Internal Egg Temperature in Response to Preincubation Warming in Broiler Breeder and Turkey Eggs

2006 Poultry Science Association, Inc. Internal Egg Temperature in Response to Preincubation Warming in Broiler Breeder and Turkey Eggs R. A. Renema, J. J. R. Feddes, 1 K. L. Schmid, M. A. Ford, and A. R. Kolk Department of Agricultural, Food, and Nutritional Science, University of Alberta, Edmonton, AB, Canada T6G 2P5 Primary Audience: Broiler Flock Managers, Researchers, Field Service Technicians, Hatchery Personnel SUMMARY Various methods of preincubation warming have been used in commercial hatcheries to increase hatchability, decrease incubation time, and increase embryonic blastoderm development. A study was conducted to determine the effect of preincubation warming and egg size on the warming rate of eggs. Three egg groupings were evaluated: small broiler breeder eggs (52 to 57 g), large broiler breeder eggs (64 to 69 g), and turkey eggs (74 to 107 g). The eggs were subjected to 2 temperature treatments. The conventionally incubated eggs were moved directly from storage (17.5 C) to the incubator (adjusted to 37.5 C). The preincubation warmed eggs were moved from the storage room to the preincubation room (28 C) for 12 h and then to the incubator. Internal egg temperature was measured once per minute to calculate the rate of warming. The warming rate potential (k value) differed for egg type and temperature treatment. The values for small and large broiler breeder eggs and turkey eggs were 0.0506, 0.0488, and 0.0471 kj/min per kj of energy in the egg, respectively. This study characterizes the maximum rate of temperature change that occurs when eggs are transferred from a storage or preincubation area to the incubator, creating baseline values for future work with the modification of hatchery management protocols. These data can contribute to more informed decisions regarding hatchery temperature profile strategies and their effect on the developing embryo. Key words: preincubation warming, warming rate, egg size DESCRIPTION OF PROBLEM In the hatching egg industry, eggs are stored in the breeder barn until transport to the hatchery occurs and at the hatchery until space becomes available in the incubators. Eggs are stored below the minimum temperature for embryonic development [1]. This temperature has been reported to be 28 C by Funk and Biellier [2] and more recently 20 to 21 C [1]. 2006 J. Appl. Poult. Res. 15:1 8 Preincubation warming is the warming of eggs prior to placement in the incubator. During prolonged storage, the periodic or intermittent warming of eggs can improve hatchability particularly for birds that have a low rate of hatchability [3, 4]. Recommended storage temperatures are lower for storage periods of greater than 7 d [6]. However, little benefit has been reported for storage periods of less than 14 d [5, 6, 7, 8]. By decreasing the storage temperature 1 Corresponding author: john.feddes@ualberta.ca

2 JAPR: Research Report further below physiological zero, any disproportionate development of embryo tissues is slowed [8]. Hen age can modulate the impact of temperature changes on the embryo. Meijerhof et al. [9] suggested that older birds tend to lay eggs with fewer viable embryos that have an increased sensitivity to temperature and a reduced ability to withstand storage. Ultimately, preincubation warming methods are most beneficial to birds with poor rates of hatchability [4], embryos subjected to long-term preincubation storage [5], and when lower storage temperatures are used [6]. When eggs are prewarmed, the temperature of their environment changes from below physiological zero to an environmental temperature where further development is possible. The intermittent preincubation warming during prolonged storage allows further proportional tissue development and increases hatchability [8]. Once these eggs are transferred to the incubator, the minimum temperature for development will not be the same for all embryonic tissues [10]. At the embryonic level, this means that it is beneficial to bring the eggs up to incubation temperature quickly to avoid abnormal growth and an increased likelihood of embryonic mortality. However, incubator design may limit the ability of the egg temperature to reach adequate levels at a reasonable rate. Preincubation warming just before transfer into the incubator can increase the basal egg temperature, possibly reducing the embryonic stress by reducing the period in which final warming occurs. The importance of providing the optimum temperature profile to achieve optimally incubated eggs cannot be discounted. Hen age should already be accounted for in incubation management, because eggs from younger hens require slightly different temperature and humidity levels than eggs from intermediate or old hens for optimal embryogenesis and hatchability [11]. There may be other differences due to variation in incubation needs among modern genetic lines. Vleck [12] suggested that domestic strains of birds are less