Abstract
This study investigated the effect of the egg cooling profile after oviposition on blastoderm development, embryonic mortality, hatchability, and hatch time of broiler hatching eggs from young and old breeder flocks. Hatching eggs were obtained from commercial Ross 308 broiler breeders at 28 wk (young) and 64 wk (old) of age. A total of 3,150 eggs laid within a 15-min period were collected and randomly assigned to 2 temperature-controlled chambers in both flocks. The eggshell temperature (EST) was cooled to 24°C either within 6 h (control) or 45 min (rapid). After the EST reached 16°C in the chambers in all groups, eggs were transported to the commercial hatchery. Eggs were stored for 6 d at 16°C and 75% relative humidity. The development of the blastoderm in sampled eggs (25 embryos in each batch) was determined immediately after egg collection and before transport to the hatchery (after cooling) on a farm in each flock. At each flock age, there were 5 replicate trays of 150 eggs per egg cooling treatment set in a single commercial incubator. The results showed that the embryonic developmental stage was retarded by rapid cooling and by the younger flock. A flock age × cooling rate interaction was observed for fertile hatchability and early and late embryonic mortality (P < 0.001). In the young flock eggs, the fertile hatchability was significantly lower in the rapid than in the control cooling treatment (88.7 vs. 92.8%) due to higher early and late embryonic mortality, whereas rapid cooling reduced early embryonic mortality (P < 0.01) and numerically increased the fertile hatchability (88.7 vs. 87.2%) in the old flock eggs. Hatch time was affected by the cooling treatment. The average hatch time was delayed by 3 h by rapid cooling (486.2 vs. 489.2 h) after oviposition compared with the control. This study showed that cooling the EST to 24°C within 45 min (rapid cooling) compared to 6 h (control) after laying retarded the blastoderm developmental stage and hatch time of eggs from both young and old broiler breeder flocks. This was apparently detrimental for the young flock as indicated by the higher early and late embryonic mortality but beneficial for the old flock due to the lower early embryonic mortality. The differences in hatchability between young and old flock eggs resulting from a rapid cooling rate might depend on the differences in embryonic development at oviposition.
Key words: egg cooling rate, temperature profile, egg storage, blastoderm development, hatchability
INTRODUCTION
Chick embryo development is generally thought as starting at incubation and lasting 21 d; however, not only does fertilization take place before the egg is laid, but some of the most critical events occur during this period (Bellairs and Osmond, 2014). The start of embryo development takes place in the oviduct, where the hen's body temperature is 40°C to 41°C. After oviposition, the eggs experience a major change in external temperature, and the first environmental parameter that the embryo encounters is cooling from body temperature (40°C) to poultry house temperature (20°C–22°C). A temperature of 24°C is considered the “physiological zero” of the embryo; therefore, embryonic development is interrupted below 24°C (Rocha et al., 2013). Aviagen (2009) recommended that eggs should be cooled to below 24°C on the farm within 4 to 6 h after collection. Similarly, Hendrix Genetics (2022) reported that eggs should be uniformly cooled from the hen's body temperature to between 22°C and 25°C in approximately 6 h. In addition, rapid cooling results in less developed embryos, and slow cooling results in too many advanced embryos. In both cases, the embryo survival of stored eggs is reduced. Most studies on the effect of egg cooling rate after oviposition were performed at the higher environmental temperature in the nest or with the eggs remaining in the nests for longer periods of time between oviposition and egg collection (Bowling and Howarth, 1981; Fasenko et al., 1991, 1999; Scott and Mackenzie, 1993; Meijerhof et al., 1994). However, little recent research has been reported on the influence of flock age and rapid egg cooling between the time immediately following oviposition and the time when the egg is cooled to below physiological zero on embryo development, hatchability and hatching time. Meijerhof et al. (1994) found no significant difference in hatchability at lower nest temperatures (10°C) compared with the control (20°C) and higher (30°C) nest temperatures from prime (37 wk) and old (59 wk) flocks. Rapid cooling improved the albumen quality and reduced the weight loss of eggs compared with slow cooling (Thompson et al., 2000). Fiúza et al. (2006) reported that hatching eggs from 31-wk-old Ross broiler breeders that were cooled 5 h after oviposition produced the highest fertile hatchability compared to those cooled immediately or 10 h after collection from the poultry house.
