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Effect of Egg Turning Angle and Frequency During Incubation on Hatchability and Incidence of Unhatched Broiler Embryos with Head in the Small End of the Egg¹

O. Elibol^* and J. Brake^,2

^* Department of Animal Science, Faculty of Agriculture, University of Ankara, Turkey 06110; and Department of Poultry Science, College of Agriculture and Life Sciences, North Carolina State University, Raleigh 27695

² Corresponding author: jbrake{at}ncsu.edu

	ABSTRACT

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The effect of turning angle (from vertical) and the interaction with turning frequency during incubation on fertile hatchability, embryonic mortality, and the incidence of embryos with head in the small end of the egg (malpositioned) was studied in 2 experiments comprising 2 trials each to determine if a turning angle of less than 45° could be successful. Hatching eggs from commercial broiler breeder flocks from 55 to 61 wk of age were utilized, and turning was for 18 d. Eggs were subjected to turning angles of 35, 40, or 45°, with a turning frequency of 24 times daily (24x) in Experiment 1. Turning angle had no effect on fertile hatchability. However, the incidence of separately enumerated, malpositioned embryos was increased by the 35° angle, compared with both the 40 and 45° angles in Experiment 1. Eggs were subjected to turning angles (from vertical) of 35°, with a turning frequency of either 24x or 96x daily, or 45°, with 24x turning in the 2 trials of Experiment 2. Turning angle and frequency had no effect on fertile hatchability or embryonic mortality, but the incidence of separately enumerated, malpositioned embryos was increased by the 35° angle with 24x turning, compared with the 35° angle with 96x turning, and the 45° angle, with 24x turning, in Experiment 2. These data demonstrated that the incidence of malpositioned embryos was increased by a reduced turning angle, but that this effect was ameliorated by a concomitant increase in turning frequency.

Key Words: turning angle • turning frequency • hatchability • malposition • broiler hatching egg

	INTRODUCTION

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Optimum turning of eggs during incubation has been of interest since the first observations of the incubational behavior of the feral fowl were made. Turning has been reported to be essential for optimum development of the extraembryonic membranes (Eycleshymer, 1907: New, 1957; Robertson, 1961a; Deeming, 1989) and correct orientation of the embryo within the egg before hatching (Robertson, 1961b; Lundy, 1969). Early data from Byerly and Olsen (1931) demonstrated that 2 to 3.5% of fertile eggs possessed embryos with their heads in the small end of the egg, and North and Bell (1990) estimated that as many as 1 to 4% of all 18-d-old embryos were malpositioned in some manner. The common malposition of chick embryos, with the head in small end of the egg, has been suggested to be due to egg orientation (e.g., set upside down), "air hunger," insufficient turning frequency, improper turning angle (Byerly and Olsen, 1931, 1933; Robertson, 1961b; Landauer, 1967; Lundy, 1969; Wilson et al., 2003), lack of turning during the first week of incubation, and increased breeder flock age (Elibol and Brake, 2004).

Angle and frequency have both been characterized as important aspects of incubational turning. Funk and Forward (1953) turned eggs at angles of 20, 30, 40, and 45° from vertical and reported increasing fertile hatchability with increased turning angle, although the difference between 40 and 45° was small. Wilson (1991) stated in a review that eggs set in the small-end-down position should be subjected to turning angles of 45 to 70° from vertical, and Funk and Forward (1960) investigated turning angles of 30, 45, 60, and 75° from vertical and found that 45° produced the best results. Optimum turning frequency has been demonstrated to be 96 times daily (96x;Wilson, 1991; Elibol and Brake, 2003), although 24 times daily (24x) has been accepted as the most practical under commercial circumstances, due to the relatively small differences between 24x and 96x (Freeman and Vince, 1974). Both Lundy (1969) and Wilson (1991) stated that high-quality hatching eggs were less sensitive to less-than-adequate turning than low-quality hatching eggs, possibly due to differences in albumen and shell quality that may be related to flock age or storage conditions (for a review, see Brake et al., 1997).

