Embryonic Malpositions in Broiler Chickens and Bobwhite Quail1

Embryonic Malpositions in Broiler Chickens and Bobwhite Quail1

2003 Poultry Science Association, Inc. Embryonic Malpositions in Broiler Chickens and Bobwhite Quail1 H. R. Wilson,2 S. L. Neuman,3 A. R. Eldred, an...

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2003 Poultry Science Association, Inc.

Embryonic Malpositions in Broiler Chickens and Bobwhite Quail1 H. R. Wilson,2 S. L. Neuman,3 A. R. Eldred, and F. B. Mather

Primary Audience: Hatchery Managers, Hatching Egg Producers, Researchers, Primary Breeders SUMMARY One of the factors contributing to failure of avian embryos to hatch is the positioning of the embryo at the end of incubation in such a manner that emergence from the egg is inhibited. Abnormal positions, or malpositions, may also be associated with other problems without directly affecting the ability of the chick to hatch. The effect of strain, breeder age, and gender of embryo on incidence of malpositions before hatching was determined in broiler embryos. The effect of strain, breeder age, pre-incubation egg storage, setting orientation, and turning during incubation on incidence of malpositions before hatching was determined in bobwhite quail embryos. Although there were variations among strains and between genders for incidence of malpositions, they were not statistically significant. Differences among settings and evaluators were as great as strain effects. No significant strain or breeder age effect on malposition incidence was found in quail. Long-term pre-incubation storage increased the incidence of quail embryos with head between the thighs, possibly related to delayed embryonic development. Setting quail eggs with the small end up resulted in 75% of the embryos with head in the small end of the egg. Eggs set normally but not turned had increased incidences of head in small end, beak away from air cell, and head over wing embryonic malpositions. Therefore, in these studies, the incidence of malpositions was affected by pre-incubation egg storage, egg orientation, and turning, whereas it was not affected by strain, embryo gender, and breeder age. Key words: chicken, embryo, hatchability, malposition, quail 2003 J. Appl. Poult. Res. 12:14–23

DESCRIPTION OF PROBLEM The avian embryo progresses through a series of positions throughout incubation and ends in a normal position for hatching. Just prior to the beginning of the hatching process, embryos of chickens and most domestic species move into a normal position within the egg, characterized by the long axis of the body being aligned 1

with the long axis of the egg. The head is curled forward and to the right with the beak tucked under the right wing and the tip of the beak pointed toward the air cell in the large end of the egg [1]. The legs are flexed and tucked against the abdominal wall with the abdomen (including the internalized yolk) between the thighs [2]. Early orientation of embryos has been reviewed by Romanoff [3]. The normal position

Florida Agricultural Experiment Station Journal Series Number R-08921. To whom correspondence should be addressed: [email protected] 3 Present address: Embrex, Inc., Research Triangle Park, NC 27709. 2

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Department of Animal Sciences, University of Florida, P.O. Box 110910, Gainesville, Florida 32611-0910

WILSON ET AL.: EMBRYONIC MALPOSITIONS

incidence of cull chicks among those that do hatch [17, 18]. Apparent strain differences have been observed in the incidence of malpositions when assessing hatchability problems in commercial broiler stocks [19]. Genetic effects have been reported in some studies [10, 20] but not in others [21]. The objective of the present studies was to establish a baseline incidence of embryonic malpositions in broiler chickens and bobwhite quail prior to hatch and to determine if differences in incidence of malpositions exist among strains examined.

MATERIALS AND METHODS Experiment 1 Eggs of two broiler strain crosses, Ross × Ross [22] and Ross × Arbor Acres [23], were obtained from a commercial hatchery that had a history of reduced hatchability. After eggs were received, they were held overnight at 70°F and then set in Jamesway 252 [24] incubators at 99.5°F and 61% relative humidity. Eggs from each strain were placed in alternating cradles on each incubator tray. The eggs were candled prior to setting to locate the air cell and assure placement of the eggs with air cell end up. Eggs were turned each hour around the small axis to about 45° until pipping. Beginning at 19 d of incubation (DOI), eggs that were pipped were removed from the incubator; embryos were euthanized via carbon dioxide asphyxiation and examined for embryonic position in the egg. Only eggs that pipped from 19 to 21 DOI were examined; those that survived to 19 DOI or later but did not pip were inadvertently lost. We examined 456 embryos for Ross × Ross and 451 embryos for Ross × Arbor Acres. Experiment 2 A second study was conducted to further establish a baseline of position incidence for all embryos prior to hatching. Eggs from Cobb × Cobb [25] broiler breeders were collected when the breeders were 45 and 50 wk of age. Eggs were stored large end up (LEU) at 55°F for up to 6 d after lay and then incubated as in experiment 1. The eggs were candled at 7 DOI, and infertile, dead, and air cell down eggs were removed. Beginning at 19 DOI, pipped eggs were