The influence of rapid egg cooling after oviposition on incubation parameters is largely unknown. Therefore, we investigated the effects of rapid eggshell temperature (EST) cooling after oviposition on blastoderm development, embryonic mortality, fertile hatchability, and hatching time of broiler hatching eggs from young and old breeder flocks.
MATERIALS AND METHODS
Experimental Design
The experiment was designed as a 2 × 2 factorial arrangement with 2 flock ages (28 wk and 64 wk) and 2 cooling rate treatments (rapid and control) after oviposition. All experimental procedures were approved by the University of Ankara Institutional Animal Care and Use Committee (Ankara, Türkiye).
Broiler Breeder Flocks
Eggs from 2 commercial Ross 308 broiler breeder flocks fed the same diet and subjected to the same management scheme within the same geographic area were used. Breeder flock ages were 28 wk (young) and 64 wk (old).
Egg Collection and Cooling Procedure
At each flock age, a total of 1,575 eggs that had been laid within a 15-min period were collected and placed in plastic egg trays. The eggs from each flock age were then randomly assigned to 2 identical climate-controlled chambers with a capacity of 800 eggs (4 chambers total; Egg Storage Cabinet, Cimuka Inc., Ankara, Türkiye) located on the farms. Eggs were cooled to 24°C within 6 h (control cooling) or within 45 min (rapid cooling) (Figure 1). The EST (18 eggs in each chamber) was measured with a ThermoScope-HT-F03A infrared thermometer (Medicare, Singapore, Malaysia) at 15-min intervals to adjust the air temperature of the chambers during the cooling process. The relative humidity (RH) in the chambers averaged 65.1 ± 5.6%. Eggs from young and old flock were kept in the chambers until the EST of both cooling groups was similar (reaching 16°C). Then, the eggs were transported (approximately 15 min) to a commercial hatchery (Erpilic, Bolu, Türkiye) in a temperature-controlled vehicle.
Figure 1.
Eggshell temperature (EST) profile of the cooling treatments for both flock ages. The EST was cooled to 24°C either within 6 h (control) or 45 min (rapid). In the temperature-controlled chambers, the temperature was adjusted by an infrared thermometer every 15 min. Young = 28 wk of age; old = 64 wk of age.
Storage and Incubation
A total of 3,000 eggs were stored for 6 d at 16.0°C ± 0.2°C and 75.2 ± 3.1% RH. Then, all eggs were incubated together in a single incubator and hatcher with a capacity of 57,600 and 19,200 eggs, respectively (Petersime, Zulte, Belgium). The remaining space in the incubator and hatcher was filled with hatching eggs that were not part of the experiment to ensure uniform airflow across eggs. A single-stage incubation program with a gradually decreasing set-point temperature of 38.1°C at embryonic day (E) 1 to 37.5°C at E19 was used. The hatcher began at a set-point temperature of 37.2°C at E19, which was gradually decreased to 36.4°C at E21. The RH was maintained at 70 ± 1.5% during the first 10 d of incubation (minimum ventilation) and then ventilated to maintain 40 ± 1.8% RH until E19. Eggs were turned 90° on an hourly basis in the incubator until being transferred to baskets and placed in a hatcher at 450 h of incubation.
Measurements
Embryo Collection and Staging
To assess the blastoderm development of eggs collected from young and old flocks, a random subset of 25 embryos from each flock age (total of 150 embryos) was examined before (at collection time) and after a rapid or control cooling period (before being sent to the hatchery). The embryos were isolated from the yolk by using the filter ring technique as described in Gupta and Bakst (1993). The dorsal and ventral sides of the embryo were examined with a stereomicroscope (Leica S6D, Leica Microsystems GmbH, Wetzlar, Germany) to determine the stage of embryonic development according to the classification of Eyal-Giladi and Kochav (1976), termed EGK.
Hatch Time
The hatcher was opened at 480, 492, and 510 h of incubation and the number of hatched chicks was counted to determine the hatch time (i.e., chicks already out of their shells, with closed navel and fairly dry). The hatching process was divided into 3 time periods. The early period was up to 480 h, the middle period was from 481 to 492 h, and the late period was from 493 to 510 h of incubation. The percentage of chicks hatched in these periods relative to the total number of hatched chicks was calculated for each group. All chicks that had completed the hatching process were removed from the hatching baskets at 510 h of incubation.
