https://orcid.org/0000-0002-1821-191X
Abstract
The aim of the study was to evaluate the effect of storage length (7, 14, 21 and 28 days), turning frequency (0, 1 and 24 times per day) and egg position (pointed end up, blunt end up and horizontal) on egg weight loss during storage and incubation; hatchling chick weight, incubation length and hatchability results in 56-week-old chukar partridges (Alectoris chukar). A total of 1800 daily collected eggs was assigned to 36 subgroups (4 × 3 × 3 experimental design) consisting of 50 eggs for each subgroup. Progressive decrease in egg weights and increase in egg weight loss during storage was observed with the lengthening of storage period (p < .001). Prominent effects were observed in total egg weight loss rate and incubation length when the eggs were stored more than 21 days (p < .001). The highest hatchling chick weights were observed in horizontal eggs stored for 7 days (p < .001). Most indices of hatching results showed detrimental effects when turning wasn’t applied and the eggs were stored with the position of blunt end up. General recommendations from the hatching results showed that chukar eggs can be stored up to 21 days of storage length irrespective of turning and egg position. If the chukar eggs are to be stored more than 21 days, turning should be implemented and the eggs should be placed with the position of pointed end up for optimum hatching results.
Due to their chicks’ valuability, partridge eggs are aimed to be incubated. In addition, scientific studies of egg hatching assessment under different conditions during storage period are lacking.
For these reasons, the study was carried out to determine optimum conditions of storage in chukar eggs.
The present results revealed that storing the chukar eggs with the position of pointed end up till 21st days improves the quality of the eggs. If the storage length is to exceed 21 days, the eggs should be turned at least once a day and placed with the position of pointed end up.
HIGHLIGHTS
Introduction
Partridges are widely bred on game farms in Mediterranean countries due to restock game reserves and provide hunting stocks (González-Redondo Citation2006; González-Redondo and Martínez-Domínguez Citation2019). Chukar partridges (Alectoris chukar) are the world’s most common type of partridge species which are reared mostly in Eurasian countries as gamebird (Barbanera et al. Citation2007; Habibi et al. Citation2019). Reduced egg production of partridge hens and high market value of their chicks motivates the producers to incubate all obtained chukar eggs.
Owing to inefficiency of daily egg incubation and transportation, egg storage is one of the most economically crucial steps in poultry industry. Intensive poultry farms practically set daily collected eggs into the storage chambers (15–20 °C and 75–80% RH) to stock them until the eggs are fully loaded to incubators (Fasenko Citation2007). Fluctuations of egg production due to seasonal changes throughout partridge breeding season instigate the need to store the partridge eggs for longer period to get enough amount of them for incubation (González-Redondo Citation2006).
Hatching traits are one of the most major determinants for profitability in poultry industry to obtain high number of day-old chicks (King’Ori Citation2011). In some countries, game farms produce partridge eggs with a sufficient average hatchability and fertility and sold them to well-developed markets. Hatching results of poultry species are affected by several storage conditions such as storage length (González-Redondo Citation2010; Gómez-de-Travecedo et al. Citation2014a), turning frequency (Khan et al. Citation2012; Melo et al. Citation2021) and egg position (Elibol and Brake Citation2008; King’Ori Citation2011; Ayeni et al. Citation2020). Among these factors, the effect of storage length on hatching performance was largely studied in the eggs from several partridge species (Woodard and Morzenti Citation1975; Ozbey and Esen Citation2007; Çağlayan et al. Citation2009; Gómez-de-Travecedo et al. Citation2014a; Günhan and Kirikçi Citation2017). At the same time, partridge eggs are more resistant to long storage period compared to other poultry species (Woodard and Morzenti Citation1975; González-Redondo Citation2010; Günhan and Kirikçi Citation2017). Egg turning of the chukar partridges during storage has revealed no significant benefits in former study (Woodard and Morzenti Citation1975). Turning frequency was partly studied in the eggs of red-legged partridges during 15-day storage period and no beneficial effect was observed due to egg-turning regime (González-Redondo and Martínez-Domínguez Citation2019). Nonetheless, previous scientific studies confirmed that egg turning during storage had several advantages such as shortened incubation duration, improved hatchability and enhanced embryonic development (Elibol and Brake Citation2008; Özlü et al. Citation2021), hence better quality of chicks in other poultry species (Damaziak et al. Citation2018). Moreover, Melo et al. (Citation2021) reported turning regime might have improved storage conditions of the eggs and therefore ensured higher hatching results. Positioning the eggs