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changes that occur throughout development have been described by Kuo [4] and Freeman and Vince [5]. There are variations of the normal position that are considered to not be detrimental to successful hatching. However, there are many positions that are associated with difficulty in hatching or are found in increased incidence in cases of poor hatchability. These are termed malpositions. Six embryonic malpositions were described in early studies [e.g., 6, 7, 8, 9]. The following classifications of malpositions have been generally accepted [1]: I Head between thighs. II Head in small end of the egg (opposite air cell). III Head to left instead of right. IV Head in normal position but rotated with beak pointed away from air cell. V Feet over head. VI Beak (or head) over right wing. Many variations and combinations of these malpositions have been described [9, 10]. Malpositions V and VI were considered too minor by Byerly and Olsen [11] to be classed as abnormal. Waters [12] and Robertson [13] described the head between the legs, or thighs (I), as a transition position, normal at earlier stages and probably due in part to retarded development. It has been estimated that in commercial stocks 1 to 4% of all 18-d embryos will be malpositioned [14]. Examination of hatch residue in a commercial hatchery in Panama revealed that 49.9% of the unhatched embryos that were more than 18 d in incubation were malpositioned, which was 1.54% of all eggs set (81,025) [15]. The observed incidence for malpositions I through VI, respectively, were 9.5, 17.8, 6.6, 6.8, 17.5, and 41.8%. Tona et al. [16] observed an incidence of 83.5% embryonic malpositions in broiler embryos that had died at 18 d of incubation or later. They also reported that the incidence of malpositions decreased as breeder age increased to 42 wk and then increased thereafter. A major cause of malposition III, especially in broiler eggs, is setting eggs small end up (air cell down). In commercial hatcheries the incidence of misoriented eggs varies from 0.3 to 3.4% [17], and in addition, there is an increased

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16 examined for embryonic position. At 21 DOI, all remaining eggs were examined. The gonads of all embryos were exposed to determine gender. The number of embryos examined was 888 and 709 in the first and second setting of eggs, respectively. Experiment 3

Experiment 4 Broiler embryos from Ross males crossed with eight lines of Arbor Acres females were examined to further determine the effect of strain or line on incidence of malpositions. All lines were grown and maintained on the same farm under the same management, nutrition, and health regimens. Eggs were delivered by truck, held overnight at 70°F, and placed in NatureForm NMC 2000 [28] incubators the following day. Incubation was at 99.5°F and 58% relative humidity. Eggs were candled prior to setting, set air cell up, and turned hourly to approximately 45° angle. Eggs from each line were distributed equally between two incubators and

Experiment 5 Eggs of bobwhite quail, which normally hatch on 24 DOI, were incubated to 22 DOI, and embryos were examined to determine position in the egg. Eleven hundred eggs were placed air cell up on modified quail egg setter flats in a Jamesway 252 incubator at 100.0°F, 58% relative humidity, and turned hourly. Eggs were removed from the incubator upon pipping or no later than the end of 22 DOI, euthanized with carbon dioxide, and then examined for embryonic position in the egg. Embryos 21 DOI or older were included in the data set. Two other groups of eggs (180 each group) were also incubated, one set small end up and turned and the other set large end up and not turned. Embryos of these eggs were examined in the same manner as those set normally. Experiment 6 The effect of pre-incubation storage of bobwhite quail eggs on the incidence of embryonic malpositions was determined on eggs stored up to 6 wk. Eggs were collected daily from a flight strain of bobwhite and stored air cell up on quail egg flats at 55°F and approximately 80% relative humidity. Eggs were set on plastic quail egg setter flats in a NatureForm NMC 2000 incubator, and the same incubation and examination procedures were used as for the normally set eggs in experiment 5. Experiment 7 Embryos of bobwhite quail were examined to determine incidence of malpositions as affected by strain and breeder flock age. The strains were a small-to-moderate-sized flight strain and a large “jumbo” strain used for meat. Eggs were set from breeders of the jumbo and young flight strains at approximately 35, 46, and 50 wk of age. Eggs were set from the old flight strain at approximately 87, 98, and 102 wk of age. At each setting, eggs from young and old flight strains and the jumbo strain were distributed equally throughout the incubator to mini-