Embryonic Mortality and Hatchability
At both flock ages, infertile and early dead (0–7 d) embryos were identified by candling, removal, and macroscopic examination at E10 by a single experienced individual. At the time of removal of chicks from hatchers (510 h of incubation), all remaining unhatched eggs were opened and examined macroscopically by the same individual to determine the remaining mid (8–18 d) and late (19–21 d plus pipped) embryonic mortality. The number of second-grade chicks, which had deformities or lesions, such as splayed legs, unhealed navels, and physical abnormalities, as judged by experienced hatchery staff was determined for each cooling group per flock age at the time of final pull. The percentage hatchability of fertile eggs was calculated as the number of chicks hatched per 100 fertile eggs.
Statistical Analysis
Each tray of 150 eggs was considered to be a replicate, and there were 5 replicate trays per subtreatment group. The data from the completely randomized design were subjected to 2-way analysis of variance (ANOVA) using the GLM procedure of SAS (version 9.1, SAS Institute, 2004). The percentage of the blastoderm development and hatching time were analyzed using the chi-square test via Minitab Version 14 (Minitab Inc., State College, PA). Statements of statistical significance were P < 0.05 unless otherwise indicated.
RESULTS AND DISCUSSION
Embryonic Development
The most common stage of embryonic development in chickens at the time of laying is stage “X”, and the embryos tend to be less developed when the embryonic developmental stage at oviposition is below stage X (<EGK10) (Fasenko, 2007). In the current study, although the average developmental stage of the embryos on the day the eggs were laid was below EGK10 in both flocks, the stage of blastoderm development was more advanced for the eggs from the old flock (EGK9.56 ± 0.507) than for the eggs from the young flock (EGK8.32 ± 1.492) (P < 0.001). At oviposition, the pregastrula stage of development (<EGK10) comprised approximately 68% of the eggs from the young flock and approximately 44% of the eggs from the old flock (Figure 2). These differences between flock age for embryo development were also observed after egg cooling, with the eggs from the old flock (EGK11.42) being on average EGK1.03 ahead of those from the young flock (EGK 10.39) (P = 0.014) (Table 1). Several studies have similarly reported that the stage of blastoderm development is more advanced both before and after storage for eggs from an old flock than for eggs from a young flock (Reijrink et al., 2009; Özlü et al., 2018, 2021; Pokhrel et al., 2018).
Figure 2.
Percentage of embryos at different EGK stages in the fresh, rapid, and control cooling treatments in eggs from young (28 wk) and old (64 wk) broiler breeder flocks. EGK = embryonic developmental stage according to Eyal-Giladi and Kochav (1976). 1Cooling profile: fresh = eggs were opened at collection time; rapid = eggshell temperature (EST) was cooled to 24°C within 45 min; control = EST was cooled to 24°C within 6 h. 2Flock age: young = 28 wk, old = 64 wk. a,bPercentages in a particular stage followed by different letters differ significantly in eggs from young flocks (χ2 = 9,792; DF = 2; P = 0.007). x,yPercentages in a particular stage followed by different letters differ significantly in eggs from old flocks (χ2 = 8,600; DF = 2; P = 0.014).
Table 1.
A comparison of the stage of blastoderm development of eggs from young (28 wk) and old (64 wk) flocks based on embryonic stage scale of Eyal-Giladi and Kochav (1976) (EGK) following the egg cooling treatments.
| Flock age1 | Cooling profile2 | n3 | Blastoderm development |
|---|---|---|---|
| EGK | |||
| Young | 50 | 10.39b | |
| Old | 50 | 11.42a | |
| SEM | 0.256 | ||
| P value | 0.014 | ||
| Rapid | 50 | 10.50b | |
| Control | 50 | 11.31a | |
| SEM | 0.256 | ||
| P value | 0.047 | ||
| Young | Rapid | 25 | 9.92 |
| Control | 25 | 10.86 | |
| Old | Rapid | 25 | 11.08 |
| Control | 25 | 11.76 | |
| SEM | 0.362 | ||
| P value | 0.492 |
Means followed by different letters differ significantly (P < 0.05).
Flock age: young = 28 wk, old = 64 wk.
Cooling profile: The eggshell temperature was cooled to 24°C either within 6 h (control) or 45 min (rapid).
There were 25 embryos per subgroup.