tolerant of variability in the physical environment than are wild birds. Decuypere and Michels [8] follow this by noting that heavily selected broiler lines are the least tolerant of temperature variation when compared with other domestic strains. With many hatcheries moving from multistage incubation toward single-stage incubation, strain-specific incubation management is possible. To achieve an ideal incubation temperature profile for different sized eggs from different strains, there needs to be a basic understanding of temperature change within different egg sizes and types. Meijerhof and van Beek [13] described the influence of climatic conditions on the temperature development during warming or cooling of eggs through mathematical modeling. They predicted exponential temperature development during an imposed temperature change on the eggs. The rate of warming for an object can be calculated with Equation 1 [14] (T final T)/(T final T initial ) = e (ha/ρcv)t k = ha/ρcv Equation [1] Equation [2] The warming rate potential is described by the convection coefficient (h), egg area (A), egg density (ρ), egg specific heat capacity (c) and egg volume (v). The units of k are kilojoules per minute of warming per kilojoule of energy in the egg. Equations 1 and 2 can be combined into Equation 3 to express warming rate potential (k) as k = ln(t final T)/t Equation [3] The objective of this study was to determine if a difference exists between the rate of internal warming of eggs that are prewarmed prior to incubation and the warming rate of eggs set immediately upon removal from the cooler. The effect of egg size on the rate of warming was also of interest. MATERIALS AND METHODS Egg Source Sixty hatching eggs consisting of 20 small broiler breeder eggs (52 to 57 g), 20 large broiler breeder eggs (64 to 69 g), and 20 turkey eggs (74 to 107 g) were obtained for each of the 3 consecutive replicates of the trial. The small and large eggs were gathered from a 35-wk-old

RENEMA ET AL.: CHARACTERIZATION OF EGG WARMING 3 broiler breeder flock and the turkey eggs were obtained from a 41-wk-old turkey breeder flock. Fresh eggs were acquired for each replicate of the study and subjected to the experimental treatments within 2 d of being laid. Each egg was assigned a number according to tray position and weight. The eggs were placed in 2 separate 68-egg trays. Each tray contained 10 eggs from each type arranged in a sequence of small broiler breeder egg, large broiler breeder egg, and turkey egg in a repeating pattern resulting in an intermixed arrangement. With this arrangement, the temperature effects were assumed to be the same for each replication since flock production had progressed to a point where egg composition was much more stable than in very early lay. Temperature Measurement A 4-mm diameter hole was drilled into the top of each egg. A thermistor sensor [15] was inserted through the opening to a depth of 1.5 cm to ensure the tip was likely in the yolk. The thermistor was secured to the shell with hot glue. Each tray also contained a thermistor for measuring the ambient temperature. The thermistors were connected to a data acquisition module that transmitted the temperature data to a nearby laptop computer. Trays were placed inside the egg cooler (17.5 C) overnight to allow the internal egg temperature to equilibrate with ambient temperature. Tray 1 was then held at room temperature (28 C) for 12 h, while tray 2 remained in the egg cooler. After 12 h, trays 1 and 2 were placed in the incubator, and temperature measurements continued for both of these trays for another 48 h. The trays were placed in a 5,000 egg capacity incubator [16] adjusted to 37.5 C. The eggs remained in an upright position throughout the study. This aforementioned movement of trays created 3 warming treatments: storage to incubator (SI), storage to room (SR) and room to incubator (RI). Individual egg temperatures were recorded every min onto a spreadsheet by the laptop computer. The warming profiles of the eggs are shown in Figure 1 as a mean of all egg types. For each egg, temperature change per minute ( T/min), k value (kj/min per kj of egg energy; equation 3), and the time required to reach a stabilized temperature t amb were determined (Table 1). The elapsed time to reach a stabilized temperature was the time the mean of the egg temperatures first reached the ambient air temperature of the eggs. The k and T/min values were determined from the linear part of the egg-warming curve using equation 3. The k mass value was normalized for egg mass by dividing the k value by the egg mass and multiplying by 1,000 (Table 1). The experimental eggs were not placed adjacent to other treatment eggs, and no other eggs were placed in the incubator or storage area during the study. This allowed for maximal rates of heat exchange between the egg and its environment and avoided confounding by impeded airflow caused by egg placement. Data Analyses Each replicate of the trial was a 3 3 factorial design with 3 