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Embryonated eggs of six strains or crosses of broiler breeders were examined to determine the effect of strain on incidence of embryonic malpositions. The eggs were obtained from a primary breeder when the breeder flocks were approximately 49 and 62 wk of age. The breeders were maintained under the same conditions of age, farm, management, and diet. The six strains were Arbor Acres Regular × Arbor Acres Classic, Arbor Acres Yieldmaster × Arbor Acres FSY (feather sex), Cobb × Cobb, Hubbard × Hubbard [26], Ross × Ross, and Avian Main × Avian 24 K [27]. The Hubbard × Hubbard strain was not included in the second setting. Three hundred sixty eggs of each strain were shipped by air resulting in about 300 intact eggs each for incubation. Eggs from each strain were placed on each incubator tray and incubated as in experiment 1. Eggs were candled at 10 DOI, and infertile, dead, broken, and air cell down eggs were removed. All remaining eggs were placed in carbon dioxide at 20 DOI to euthanize the embryos; eggs were then examined to determine embryonic position. Only embryos older than 18 DOI were included in the data set.

positions within incubators. At 20 DOI, all eggs were euthanized with carbon dioxide and examined for embryonic position. Only embryos older than 18 DOI were included in the data set.

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TABLE 1. Incidence of malpositions in pipped eggs of two commercial broiler strains (experiment 1) Ross × Ross PositionA Total Normal

Number

All (%)

Malpositions (%)

Number

All %

Malpositions (%)

456 375

— 82.2

— —

451 380

— 84.2

— —

79 0 0 1 3 2 73

17.3 0.0 0.0 0.2 0.7 0.4 16.0

100.0 0.0 0.0 1.3 3.8 2.5 92.4

71 0 0 0 0 1 70

15.7 0.0 0.0 0.0 0.0 0.2 15.5

100.0 0.0 0.0 0.0 0.0 1.4 98.6

A Total = total eggs examined; Normal = normally positioned embryos; Malpositions = malpositioned embryos: I = head between thighs, II = head in small end, III = head to left, IV = beak away from air cell, V = feet over head, and VI = beak over right wing. B Distribution of malposition incidence did not differ significantly between strains (P > 0.05).

mize possible placement effects. Incubation was in NatureForm NMC 2000 incubators at 100.0°F, 58% relative humidity, and with hourly turning. At 22 DOI the eggs were candled, live embryos euthanized with carbon dioxide, and each egg examined to determine embryonic position. Statistical Analysis The malposition incidence distributions were tested using chi-square analysis with significant differences accepted at P ≤ 0.05.

RESULTS AND DISCUSSION Experiment 1 The Ross × Ross embryos had 17.3% classified as malpositioned. The majority of these (92.4%) were malposition VI (head over right wing), whereas 3.8% were malposition IV (head away from air cell), 2.5% were malposition V (feet over head), and 1.3% were malposition III (head to left) (Table 1). Ross × Arbor Acres embryos had 15.7% malpositioned, 98.6% of which were malposition VI, and the remainder were malposition V. A strain effect is suggested; however, the difference was not significant (P < 0.10), and it could have been affected by the incidence of malpositions in the unexamined nonpipped eggs. Experiment 2 The incidence of malpositions for the 1,597 Cobb × Cobb embryos examined was 12.3%