during storage is important to prevent adverse effect of the prolonged storage time on embryonic mortality and hatchability (Tiwary and Maeda Citation2005; Elibol and Brake Citation2008). Several authors stored the partridge eggs with the position of blunt end up (BEU) with a lack of any experimental study (González-Redondo Citation2010; Gómez-de-Travecedo et al. Citation2014b; González-Redondo and Martínez-Domínguez Citation2019). Moreover, some researchers reported the beneficial effects of eggs stored with pointed end up (PEU) in other poultry species (Tiwary and Maeda Citation2005; Elibol and Brake Citation2008; Mukhtar et al. Citation2013). These potential advantages of turning eggs and egg positions during storage mainly occur in longer storage periods (Elibol O et al. Citation2002; Elibol and Brake Citation2008; Mukhtar et al. Citation2013). Although numerous scientific publications have been conducted about egg storage and hatching performance in various poultry species; there are limited studies investigating the effect of different storage conditions, especially for the factors such as turning frequency and egg position together. Moreover, there are several studies about the effect of storage duration or egg turning during storage in partridges, positioning of the eggs in combination with the storage length and turning frequency during storage for optimum incubation results hasn’t been fully documented yet. Thus, the breeders would store the partridge eggs under optimum storage conditions which would be beneficial for partridge breeding.
Based on the limitations of previous studies that focussed on storage period of partridges, this study aimed to optimise the effect of storage time (7, 14, 21 and 28 days), turning frequency (0, 1 and 24 times a day), egg position (pointed end up, blunt end up and horizontal) and ascertain the interaction between these factors on egg characteristics during storage and incubation, length of incubation period and hatching results in chukar partridges.
Material and methods
Experimental site
The study was conducted at partridge hatchery of Bahri Dagdas International Agricultural Research Institute in Konya, Turkey (37° 52′ 5.7612" and 32° 33′ 12.8088").
Breeder flock and husbandry
Fifty-six-week-old chukar partridges were kept in semi-open wire mesh cages (6.0 × 1.2 × 1.5 m) as 30 females to 10 males per each cage. In addition to the natural photoperiod, artificial lighting was implemented by increasing 1 h per week to 16-h lighting from 36 week of age for natural mating. All the partridges were allowed access to water and feed ad libitum (Table ).
Table 1. The ingredients and chemical composition of partridge diet.
Experimental design
For both storage and incubation, the study was designed as 4 × 3 × 3 factorial arrangement with four storage period (7, 14, 21 and 28 days), three turning frequency (0, 1 and 24 times a day) and three egg position (pointed end up, blunt end up, horizontal) treatments (Table ).
Table 2. The details of experimental design.
Egg collection, storage and incubation conditions
A total 1800 daily fresh chukar eggs between 19–24 g (Kırıkçı et al. Citation2018) was collected throughout four consecutive days according to four storage length groups. All daily collected eggs were numbered and then set to three storage chambers (HD-960L-3in1, Turkey) at average 15 °C and 75% RH for the purpose of forming up three different turning treatments (0, 1 and 24 times a day) as shown in Table . The storage chambers were in the same room where the environmental conditions were controlled. Both hatchery and storage room were located near the partridge cages. The position groups were formed homogenously in the storage chambers. In two of the storage chambers, the eggs were turned with 45° angle from vertical plane. After storage, the eggs were kept at room temperature (22 ± 1 °C) for 18 h and a few cracked ones were excluded from the study. After disinfection with fumigation (formaldehyde + potassium permanganate, 2:1 v/w) for 10 mins; the eggs, a total of 50 of them per each subgroup, were set into an incubator with the position of blunt end up at 37.7 °C, 59% RH (Çimuka T1600 C, Turkey) for 21 days where the eggs were turned 6 times a day. On the 21st d of incubation, the eggs were put into linen bags for exact identification and transferred to hatching baskets (37.2 °C, 72% RH). Turning wasn’t applied at hatchery baskets. All the eggs were weighed before and after storage period, as well as after 21 days of incubation to determine weight (mass) losses. All the subgroups were loaded into the same incubator and hatchery basket. The hatched eggs were counted once a day at the same time on the 23rd, 24th, 25th and 26th days of incubation to identify the incubation length. The hatched partridge chicks were individually weighed at the time after emerged from the shell. All weighing regime was implemented with a digital scale with 0.01 g sensitivity (KERN PFB 1200-2). On 26th day of incubation, all unhatched eggs were opened for rough macroscopic examination by the same experienced researchers and classified as infertile, early (0–9th days), middle (9–21st days), late death (after 21st days) and pipped.