The ability to utilize a reduced turning angle during incubation could provide the opportunity to increase incubator capacity, alter airflow, improve the ability to deal with very large eggs in commercial machines, and reduce incubation costs per chick. French (1997) reported that increasing the distance between trays by reducing the turning angle could result in an exponential decline in the required air speed in commercial incubators. Lundy (1969) stated that although much was known about the turning (e.g., angle, frequency, position) of hatching eggs, little was known about the interaction of these factors. The objective of the present research was to determine the effect of incubation turning angle and the interaction with turning frequency on fertile hatchability, embryonic mortality, and the incidence of 1 common type (head in the small end of the egg) of malpositioned embryo known to be sensitive to these factors in eggs from older broiler breeder flocks. Our hypothesis was that aberrations in embryo development, as evidenced by an increased incidence of malpositioned embryos, could be induced by a reduced turning angle in eggs from older broiler breeder flocks and then ameliorated by a concomitant increase in turning frequency.

	MATERIALS AND METHODS

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Experiment 1
Hatching eggs were obtained from commercial flocks that had Ross 344 males mated to Ross 308 slow-feathering females at 55 and 57 wk of age in 2 trials. Eggs had been collected 4 times daily and stored for 2 d at 18°C and 75% RH before use. Eggs were set the same day that they were removed from the commercial hatchery cool room in such a manner as to prevent eggs from being set in the upside-down (small end up) position. Any abnormally shaped eggs were eliminated. A total of 1,500 eggs were placed in thirty 50-egg trays and set in 3 Çimuka (Çimuka, Ankara, Turkey) laboratory incubators previously determined to operate in a similar manner. The turning angle for the 10 trays in each of the 3 incubators was precisely set at 35, 40, or 45° from vertical in each trial. Incubators were operated at 37.4°C dry-bulb and 28.9°C wet-bulb temperatures for the first 18 d of incubation. The conditions were then changed to 37.2°C dry-bulb and 30.0°C wet-bulb temperatures to 19 d of incubation. The wet-bulb temperature was then increased to 31.1 and 32.2°C on 20 and 21 d of incubation, respectively. Machines were monitored 4 times daily for proper operation. Eggs were turned 24x and were hatched in the same machines by transfer to fixed hatching baskets. Correct positioning of eggs (small end down) was confirmed by candling at transfer, but all eggs were transferred, rather than removing the eggs that had been marked as being infertile or containing early dead embryos, to maintain similar ventilation among the trays and avoid this potential confounding factor during hatching. The various turning treatments were rotated to another machine between trials.

Experiment 2
Hatching eggs were obtained from commercial flocks of the same strain, company, and management at 57 and 61 wk of age in 2 additional trials. Experimental details were as for Experiment 1, with the following exceptions. A total of 1,500 eggs were placed in thirty 50-egg trays and distributed among 3 laboratory incubators. The 2 machines with eggs at an angle of 35° were turned either 24x or 96x daily, whereas eggs in the 45° machine were turned 24x daily. The various turning treatments were rotated to another machine between trials.

Hatching and Embryo Classification
After hatching was completed at 510 h, a single experienced individual examined all unhatched eggs macroscopically. Unhatched eggs were classified as either fertile or infertile. Fertile eggs were then further classified as early dead (0 to 7 d), middle dead (8 to 17 d), or late dead (18 to 21 d plus pipped eggs) that possessed embryos with their heads away from the large end of the egg, generally in the small end of the egg. A very specific and laborious classification of all embryos by a classic type of malposition (Buhr, 1989; Wilson et al., 2003) was not necessary for the purposes of this investigation and was therefore not attempted. The embryos that were positioned with their heads in the small ends of the eggs were recorded as being malpositioned separately from the remaining late-dead embryos. Hatchability of fertile eggs set (fertile hatchability) was calculated based upon the number of fertile eggs in each tray.

Statistical Analyses
Each tray of 50 eggs was considered to be a replicate for each turning or turning plus frequency treatment, so that there were 10 replicates per incubation treatment in each of the 2 trials in each experiment. Data from the completely randomized designs were subjected to ANOVA using the GLM procedure of SAS (SAS Institute, 1996). Initial analyses showed no significant treatment by trial interactions, so the data from each experiment were analyzed a final time with trial as a block. Differences among means were partitioned by the Duncan option (SAS Institute, 1996). Statements of statistical significance were based upon P < 0.05, unless otherwise indicated.