temperature treatments and 3 egg sizes. The 3 consecutive replicates were carried out for 1 wk. A 3-way ANOVA (egg type temperature treatment replicate) was conducted using the GLM procedures of SAS [17]. The experimental unit was the egg type or tray within each experimental replicate. The least significant difference procedure was used to separate means when significant differences were indicated. Significance was assumed at P 0.05. RESULTS AND DISCUSSION The warming characteristics for the 3 egg types and the 3 temperature profiles were determined (Table 1). Egg mass differed (P 0.05) among the 3 egg types (small broiler breeder, large broiler breeder, and turkey; Table 1). The egg types also differed in their T/min and k value characteristics, and the k mass value differed among the 3 egg types. The interaction of egg type by warming treatment was not significant. The value of t amb was not different for egg type. The T per minute and the k value showed no significant difference between the large broiler breeder and turkey eggs (Table 1). However, the k mass value differed among these egg types. As shown in Figure 2, in which a representative portion of the warming profile is presented for illustration, the warming profiles appear to be very similar. These results were unexpected as we had hypothesized that because larger eggs have a smaller surface area to volume ratio they would warm more slowly than smaller eggs. The

4 JAPR: Research Report Figure 1. Mean comparison of warming profiles between preincubation warming and conventional incubation for all 3 egg types. surface area (4πr 2 ) to volume ratio (1.33 πr 3 ) was determined mathematically for the egg types as 3/r where r is the radius of an equivalent circle to that of an egg [18]. The eggs were assumed to have a specific gravity similar to that of water (1 g /ml), because the specific gravity of an egg is between 1.066 and 1.094. The surface area to volume ratio was 1.3 for small eggs, 1.2 for large eggs, and 1.1 for turkey eggs. Although there was a difference in the surface area to volume ratio and an average weight difference of 22 g between the large broiler breeder and Table 1. Egg warming characteristics for 3 different egg types subjected to 3 different temperature treatments Time Egg Temperature to ambient weight change temperature k 2 3 k mass Source (g) ( C min 1 ) (t amb ) 1 (min) (kj min 1 kj) (kj min 1 kj 1 g 1,000) Egg type Small broiler breeder 4 54.22 c 0.204 a 210 0.0506 a 0.93 a Large broiler breeder 5 66.05 b 0.195 b 213 0.0488 b 0.74 b Turkey 6 87.74 a 0.190 b 218 0.0471 b 0.54 c SEM 0.56 0.0027 5 0.0007 0.03 Warming treatment Storage to incubator 7 0.295 a 196 b 0.0507 a Storage to room 8 0.132 c 309 a 0.0441 b Room to incubator 9 0.163 b 136 c 0.0517 a SEM 0.0027 5 0.0007 a c Means within a column and a source with no common superscripts significantly differ (P < 0.05). 1 Time to ambient temperature from the imposition of the temperature treatment (min). 2 Warming rate potential calculated from the linearly increasing portion of the warming rate profile. 3 k value normalized for egg mass. 4 Target range 52 to 57 g. 5 Target range 64 to 69 g. 6 Target range 74 to 107 g. 7 Moved from storage to incubator temperature (SI). 8 Moved from storage to room temperature (SR). 9 Moved from room to incubator temperature (RI).

RENEMA ET AL.: CHARACTERIZATION OF EGG WARMING 5 Figure 2. A sample response of egg type to temperature change from the room to incubator. turkey eggs, the warming behavior between these egg types expressed as a k value was similar; however, the warming behavior was different when expressed on a mass basis (k mass ; Table 1). This finding suggests that the mass rather than the surface area to volume ratio of the egg explained the difference in warming rate. The dynamics of temperature may be more apparent between egg types in a full incubator, where egg size and incubation tray design may affect airflow. Coleman et al. [19] previously indicated that egg mass and egg size are directly proportional to the amount of time required for an egg to reach ambient temperature. The T/min, t amb, and k values were different for the 3 temperature profiles: SI, SR, and RI (P 0.05) (Table 1). Figure 3 illustrates a portion of the warming profile of large broiler breeder eggs for each of the treatments. A difference was found in the warming rate between preincubation treated eggs (SR RI) and conventionally treated eggs (SI), for which it was shown that the 3 types of eggs in the preincubation warming treatment had a more gradual warming rate. The warming profile was found to be more gradual in the preincubation warming temperature treatment (Table 1; Figures 1 and 3) because of the lower temperature gradient between the storage and the preincubation room. These rooms were not heated with forced-air systems, which would virtually eliminate air movement in the immediate vicinity of the egg compared with those placed directly into the incubator. Consequently, the t amb value for