In the present study, the blastoderm stages of embryos in the control cooling treatment were more advanced than those in the rapid cooling treatment (EGK 11.31 vs. 10.50) (Table 1). In the present study, percentages of eggs in the pregastrula stage of embryo development (<EGK10) were 48 and 24% for the rapid and control cooling treatments, respectively, in young flock eggs. The percentages were 24 or 8% for the rapid and control cooling treatments in old flock eggs, respectively. The results of this study agree with those of previous studies (Fasenko et al., 1991, 1999; Hudson et al., 2004), which indicate that the embryonic developmental stage is accelerated by the higher environmental temperature in the nest or when the egg remains in the nest for a longer period of time between oviposition and egg collection.
No interactions were observed between flock age and cooling treatment for the stage of embryonic development (Table 1).
Hatchability, Embryonic Mortality, and Second-Grade Chicks
In the present study, an interaction between flock age and cooling rate was observed for fertile hatchability and early and late embryonic mortality (P < 0.001; Table 2). In the young flock eggs, the fertile hatchability was significantly lower in the rapid cooling than in the control cooling treatment, whereas the hatchability was not affected by the cooling treatment in the old flock eggs. A similar effect was also observed on late embryonic mortality. Moreover, an interaction effect was observed on early embryonic mortality, as it was significantly (P < 0.05) increased by the rapid cooling treatment compared with the control in young flock eggs, but the opposite was observed in eggs from the old flock, in which rapid cooling reduced early embryonic mortality (P < 0.05).
Table 2.
Effects of cooling profile on the hatchability of fertile eggs and embryonic mortality.
| Flock age1 | Cooling profile2 | n3 | Hatchability of the fertile eggs | Embryonic mortality |
Cull4 | ||
|---|---|---|---|---|---|---|---|
| Early | Mid | Late | |||||
| (%) | |||||||
| Young | 10 | 90.74a | 4.66b | 0.42b | 3.33 | 0.85b | |
| Old | 10 | 87.76b | 6.51a | 0.99a | 2.42 | 2.33a | |
| SEM | 0.598 | 0.313 | 0.178 | 0.333 | 0.166 | ||
| P value | 0.001 | 0.001 | 0.032 | 0.06 | 0.001 | ||
| Rapid | 10 | 88.51 | 5.65 | 0.76 | 3.59a | 1.50 | |
| Control | 10 | 90.00 | 5.52 | 0.65 | 2.16b | 1.67 | |
| SEM | 0.598 | 0.313 | 0.178 | 0.333 | 0.166 | ||
| P value | 0.11 | 0.76 | 0.67 | 0.005 | 0.46 | ||
| Young | Rapid | 5 | 88.67b | 5.38b | 0.71 | 4.54a | 0.70 |
| Control | 5 | 92.82a | 3.95c | 0.14 | 2.11b | 0.99 | |
| Old | Rapid | 5 | 88.65b | 5.93b | 0.81 | 2.33b | 2.29 |
| Control | 5 | 87.17b | 7.08a | 1.17 | 2.22b | 2.36 | |
| SEM | 0.845 | 0.443 | 0.252 | 0.471 | 0.235 | ||
| P value | 0.006 | 0.006 | 0.07 | 0.039 | 0.64 | ||
Means in a column followed by different letters differ significantly (P < 0.05).
Flock age: young = 28 wk, old = 64 wk.
Cooling profile: rapid = eggshell temperature (EST) cooled to 24°C within 45 min; control= EST cooled to 24°C within 6 h.
There were 5 replicate trays of 150 eggs (750 eggs) set per subgroup.
Cull is the second-grade chick percentage.
According to Meir and Ar (1998) and Reijrink et al. (2009), on the collection day, embryos at the pregastrula stage (<EGK10) are sensitive to prolonged egg storage. In the present study, although the eggs were stored for a short period (6 d), this might be true for the young flock, where the average developmental stage was EGK9.92 (47% of the embryos were below EGK10 after egg cooling), with reduced hatchability as a result of cooling the EST to 24°C within 45 min after oviposition. Embryos at the pregastrula stage might be advanced to a stage that is more resistant to storage or to an early period of incubation by heating eggs before or during storage (Güçbilmez et al., 2013; Özlü et al., 2021).