Statistical analyses
Egg traits and incubation length were analysed with univariate GLM procedure in SPSS (version 22.0), considering 5% probability and storage length, turning frequency and egg position were selected as fixed effects. The one-way ANOVA was applied in the related factors with significant interactions. Bonferroni multiple range test was used to determine the significant differences in multiple comparisons. Statistical differences in hatching traits were analysed by performing Pearson Chi-square test with Monte Carlo correction method.
The experimental procedure has been accepted by Ethics Committee of Selcuk University Faculty of Veterinary Experimental Animals Production and Research Center (Permit No. 2020/121, date of approval: 28.12.2020).
Results
Egg traits and incubation length
The means of egg traits and incubation length are presented in Table . The effect of fixed factors on those traits are also illustrated in Table . Storage length showed significant effect on all observed traits. The weight loss rate of chukar eggs during storage was increased progressively with lengthening of storage period (p < .001). However, significant difference in weight loss rate during incubation occurred in the eggs stored for 28 days (p < .001). As for total egg weight loss (%); the significant effects became prominent after 21 days of storage period (p < .001). The chukar chicks from the eggs stored for 7 days had the lowest weights (p < .001). Incubation period started to lengthen when the eggs were subjected to more than 21 days of storage period (p < .001). Neither turning frequency nor egg position had any significant effect on the egg traits and incubation length except for the chicks from the eggs stored horizontally, the average weight of which was significantly greater than other position groups (p < .001).
Table 3. Incubation length and egg weight traits during storage and incubation period in different storage conditions.
Table 4. The effect of storage length, turning frequency and egg position on incubation length and egg weight traits during storage and incubation period of chukar eggs.
Significant interactions between factors and the raw means of subgroups are given in Tables and . There was no significant interaction among the fixed effects for egg weight, egg weight loss during incubation and total egg weight loss. The significant interactions as shown in Table were mostly based on the eggs stored horizontally or stored for more than 21 days. The eggs turned 24 times a day had the longest incubation length in the treatments submitted to 7th days of storage while unturned eggs stored for 21 days had the longest incubation length. Chukar chicks from the eggs stored horizontally for 7 days had the heaviest weight (p < .001). Significant interaction of all factors (storage length × turning frequency × egg position) was observed in egg weight loss during storage (p < .05) and incubation length (p < .01).
Hatching results and embryonic mortality
Generally, hatchability of chukar eggs wasn’t significantly affected by storage length and turning frequency (Table ). The eggs positioned with the pointed end up were characterised by higher hatchability (Table ). The application of egg turning during storage had significant differences for hatchability rate in the eggs stored horizontally (Table ). The highest hatchability rate was observed in the eggs turned 24 times a day during 21 days of storage period (Table ). Furthermore, hatchability rate increased with turning frequency for the eggs positioned pointed end up during 21 days of storage (Table ).
Table 5. The overall effects of fixed factors on hatchability and embryonic mortality results of CHUKAR eggs.
Table 6. The effect of both storage length and turning frequency on hatchability and embryonic mortality results of chukar eggs.
In general, hatchability of fertile eggs wasn’t significantly affected by any of investigated factors (Table ). But, when turning wasn’t applied during the storage, hatchability of fertile eggs increased in eggs positioned pointed end up during storage (Table ). This favourable effect was more evident in the 21 days of storage period (Table ).