conventionally warmed eggs (SI) was 196 min; the prewarmed eggs went from storage temperature to incubator temperature (SR t amb + RI t amb ) in 445 min. This was also reflected in the warming rate ( T/min). Eggs in the SI treatment warmed at a rate of 0.30 C per minute, which was significantly different from the SR warming rate (0.13 C/min) and the RI warming rate (0.16 C/min; Table 1). These differences are attributed to the difference in temperature between time of introduction to the treatment and reaching the new temperature. The k values determined in this study from the rates of warming were compared with the k values for eggs cooled in storage as previously determined [20]. Eggs that were partially exposed to moving air in the cooling trial had a k value of 0.0167 kj/min per kj of egg energy, whereas eggs enclosed with no air movement had a k value of 0.0023 kj/min per kj of egg energy. The values for the partially exposed eggs were exceeded by approximately 3 times in this trial (0.0506, small broiler breeder eggs; 0.0488, large broiler breeder eggs; and 0.0471 kj/min per kj of egg energy for turkey eggs). The lowdensity filling of the trays used in this warming trial allowed for a high degree of egg surface area

6 JAPR: Research Report Figure 3. A sample of initial temperature response of large broiler breeder eggs to 3 different temperature treatments. exposure to air movement within the incubator. This demonstrates that maximum rates of temperature change among the egg types and temperature treatments occurred. Full egg trays and incubators may result in a reduced rate of temperature change if airflow is hindered. For example, a range in embryo temperatures within the incubator can be related to both airflow and egg size. Although embryos of all sizes will die when their internal temperature reaches 48.5 C, larger eggs can reach this temperature earlier because of their greater production of metabolic heat [21]. The practical application for larger eggs may affect the efficiency of heat transfer between the air and the egg. Larger eggs will have less ability to lose heat per unit of mass as well as less surface area per unit of mass. Also, egg shape (narrowness or roundness of the egg) can affect hatchability by impeding embryo rotation late in incubation [22]. However, egg shape can also affect the shape and thickness of the air cell and influence airflow at the egg surface and between the eggs. Air velocity affects heat transfer, meaning that heat transfer can be partially inhibited if air velocity is limited [23]. Proudfoot and Hulan [24] indicated that it took approximately 1 h to raise the internal egg temperature from 16 to 38 C in a warming chamber. In the current study, the time to a completely stable, ambient temperature was measured, which explained some of the difference in times between these 2 studies. Figure 3 shows that the period of most rapid temperature change was quite comparable. Wilson [7] has suggested that prolonging the period the embryo spends between 27 and 35 C can result in disproportionate development of tissues. The treatments in the current study brought the eggs to a constant temperature near the bottom of this range (28 C) to allow a more uniform movement through this temperature range. Whereas a 26 C room temperature would have been more desirable for this study, this was difficult to achieve in the research hatchery. Under ideal incubator conditions, the process of bringing the egg up to incubation temperature would be quite rapid. Because variation in egg heating can occur due to efficiency of air movement and heat transfer to the egg, partially heating the eggs prior to transfer into the incubator could make this final heating phase more rapid. The current study provides background data that can contribute to more informed decisions regarding hatchery temperature profile strategies, such as rate of temperature change for bird strain, bird age, or egg size. The empirical values determined for warming rates of the 3 egg types could be used as a basis for further studies on optimal incubation conditions. Managers of multispecie hatcheries may benefit from the knowledge that turkey eggs

RENEMA ET AL.: CHARACTERIZATION OF EGG WARMING 7 have similar warming characteristics to large broiler breeder eggs. Although preincubation warming leads to a warming process that is overall more gradual, it may also ensure eggs do not need as much time in the incubator to fully initiate embryo development. It may at least create a more uniform initiation of embryonic development compared with what may result from direct transfer to an incubator with nonuniform CONCLUSIONS AND APPLICATIONS 1. Warming rate potentials for small broiler breeder eggs (52 to 57 g), large broiler breeder eggs (64 to 69 g), and turkey eggs (74 to 107 g) were 0.0506, 0.0488, and 0.0471 kj/min per kj of energy potentially stored in the egg under ideal incubator conditions. 