In the current study, rapid cooling after oviposition reduced early embryonic mortality and numerically increased hatchability in old flock eggs. This might be due to maintaining albumen quality (Thompson et al., 2000) and controlling embryo development. This finding was consistent with the findings of previous studies that used a plastic rather than cardboard egg tray and significantly increased fertile hatchability in eggs from older but not younger flocks (Dişa et al., 2015) or prime flocks (Uysal et al., 2008) due to faster egg cooling.
In the present study, the second-grade chick percentage did not differ significantly between the rapid and control cooling treatments, with averages of 1.50 and 1.67%, respectively (Table 2). However, the number of second-grade chicks from eggs from the young flock was lower than that from eggs from the old flock (0.85 vs. 2.33%) (P < 0.001). This was in agreement with the studies by Ipek and Sozcu (2015) and Özlü et al. (2021), who found that the second-grade chick percentage was significantly higher in older flock eggs than in young flock eggs.
Hatch Time
In the current study, flock age had no influence on hatch time, but hatch time was affected by the cooling treatment (Table 3). The average hatch time of chicks was delayed by 3 h by rapid cooling (486.2 vs. 489.2 ± 0.43 h) after oviposition. In addition, the percentage of chicks hatched early or late differed between the cooling treatments. Rapid cooling decreased the percentage of early hatched chicks (P = 0.006) but increased the percentage of late hatched chicks (P = 0.001) compared to the control treatment at both flock ages. This can be explained by the fact that rapid cooling after oviposition (reducing EST to 24°C within 45 min) slows blastoderm development. These results are consistent with those reported by Bowling and Howarth (1981), which indicated that in eggs exposed to 2 temperature levels (21°C–24°C or 35°C) for 3, 6, or 12 h, the hatch time of the chicks was earlier in eggs exposed to 35°C for 6 and 12 h than in the other treatments.
Table 3.
Effect of flock age and cooling rate on hatching time.
| Flock age1 | Cooling2 | Hatching time3 |
|||
|---|---|---|---|---|---|
| Early | Mid | Late | Average | ||
| (% of chicks completing hatching) | (h) | ||||
| Young | 23.5 | 54.4b | 22.1a | 488.0 | |
| Old | 20.2 | 70.3a | 9.6b | 487.4 | |
| SEM | 2.63 | 2.34 | 1.10 | 0.43 | |
| Rapid | 15.9b | 63.4 | 20.7a | 489.2a | |
| Control | 27.8a | 61.3 | 11.0b | 486.2b | |
| SEM | 2.63 | 2.34 | 1.10 | 0.43 | |
| Young | Rapid | 18.3 | 52.2 | 29.5a | 489.7 |
| Control | 28.7 | 56.6 | 14.8b | 486.4 | |
| Old | Rapid | 13.5 | 74.6 | 12.0b | 488.7 |
| Control | 26.9 | 65.9 | 7.2c | 486.1 | |
| SEM | 3.72 | 3.30 | 1.55 | 0.61 | |
| P value | |||||
| Flock age | 0.387 | 0.001 | 0.001 | 0.312 | |
| Cooling | 0.006 | 0.530 | 0.001 | 0.001 | |
| Flock age × Cooling | 0.684 | 0.066 | 0.005 | 0.630 | |
Means or percentages in a column followed by different letters differ significantly (P < 0.05).
Flock age: young = 28 wk, old = 64 wk.
Cooling profile: rapid = eggshell temperature (EST) cooled to 24°C within 45 min; control = EST cooled to 24°C within 6 h.
Early hatching time was 468 to 480 h, mid hatching time was 481 to 492 h, and late hatching time was 493 to 510 h.
SEM for n = 5 baskets of 150 eggs per subtreatment.
In conclusion, the data from this study clearly demonstrated that rapid cooling after laying retarded the stage of blastoderm development and hatch time of the chicks in eggs from both young and old broiler breeder flocks. This was apparently detrimental for the young flock eggs as indicated by the higher early and late embryonic mortality but beneficial for the old flock eggs as indicated by the lower early embryonic mortality. The hatchability differences between young and old flock eggs induced by a rapid cooling rate might depend on the differences in embryonic development at oviposition.
ACKNOWLEDGMENTS
The excellent technical advice of Murray R. Bakst is gratefully acknowledged, and the authors are grateful for the practical advice given by Orhan Erkan (Erpilic Inc., Bolu, Türkiye) while conducting the experiment.
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.
Footnotes
The use of trade names in this publication does not imply endorsement of the products mentioned nor criticism of similar products not mentioned.
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