Table 7. The effect of both storage length and egg position on hatchability and embryonic mortality results of chukar eggs.
Table 8. The effect of both storage length and egg position on hatchability and embryonic mortality results of chukar eggs.
Table 9. Hatchability and embryonic mortality results of chukar eggs under different storage conditions.
Generally, no significant effect of embryonic mortality rate among all the experimental groups (storage period, turning frequency, egg position) was reported. As for the stage of embryonic mortality, early death rate was decreased with eggs turning in 21-d stored eggs (Table ). The rate of eggs pipped but unhatched was increased in the eggs with the position of blunted end up during 7 days of storage time (Table ). The total embryonic mortality rate was found to be higher in the unturned eggs with the position of blunt end up (Table ) which was more evident in those stored for 21 days (Table ).
Discussion
Storage time
Storing eggs for a certain period of time is one of the most common practices in poultry farms because of the fact that daily incubation and marketing of eggs is uneconomical method (Melo et al. Citation2021). In general, storing eggs more than 7 d is known to be negatively affected the egg quality traits, hatchability results and embryonic mortality rates (Fasenko Citation2007). Although partridge eggs are more resistant to lengthened storage time comparing with the other poultry species, nevertheless, it causes some negative effects on hatching and embryonic mortality results (Günhan and Kirikçi Citation2017). In the present study, average egg weight loss rate during storage was noticeably increased by lengthening of storage period similar to the findings of red-legged partridges (González-Redondo Citation2010; Gómez-de-Travecedo et al. Citation2014b) and rock partridges (Günhan and Kirikçi Citation2017). The excessive weight loss during storage might be detrimental due to dehydration during incubation, which impairs gas exchange for embryo development (Rocha et al. Citation2013). However, the rise in our egg weight loss with lengthening of storage period was within the normal range which resulted in no significant differences of embryonic mortality. Furthermore, weight loss of stored egg isn’t harmful when compared to eggs incubated directly after collecting which may have low hatching results (Benton and Brake Citation1996). The rate of egg weight loss during incubation was decreased in the 28 d of storage period which was inconsistent to the results of red-legged partridge eggs up to 28 day of storage length (González-Redondo Citation2010). The significant increases for total egg weight loss rate became prominent when the partridge eggs were stored more than 21 days. Gómez-de-Travecedo et al. (Citation2014b) reported an increase in total egg weight loss of red-legged partridges when the storage period was lengthened from 7 to 42 days. The possible explanation of egg weight loss during extended storage may be due to the increase of water loss from egg by evaporation (Tiwary and Maeda Citation2005) which was also related to deterioration of internal quality of eggs.
Chick weight of chukar partridges at hatch was affected by storage length. The chicks obtained from the eggs stored for 7 days had the lowest weight at hatch. This might be due to low liquefaction of albumen during short storage period, resulting in lower nutrient and oxygen supply to the chicks (Rocha et al. Citation2013). With the lengthened storage time, different chick weight at hatchling emerged due to egg weight loss. In contrast, Gómez-de-Travecedo et al. (Citation2014b) reported that storing red-legged partridge eggs for 7 and 42-d had no significant effect on hatchling weight of the chicks. The chukar eggs subjected to more than 21-d of storage had longer incubation periods. These results were consistent with the study of Gómez-de-Travecedo et al. (Citation2014b), in which extending the storage time from 7-d to 42-d increased incubation duration in red-legged partridges. These findings supported the hypothesis of Fasenko (Citation2007), which puts forward a notion that the embryos from long-stored eggs might have developed at a slower rate during incubation.
The literature agreed that partridge eggs could be stored throughout 21 days of storage duration without any severe adverse effect for hatching traits (Woodard and Morzenti Citation1975; Ozbey and Esen Citation2007; Çağlayan et al. Citation2009; González-Redondo Citation2010; Günhan and Kirikçi Citation2017; Akbulut et al. Citation2021). Some researchers confirmed no detrimental loss of hatchability traits for partridge eggs stored up to 28-d (Woodard and Morzenti Citation1975; González-Redondo Citation2010). Gómez-de-Travecedo et al. (Citation2014b) reported no detrimental loss of hatchability traits except for hatchability of fertile eggs and late embryonic mortality when eggs of red-legged partridges were held up to 42 days. However, Günhan and Kirikçi (Citation2017) reported some detrimental effects of hatching results in rock partridge eggs when the storage period exceeded 21 days. The current study confirms most of the previous studies that the eggs of chukar partridges can be stored without decline in hatching traits up to 28 days of storage.
