of the brooding period was significantly longer than that of early stage (P < 0.05). The daily brooding time of early, middle, and later stage of the brooding period were 13.59 h/day, 21.62 h/day, and 5.26 h/day, respectively. The daily brooding time of middle stage of the brooding period was significantly longer than that of early and later stage (P < 0.05), the daily brooding time of early stage of the brooding period was significantly longer than that of later stage (P < 0.05). The feeding frequency of early, middle, and later stage of the brooding period were 3.76 times/day, 2.13 times/day, and 4.05 times/day, respectively. The feeding frequency of middle stage of the brooding period was significantly lower than that of early and later stage (P < 0.05). The drinking frequency of early, middle, and later stage of the brooding period were 4.79 times/day, 2.41 times/day, and 5.59 times/day, respectively. The drinking frequency of middle stage of the brooding period was significantly lower than that of early and later stage (P < 0.05), the drinking frequency of early stage of the brooding period was significantly lower than that of later stage (P < 0.05).
The difference in average brooding days between different brooding periods in the annual reproductive cycle was shown in Figure. 1A. The average brooding days of the first, second, and third brooding periods were 14.01 d, 14.79 d, and 11.06 d, respectively. The average brooding days of third periods were significantly lower than that of the first and second periods (P < 0.05). There was no significant difference in the average brooding days between the first and second brooding periods.
The correlation coefficients between egg production and brooding time were presented in Table 4. The egg production was negatively correlated with the total brooding days (r = -0.49, P < 0.05) and the total frequency of brooding period (r = -0.56, P < 0.05). In detail, the egg production was negatively correlated with the duration of broodiness in early (r = -0.26, P < 0.05), middle (r = -0.34, P < 0.05), and later (r = -0.25, P < 0.05) stage of the brooding period and the daily brooding time of early (r = -0.23, P < 0.05) and middle (r = -0.31, P < 0.05) stage of the brooding period. The total brooding days was positive correlated with the total frequency of brooding period (r = 0.90, P < 0.05), and it also positive correlated with the duration of broodiness in early (r = 0.46, P < 0.05), middle (r = 0.49, P < 0.05), and later (r = 0.40, P < 0.05) stage of the brooding period and the daily brooding time of early (r = 0.23, P < 0.05) and middle (r = 0.42, P < 0.05) stage of the brooding period.
The total frequency of brooding period correlated with the duration of broodiness in early (r = 0.45, P < 0.05), middle (r = 0.58, P < 0.05), and later (r = 0.40, P < 0.05) stage of the brooding period and the daily brooding time of early (r = 0.37, P < 0.05) and middle (r = 0.47, P < 0.05) stage of the brooding period.
The effect of the frequency of the brooding on egg production in the annual reproductive cycle was shown in Figure 1B. The average egg production of non-brooding goose and goose with, one, two, and three brooding periods were 28.50, 25.58 d, 20.20 and 16.21, respectively. The average egg production of non-brooding goose was significantly higher than that of goose with two or three brooding periods (P<0.05). The average egg production of goose with one brooding period were significantly higher than that of goose with two or three brooding periods (P<0.05). The average egg production of goose with two brooding period were significantly higher than that of goose with three brooding periods (P<0.05).
(A) The difference in average brooding days between different brooding periods in the annual reproductive cycle. (B) Effect of the frequency of the brooding on egg production in the annual reproductive cycle. Fb = 3; The frequency of brooding was 3 in the annual reproductive cycle. Fb = 2; The frequency of brooding was 2 in the annual reproductive cycle. Fb = 1; The frequency of brooding was 1 in the annual reproductive cycle. Fb = 0; The frequency of brooding was 0 in the annual reproductive cycle. The data were shown as mean ± SD. The different letters indicate significant difference (P<0.05).
The effects of different reproductive stages on body weight and body temperature were showed through Box plots in Figure 2. The body weight of goose during laying stage were significantly higher than that of goose during early (P<0.05) and middle (P<0.05) stage of brooding periods. There was no significant difference in body weight of goose between the laying stage and later stage of brooding period. The body temperature of goose during laying stage were significantly higher than that of goose during early (P<0.05) and middle (P<0.05) stage of brooding periods. There was no significant difference in body weight of goose between the laying stage and later stage of brooding period.
Effects of different reproductive stages on body weight and body temperature. (A) Box plots to show the body weight (g) of Wanxi white geese at different reproductive stages. (B) Box plots to show the body temperature (℃) of Wanxi white geese at different reproductive stages. ns; no significant. **; significant difference (P<0.05).