with greater than 70% of those being VI (head over right wing) (Table 2). Malposition V (feet over head) was 14.8% in female embryos compared to 22.9% in males, whereas IV (beak rotated away from air cell) was 4.5% in females and 1.8% in males. All other malpositions accounted for about 5% of the total. There were no significant differences in malposition distributions between male and female embryos. Experiment 3 The pattern of malposition incidences was similar among the six broiler strains, and none of the crosses differed significantly from the average (Tables 3 and 4). A possible age effect occurred in that a higher incidence of malposition V occurred in the embryos from young breeder birds; however, it was only marginally significant (P < 0.10). Experiment 4 The incidences of embryonic malpositions I, II, III, and IV were relatively low across all eight lines of Arbor Acres and no significant line effects were found (Table 5). The number of embryos with head in the small end (II) was lower than in typical commercial settings because no eggs were set with air cell down; nevertheless, four lines had 1.0 or 1.4% of the embryos in that position. The incidence of malposition V (feet over head) ranged from 1.1 to 3.7% across lines with an average of 2.6%. Head over wing (malposition VI) was high in all lines (15.4%

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MalpositionedB I II III IV V VI

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TABLE 2. Incidence of malpositioned embryos in pipped eggs of Cobb × Cobb broiler eggs (experiment 2) Female PositionA Total Normal

Number

All (%)

Malpositions (%)

Number

All (%)

Malpositions (%)

781 693

— 88.7

— —

816 707

— 86.7

— —

88 1 2 2 4 13 66

11.3 0.1 0.2 0.2 0.5 1.7 8.4

100.0 1.1 2.3 2.3 4.5 14.8 75.0

109 1 0 4 2 25 77

13.3 0.1 0.0 0.5 0.2 3.1 9.4

100.0 0.9 0.0 3.7 1.8 22.9 70.6

A Total = total eggs examined; Normal = normally positioned embryos; Malpositions = malpositioned embryos: I = head between thighs, II = head in small end, III = head to left, IV = beak away from air cell, V = feet over head, and VI = beak over right wing. B Distribution of malposition incidence did not differ significantly between male and female embryos (P > 0.05).

average) with the highest incidences in lines 1 (19.8%), 4 (18.9%) and 8 (17.8%) or 63, 54, and 54% of all malpositions, respectively. The lowest incidence of malposition VI was in line 6 (11.8%); however, that was 55% of all malpositions. Two other positions were observed that could not be easily classified into malpositions I through VI. One position was the right leg turned or twisted to the left with the foot behind the head or ventral to the navel. This occurred in an average of 3.6% of the embryos, ranging from 7.0% in line 4 to 1.5% in line 6. The second position was “tucked wing tip” in which the tip of the right wing was tucked back toward the

shoulder, usually under the neck. The incidence ranged from 3.1 to 6.9% with an average of 5.1%. This position was often associated with other malpositions, and its effect, if any, on hatchability of the embryo is unknown. Experiment 5 The distribution of malpositions in quail embryos (Table 6) was similar to that observed in broiler strains in experiment 3. There was a relatively high incidence of malposition V (12.4%) and a higher incidence of malposition VI (14.0%). The incidence of malposition II (head in small end) was 1.1% even though the

TABLE 3. Incidence of malpositions in embryos at 19 d of incubation or more from six commercial broiler strains or crosses, 49 wk of age (experiment 3) Strain 1A PositionB Total Normal MalpositionsC I II III IV V VI

Strain 2

Strain 3

Strain 4

Strain 5

Strain 6

n

%

n

%

n

%

n

%

n

%

n

%

295

100 71

292

100 63

299

100 66

300

100 68

306

100 74

303

100 78

28 0 2 1

37 0 8 1

33 1 2 2

32 1 2 0

26 1 3 0

22 0 2 0

13 19

8 20

11 18

9 22

7 14

13 11

A Strains 1 to 6 were AA Regular × Classic; AA Yieldmaster × FSY; Cobb × Cobb; Hubbard × Hubbard; Ross × Ross; Avian Main × Avian 24K. B Total = total eggs examined; Normal = normally positioned embryos; Malpositions = malpositioned embryos: I = head between thighs, II = head in small end, III = head to left, IV = beak away from air cell, V = feet over head, and VI = beak over right wing. C Distribution of malposition incidence of each strain did not differ significantly from the average of all strains (P > 0.05).