2. Increased egg size was assumed to decrease warming rate. This hypothesis was true for small broiler breeder and large broiler breeder eggs; however, turkey eggs were much like broiler breeder large eggs, even though turkey eggs are much larger. Strain or egg type may influence the development of optimal heating profiles. 3. Eggs that were transferred directly from storage to incubator warmed at a rate of 0.30 C/min, whereas the prewarmed eggs warmed at rates of 0.13 C and 0.16 C/min for the storage to room and room to incubator treatments, respectively. However, by prewarming the eggs, the time to reach the ambient incubator temperature was 60 min less (136 min) for eggs transferred from room to incubator compared with those transferred directly from storage to the incubator (196 min). This finding has application in the comparison of efficiencies of incubator performance and egg warming rate. 1. Proudfoot, F. G., and H. W. Hulan. 1982. Care of hatching eggs before incubation. Publication 1573/E. Commun. Branch, Agric. Canada, Ottawa, ON, Canada. 2. Funk, E. M., and H. V. Biellier. 1944. The minimum temperature for embryonic development in the domestic fowl (Gallus domesticus). Poult. Sci. 23:538 540. 3. Kosin, I. L. 1956. Studies on the pre-incubation warming of chicken and turkey eggs. Poult. Sci. 35:1384 1392. 4. Becker, W. A., and G. E. Bearse. 1958. Pre-incubation warming and hatchability of chicken eggs. Poult. Sci. 37:944 948. 5. Proudfoot, F. G. 1966. Hatchability of stored chicken eggs as affected by daily turning during storage and pre-warming and vacuuming eggs enclosed in plastic with nitrogen. Can. J. Anim. Sci. 46:47 50. 6. Mayes, F. J., and M. A. Takeballi. 1984. Storage of the eggs of the fowl (Gallus domesticus) before incubation: A review. World s Poult. Sci. J. 40:131 140. 7. Wilson, H. R. 1991. Physiological requirements of the developing embryo: temperature and turning. Pages 145 156 in Avian Incubation. S. G. Tullett, ed. Butterworths, London, UK. 8. Decuypere, E., and H. Michels. 1992. Incubation temperature as a management tool: A review. World s Poult. Sci. J. 48:28 38. 9. Meijerhof, R., J. P. T. M. Noordhuizen, and F. R. Leenstra. 1994. Influence of pre-incubation treatment on hatching results of REFERENCES AND NOTES heat transfer conditions. By bringing eggs up to a temperature just below that where differential tissue development begins [7], the time to final temperature is reduced (Table 1), which may somewhat compensate for inconsistencies in the rate of heating. Special cases, such as the thinner-shelled eggs from older birds may require a different rate of temperature change to ensure viable embryonic development. broiler breeder eggs produced at 37 and 59 weeks of age. Br. Poult. Sci. 35:249 257. 10. Kaufman, L. 1948. The effect of certain thermic factors on the morphagenesis of fowl embryos. Proc. 8th World s Poult. Congr., Copenhagen, Denmark 1:351 355. 11. Peebles, E. D., M. R. Burnham, C. W. Gardner, J. Brake, J. J. Bruzual, and P. D. Gerard. 2001. Effect of incubational humidity and hen age on embryo composition in broiler hatching eggs from young breeders. Poult. Sci. 80:1299 1304. 12. Vleck, C. M. 1991. Allometric scaling in avian embryonic development. Pages 39-57 in Avian Incubation. S. G. Tullett, ed., Butterworths, London, UK. 13. Meijerhof, R., and G. van Beek. 1993. Mathematical modeling of temperature and moisture loss of hatching eggs. J. Theor. Biol. 165:27 41. 14. Karlekar, V. K., and R. M. Desmond. 1977. Engineering Heat Transfer. West Publ. Co., New York, NY. 15. Onset Computer Corporation, Bourne, MA. 16. Jamesway Incubator Co. Inc., Cambridge, ON, Canada. 17. SAS Institute. 1999. The SAS System for Windows, NT. Version 8.0. SAS Institute, Cary, NC. 18. Protter, M. H., and C. B. Morrrey. 1963. Calculus with Analytical Geometry. Addison-Wesley Publ. Co. Inc., Reading, MA.

8 JAPR: Research Report 19. Coleman, J. W., H. S. Siegel, and G. F. Krause. 1964. Initial internal temperature changes of incubating eggs. Poult. Sci. 43:205 208. 20. Feddes, J. J. R., F. E. Robinson, W. Korver, B. Koberstein, and L. D. Watson. 1993. Internal cooling rates of stored eggs: Effects of packing and egg size. J. Appl. Poult. Res. 2:324 329. 21. Ono, H., P. C. L. Hov, and H. Tazawa. 1994. Responses of the developing chicken embryo to acute changes in ambient temperatures: Noninvasive study of heart rate. Isr. J. Zool. 40:467 480. 22. Narvuslim, V. G., and M. N. Romanov. 2002. Egg physical characteristics and hatchability. World s Poult. Sci. J. 58:297 303. 23. Meijerhof, R. 2002. Principles and practice of incubator design. Pages 41 46 in Practical Aspects of Commercial Incubation in Poultry. D. C. Deeming, ed. Ratite Conf. Books, Oxford, UK. 24. Proudfoot, F. G., and H. W. Hulan. 1982. Effect of preincubation warming on the hatchability of hens eggs from normal and semidwarf parental genotypes. Can. J. Anim. Sci. 62:321 322. Acknowledgments The supply of eggs by G. Olson and Lilydale Hatchery and the invaluable assistance of the staff and students of the Alberta Poultry Research Centre are greatly appreciated.