The effect of different reproductive stages on plasma hormone level was shown in Table 5. The PRL and AMH levels of laying stage were significantly lower than that of early, middle, and later brooding stages (P < 0.05). Among different brooding stages, the PRL level of middle stage was significantly higher than early and later stages (P<0.05). The PRL level of early stage was significantly higher than later stage (P<0.05). The AMH level of early stage was significantly lower than that of middle and later stages (P<0.05). The LH, FSH, E2, and P4 levels of laying stage were significantly higher than that of early, middle, and later brooding stage (P<0.05). Among different brooding stages, the E2 level of later stage was significantly higher than early and middle stages (P<0.05). The E2 level of early stage was significantly higher than that of middle stage (P<0.05).
DISCUSSION
For most goose breeds, the low egg production and long reproduction period result in high price and seasonal supply shortage of commercial goose seedlings. Many scholars have confirmed that strong broodiness is an important factor leading to low egg production (Qin et al., 2021; Zhang et al., 2021), this causal relationship has been demonstrated not only in geese, but also in turkeys (Begli et al., 2019), chickens (Jiang et al., 2010), and other poultry (Ye et al., 2019). In the current study, a total of 92 geese were observed for nearly five months. Among them, only two geese showed non-broodiness during the entire observation period, and the remaining 90 showed brooding behavior. According to field research, the percentage of broodiness (98%) in this study is consistent with farming experience of the farm staff. The high percent of broodiness of local geese brings great difficulties to breeding of high-reproductive geese by selecting non-brooding individuals (Yao et al., 2019). In fact, over the past decade, the egg production of Wanxi white goose (average 25 eggs per year) was difficult to improve due to strong broodiness (close to 98% of the broodiness rate), which seriously affected the expansion of industrial scale.
In the long-term observation, we found that the important performances of broodiness were hatching eggs and other related brooding behaviors. These findings were consistent with previous studies (Romanov et al., 2002; Yao et al., 2019). In addition to the brooding behavior that has been found by predecessors, we found that some brooding geese would turn eggs that are not picked up in time, or bury the eggs with feathers or fragments, even if these eggs are not born by them. This may reflect egg-shaped objects will cause brooding occurrence, whether the egg-shaped object is produced by itself or by other geese.
The duration of brooding behavior has also attracted our attention. In order to further study the brooding duration, the brooding period in this experiment was divided into three periods according to the differences in brooding behavior, which was mainly based on previous study on Zhedong geese (Yao et al., 2019). It is worth signaling that we usually make repeated video observations on a female goose to confirm whether it is in the end of laying period or early stage of brooding period during the observation period. At the end of the laying period, some geese begin to exhibit brooding behavior of early stage of brooding period (the brooding time of geese gradually increased, but not continuous, each brooding lasted 2-6 hours). This phenomenon occurs in some geese, lasts for one or two days, and finally lays an egg. It can be assumed that some female geese may have dystocia at the end of laying period, so they need to enter the laying area for many times within 1 - 2 days.
In the current study, the egg production was negatively correlated with the total brooding days and the duration of broodiness in early and middle stage of brooding period. It can be inferred that the egg production of geese may be increased by reducing the brooding days, especially the duration of broodiness in the early and middle stages of brooding period. It is logical to assume that the annual egg production of geese can be increased through waking up the brooding geese in the early or middle stage of brooding period during the production process. Besides, in this study, the body weight and body temperature of geese during laying stage were significantly higher than that of goose during early and middle stage of brooding periods. Combined with the actual observation of the state of geese, we concluded that the brooding goose is very weak, which is manifested by the decrease in body weight and body temperature. Therefore, it is obvious that waking up the brooding goose will further aggravate the weak state of the goose and even cause potential body damage.
In this scenario, the brooding geese should be woken up at the right time during the brooding period to reduce the damage to the geese. In the current study, the feeding frequency and drinking frequency of middle stage of the brooding period was significantly lower than that of early stage. Moreover, the daily brooding time of middle stage of the brooding period was significantly longer than that of early and later stage. Herein, it can be speculated that the potential damage to geese was lower when the geese woke up in the early stage of brooding period rather than at the middle stage of brooding period. Meanwhile, considering the short early stage of brooding period and the long middle nesting period of geese, the geese in the early stage of brooding period should be awakened in time during production period to prevent the extension of the total brooding days. However, as mentioned above, it is difficult to make a subjective distinction between the end of laying period and the early stage of brooding period. Considering the difficulty of production management, most breeding farm breeders usually only wake up a batch of brooding geese on a fixed date. In such a situation, it is difficult to accurately calculate the brooding period of each goose, resulting in the artificial selection of geese with short brooding period is often difficult to carry out.