Turning frequency
Egg turning during incubation is crucial application for the fact that unturned eggs lead to abnormal adhesion of the embryonic membrane to shell membrane resulting in malposition of the embryo and high embryonic mortality due to inadequate albumen utilisation (Decuypere and Bruggeman Citation2007). Furthermore, turning is applicable method during the long storage period in hatcheries to reduce abnormal development of choriallantoic membrane during incubation (Melo et al. Citation2021). Turning eggs during storage has been mostly investigated in chickens (Gallus gallus) (Elibol O et al. Citation2002; Khan et al. Citation2012; Melo et al. Citation2021; Özlü et al. Citation2021). There is a lack of literature about the effect of turning frequency during storage in partridges. Egg weight loss rate, hatchling chick weight and incubation length weren’t affected by turning frequency during storage and the results were in line with González-Redondo and Martínez-Domínguez (Citation2019), who investigated turning frequency of red-legged partridge eggs stored for 15 days. This may be due to non-significant difference of partridge egg weight loss among turning groups in both studies. Significant interactions for weight loss and chick weight between storage duration and turning frequency weren’t reported in our experiment. According to Melo et al. (Citation2021), an interaction for neither egg weight loss nor chick weight between turning frequency and storage duration was observed in broiler eggs which were in line with our results.
The results showed the importance of egg turning on hatchability of chukar eggs exposed to different storage lengths. In the 21-d of storage period, hatchability rate was negatively influenced due to high early embryonic death in unturned eggs. These results partly confirm the point of Elibol and Brake (Citation2008) which stated that egg turning during long-term storage may allow the blastoderm to interact with more fresh albumen to promote embryonic development at setting. Egg turning during preincubation storage period inhibits early embryo mortality rates (Khan et al. Citation2012). Damaziak et al. (Citation2018) observed positive development of broiler embryos in the first 72 h of incubation when the eggs were turned during storage. Consequently, the beneficial effects of embryo survival due to egg turning during storage improved the hatchability results under long-term storage conditions. The results also partly confirm the beneficial effects of egg turning during storage on broiler egg mortality (Elibol O et al. Citation2002; Özlü et al. Citation2021). González-Redondo and Martínez-Domínguez (Citation2019) turning eggs one, four and 24 times in a day did not influence the hatchability results of the red-legged partridge eggs in the 15 d of storage period. Woodard and Morzenti (Citation1975) reported no appreciable benefit for the hatchability of chukar eggs turned once a day up to 28-d of storage. These studies of partridge eggs weren’t as comprehensive as ours to explain whether egg turning with different frequencies had beneficial effects under different storage conditions. Melo et al. (Citation2021) reported an increase in hatchability of broilers when the eggs were daily turned 180° from the vertical plane irrespective of storage length.
Egg position
Egg position during storage is one of the most crucial factors for hatchability results (Salamon Citation2020). Storing the eggs with the blunt end up position is known to be a traditional way in hatcheries (Terčič and Pestotnik Citation2016) and the researchers from previous studies usually stored the partridge eggs with the position of blunt end up but none of them investigated the potential effect of egg position during preincubation storage conditions (González-Redondo Citation2010; Gómez-de-Travecedo et al. Citation2014b; González-Redondo and Martínez-Domínguez Citation2019). In addition, several studies reported better hatching results in broiler eggs stored with the position of pointed end up (Tiwary and Maeda Citation2005; Elibol and Brake Citation2008; Ayeni et al. Citation2020).
In the present study, egg weight loss wasn’t affected by positioning the eggs blunt end up or pointed end up which was in accordance with the findings of Tiwary and Maeda (Citation2005). Nevertheless, egg weight loss during storage may differ in different storage length when the eggs were stored horizontally. Egg position affected the hatchling weight of the chicks which the highest value was determined in eggs stored horizontal position for 7 days. Similarly, the findings of broilers revealed that the effect of chick weight on egg position became significant in the 7-d of storage period (Ayeni et al. Citation2020).