	RESULTS

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Fertility did not differ among the treatments in either experiment (Tables 1 and 2). Fertile hatchability, embryonic mortality, contaminated eggs, and malpositioned embryos from Experiment 1 are shown in Table 1. Turning angle with 24x turning had no overall effect on fertile hatchability, even though the incidence of early-dead embryos was reduced by the 40° angle compared with the 35° angle; the incidence in the 45°-angle group was intermediate. The incidence of malpositioned embryos was increased (P < 0.01) by the 35° angle compared with the 40 and 45° angles in Experiment 1.

	DISCUSSION

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These experiments were not intended to deal with the causes of the various classic types of embryonic malpositions, as reviewed and detailed by other recent studies (Buhr, 1989; Wilson et al., 2003). The present approach was to utilize observations of an obvious malposition (head away from the large end of the egg, in most cases malposition II: head in small end of the egg) that has been shown to be sensitive to turning deficiencies, as a means to determine the feasibility of compensating for a reduced turning angle with increased turning frequency. The choice of this particular class of malposition was obvious because Landauer (1967) noted that many malpositions could be variations of normal stages of development or simply cessation of development at some normal position when the embryo died. However, malposition II was considered to be different by Landauer (1967), in that embryonic position deviations as early as 4 to 6 d of incubation could be directly related to the development of malposition II (Taylor, 1932; Cavers and Hutt, 1934). This particular malposition has been most often associated with eggs set upside down, which did not occur in the present study, so that these experiments were a good bioassay of the adequacy of turning. Although embryos with their heads in the small ends of the eggs can generally be considered to be malposition II, there could be some confusion with other types of malposition in a limited number of eggs in the present study, but this was judged to be at a relatively low frequency that would not interfere with the basic conclusions of the present work. In any case, all studies have reported a certain "background" of malpositioned embryos, even under normal incubation conditions (Buhr, 1989; Wilson et al., 2003), and the present studies reflected that principle, with less than 0.4% malpositions appearing in the 45° (24x) turning groups, considered to be the control treatment in these studies. It was also important that in both experiments a turning angle of 35 vs. 45° with 24x daily turning produced an increased percentage of malpositions that was reduced significantly by an increased turning frequency but not by a 5° increase in angle. Statistical differences for fertile hatchability were probably not attained due to the non-treatment-related random variation in the other types of embryonic mortality (e.g., the unexplained significant effect on early-dead embryos in Experiment 1).

Elibol and Brake (2004) found an increase in malpositioned embryos (primarily head in small end of the egg), with a complete absence of turning during the first, but not second, week of incubation. The absence of turning during the first week also elevated all classes of embryonic mortality as compared with the lack of effect on embryonic mortality other than that associated with malpositioned embryos in the present study. Interestingly, Buhr (1989) previously reported that tilting during the first week of incubation (turning to an angle but immediately returning to the original position) was very detrimental to hatchability and elevated the incidence of malposition II as well. These data would seem to support findings of early studies that demonstrated that hatching position could be established early during incubation (Taylor, 1932; Cavers and Hutt, 1934), with turning certainly playing a major role. Furthermore, the data of Buhr (1989) indicated that the egg must remain in the turned position for some minimum period in order for the requisite development to occur (i.e., it is not enough to simply change the position of the egg for a very short period). The data of the current study suggested that a combination of reduced turning angle and increased turning frequency, rather than the classic hourly turning at 45°, could meet the requirements for positioning of the chicken embryo.

The data of the present study also succinctly addressed the statement in the review of Lundy (1969) that, although much was known about the turning (e.g., angle, frequency, position) of hatching eggs, little was known about the interaction among these factors. In the present experiments, the incidence of malpositioned embryos was increased by a reduced turning angle and then corrected by a concomitant increase in turning frequency. These data demonstrated that a reduced turning angle may be utilized commercially for purposes such as increasing incubator capacity or improving airflow if the turning frequency was concomitantly increased. Further, our personal observations suggested that a turning angle of less than 45° might often be encountered in commercial incubators. The present data suggest that small deviations could numerically increase the incidence of malpositioned embryos in certain cases (e.g., Table 1).

	ACKNOWLEDGMENTS

 
Financial support for this project was provided by the University of Ankara (project no. 2003.07.11.068 [EC] ).

	FOOTNOTES

 
¹ The use of trade names in this publication does not imply endorsement of the products mentioned nor criticism of similar products not mentioned.

Received for publication December 28, 2005. Accepted for publication May 20, 2006.

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