As is well-known, most avian species are seasonally and their reproductive process is initiated by environmental queue (Rangel and Gutierrez, 2014). In the chickens, a previous study indicated that initiation of avian reproductive season may be caused by the decrease of melatonin and gonadotropin-inhibitory hormone (GnIH) with the increase of day length (Ono et al., 2009). Similarly in the geese, based on the principle that photoperiod affects avian reproduction, lighting management has become an effective means to improve goose egg production (Liu et al., 2018). In essence, geese have evolved endocrine mechanisms coincide with the photoperiod to control their reproductive process (Akhtar et al., 2021), including regulation of brooding behavior (Chen et al., 2020; Zhang et al., 2021). Light acts on avian photoreceptors to stimulate the secretion of hypothalamic gonadotropin-releasing hormone (GnRH), which in turn induces the secretion of FSH and LH (Chen et al., 2017). FSH and LH promote the development and maturity of follicles, while GnIH interferes with the secretion of FSH and LH hormones, thus affecting maturation and recruitment of follicles (Bédécarrats et al., 2009). In the current study, we found the LH and FSH levels of laying stage were significantly higher than that of early, middle, and later brooding stage. These results corroborated previous findings from turkeys (Porter et al., 1991) and goose (Wang et al., 2021). Moreover, a previous study indicated that adequate photoperiod stimulates LH and FSH secretion to promote reproductive organs and follicle development of laying ducks (Cui et al., 2021).
P4 and E2 are also important reproductive hormones, which cooperate with FSH and LH to promote gonad maturation, induce ovulation, and maintain reproductive performance in avian (Farias et al., 2016). P4 is released by granulosa cells of graded follicles and play a key role in determining the length of the laying period (Wilson and Sharp, 1976). The developing follicle produces E2. E2 allows P4 to stimulate GnRH secretion and acts as a hypothalamic primer for P4 (Kawashima et al., 1979). In this study, we found E2 and P4 levels of laying stage were significantly higher than that of early, middle, and later brooding stage. This result was consistent with previous study in Muscovy duck (Ye et al., 2019). It is worth signaling that only the E2 of the four hormones fluctuated greatly during the brooding period. In this study, E2 level increased rapidly and recovered after reaching the lowest point in the middle of the brooding stage. This result also followed the same trend as pasting findings in Zhedong white geese (Yu et al., 2016b). These results confirmed that LH, FSH, E2, and P4 play an important role in maintaining reproductive performance of Wanxi white geese. Among these, we concluded that E2 may be a marker hormone for laying stage of Wanxi white geese.
AMH is an important factor associated with broodiness in avian. AMH is associated with enhanced ovarian granulosa cell proliferation and follicular development selection (Rey et al., 2003). In the current study, the PRL and AMH levels of laying stage were significantly lower than that of early, middle, and later brooding stages. This result was consistent with previous study in hen (Johnson et al., 2009). Moreover, it was reported in goose that AMH may hinder follicular development by reducing pituitary FSH secretion and follicular sensitivity to FSH (Chen et al., 2020). Furthermore, it has also been speculated in goose that active immune against recombinant protein AMH can promote LH secretion, regulate follicular development, and reduce broodiness rate (Zhang et al., 2021).
PRL is considered to be a marker hormone for broodiness in birds and plays a key role in initiating and maintaining brooding behavior (Wilkanowska et al., 2014). In the current study, we found the PRL level of laying stage were significantly lower than that of early, middle, and later brooding stage. The result agrees with previous studies in goose (Yao et al., 2019; Wang et al., 2021). Moreover, a previous research indicated that reducing PRL levels by regulating photoperiod can reduce the rate of broodiness in hens (Geng et al., 2014). Furthermore, it is well established that stimulation of long photoperiod increased PRL secretion and decreased LH secretion in Magang geese, resulting in the end of reproductive activities, while stimulation of short photoperiod led to LH secretion and inhibited PRL secretion in Magang geese, promoting the beginning of reproductive activities (Shi et al., 2007). Besides, a previous study indicated that the reproductive activities degradation of birds was accompanied by an increase in the secretion of PRL hormone (Dawson and Sharp, 1998). Consistently, in the current study, the content of PRL reached its peak in the middle stage of brooding period. The aforementioned results confirmed that PRL is a marker hormone for brooding stage of Wanxi white geese.
CONCLUSIONS
Through this study, the brooding behaviors and physiological differences of Wanxi white geese in different brooding periods were revealed. We demonstrated that annual egg production of geese can be increased through waking up the brooding geese in the early or middle stage of brooding period during the production process. And the E2 may be a marker hormone for laying stage of Wanxi white geese.
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Publication Dates
-
Publication in this collection
14 July 2025 -
Date of issue
Jul-Aug 2025
History
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Received
19 Sept 2024 -
Accepted
26 Oct 2024