On an overall basis, hatching results of chukars appeared to show similar performance in different storage positions. However, most indices of hatching performance were negatively affected for the eggs stored with blunted end up position compared with those stored with pointed end up when the chukar eggs were stored more than 21 days and turning wasn’t applied. The results of the present study is in line with findings of Elibol et al. (Citation2002), who reported pointed end up position or adequate turning during storage facilitates normal development of chorioallantoic membrane during incubation. Melo et al. (Citation2021) reported extended storage period caused an increase in embryonic mortality even if the eggs turned during storage in the broiler eggs stored with the position of blunt end up. The literature recommended storing the eggs in the blunted end up position for the fact that highest embryonic mortality rates occurred in those with the position of blunt end up during extended storage period (Tiwary and Maeda Citation2005; Elibol and Brake Citation2008). Thus, hatchability would increase in prolonged storage periods if air cell of the eggs was positioned down (Elibol and Brake Citation2008; Ayeni et al. Citation2020). The explanation of high mortality in the position of air cell up during storage is that increasing the size of air sac due to lengthening of storage period causes embryonic disc to contact with eggshell membrane which may result in embryo sticking and mortality (Tiwary and Maeda Citation2005). However, when the eggs are stored in the position of pointed end up, the chance of lower mortality will increase due to the fact that the embryonic disc can’t contact air sac, which is located at the large end of the eggs, and therefore inner shell membrane. Another explanation may be the fact that the presence of large number of pores on the blunt end increases the weight loss of the eggs (Melo et al. Citation2021). This may cause faster embryo dehydration associated with closer contact with embryonic disc to inner shell membrane. In contrast to these reports, Sahan et al. (Citation2003) could store the ostrich eggs without any adverse effect irrespective of storage position up to 7 days.
Conclusions
The study reproved the durability of partridge eggs under long-term storage periods compared with other poultry species (Fasenko, Citation2007). Specifically, chukar eggs can be stored without serious adverse effects up to 21 days of holding period, regardless of egg storage position and frequency of turning during storage. However, if the holding period is to exceed 21 days, chukar eggs are strongly advised to be stored with the applied modifications such as placing the eggs with position of pointed end up and turning of the eggs for optimum hatching results. The results obtained from chukar partridges also supported the idea that the eggs should be turned and placed with the position of air sac down during prolonged storage, which is essential for high-volume hatcheries of other poultry species. Further storage lengths (> 28 days) can be investigated with the application of these suggested modifications in partridges.
Ethical approval
The study was received financial support from Scientific Research Projects Coordination Unit, Selcuk University (Project Number: 21401031). The experimental procedure has been accepted by Ethics Committee of Selcuk University Faculty of Veterinary Experimental Animals Production and Research Centre (Permit No. 2020/121, date of approval: 28.12.2020).
Author contributions
Conceptualisation, M.Ç.; methodology, M.Ç.; software, Z.K.K and S.G.; validation, M.Ç. and K.K.; formal analysis, M.Ç.; investigation, M.Ç and K.K.; resources, H.H.; data curation, Z.K.K and S.G.; writing—original draft preparation, M.Ç., Z.K.K. and S.G.; writing—review and editing, M.Ç., Z.K.K. and S.G.; visualisation, M.Ç.; supervision, M.Ç., H.H. and K.K.; project administration, M.Ç.; funding acquisition, M.Ç. All authors have read and agreed to the published version of the manuscript.
Acknowledgements
The authors wish to thank the personnel of Bahri Dagdaş International Agricultural Research Institute for their help during the study. The authors are also grateful to Mücahit Çam from Ankara University and Sundus Tewfik from Bloomsnano Limited UK for grammatical revision of the manuscript before submission. The summary of this study was presented as an oral presentation (abstract) in the International Conference on Veterinary, Agriculture and Life Sciences on November 5–8, 2021.
Disclosure statement
No potential conflict of interest was reported by the author(s).
Data availability statement
Upon reasonable request, the datasets of this study can be available from the corresponding author.
Additional information
Funding
References
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