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MalpositionedB I II III IV V VI

Male

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TABLE 4. Incidence of malpositions in embryos at 19 d of incubation or more from five commercial broiler strains or crosses, 62 wk of age (experiment 3) Strain 1A PositionB Total Normal

Strain 3

Strain 4

Strain 5

n

%

n

%

n

%

n

%

n

%

207 156

100.0 75.4

261 199

100.0 76.2

289 206

100.0 71.3

282 208

100.0 73.8

288 226

100.0 78.5

51 1 8 0 2 3 37

24.6 0.5 3.9 0.0 1.0 1.4 17.9

62 0 6 0 2 5 49

23.8 0.0 2.3 0.0 0.8 1.9 18.8

83 1 8 4 1 6 63

28.7 0.3 2.8 1.4 0.3 2.1 21.8

74 0 7 0 1 5 61

26.2 0.0 2.5 0.0 0.4 1.8 21.6

62 0 3 0 1 2 56

21.5 0.0 1.0 0.0 0.3 0.7 19.4

A Strains 1 to 5 were AA Regular × Classic; AA Yieldmaster × FSY; Cobb × Cobb; Ross × Ross; Avian Main × Avian 24K. B Total = total eggs examined; Normal = normally positioned embryos; Malpositions = malpositioned embryos: I = head between thighs, II = head in small end, III = head to left, IV = beak away from air cell, V = feet over head, VI = beak over right wing. C Distribution of malposition incidence of each strain did not differ significantly from that of the average of all strains (P > 0.05).

conical shape of quail eggs make the large and small ends obvious and unlikely to be set incorrectly. Setting eggs small end up resulted in a significantly higher incidence (75.5%) of head in small end embryos (malposition II) and an accompanying significant decrease in malpositions V and VI. However, embryos that were in malposition II as well as V or VI were only included in the II group.

Eggs set large end up but not turned had increased incidences of malpositions II, IV, and VI. Although the incidence of malposition I was low, it was increased by not turning the egg or by setting it small end up. Experiment 6 Pre-incubation storage of bobwhite eggs for up to 3 wk did not impact the incidence of em-

TABLE 5. Incidence of malpositions in embryos at 19 d of incubation or more from eight commercial broiler strains or crosses (experiment 4) PositionA Embryos (n)

Line 1B 298

Line 2

Line 3

Line 4

Line 5

Line 6

Line 7

Line 8

All lines

279

268

286

275

279

291

298

2,274

MalpositionsC (%) I II III IV V VI

0.0 1.0 0.0 0.0 1.3 19.8

0.7 0.4 0.7 0.0 1.1 14.0

0.4 0.0 0.4 0.4 4.1 14.2

0.0 0.7 0.0 0.0 3.2 18.9

0.0 1.4 0.4 0.0 2.2 13.8

0.4 0.7 0.0 0.0 2.9 11.8

0.0 1.4 0.0 0.0 2.8 12.7

0.0 1.0 0.3 0.0 3.7 17.8

0.2 0.8 0.2 <0.1 2.6 15.4

Other malpositionsC (%) Right foot to left, behind head or below navel Tucked wing tip All malpositions (%) Multiple malpositions (%)

3.4 6.0 31.5 3.7

2.2 5.0 24.0 1.4

2.6 4.1 26.1 3.0

7.0 5.6 35.3 6.3

2.6 6.9 27.3 2.5

1.5 4.3 21.5 1.1

4.8 3.1 24.7 2.8

4.7 5.7 33.2 4.0

3.6 5.1 28.1 3.1

A Embryos = embryos examined; Malpositions: I = head between thighs, II = head in small end, III = head to left, IV = beak away from air cell, V = feet over head, and VI = beak over right wing. B Lines were Ross male × various Arbor Acres FSY lines. C Distribution of malposition incidence of each line did not differ from the average of all lines (P > 0.05).

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MalpositionsC I II III IV V VI

Strain 2

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TABLE 6. Incidence of embryonic malpositions in eggs of bobwhite quail set normally, unturned, or small end up (experiment 5) PositionA

Small end up

Large end upnot turned

774 72.0

135 17.8

128 38.0

28.0 0.4 1.1 0.1 0.0 12.4 14.0

85.6 1.5 75.5 0.0 0.0 4.7 3.9

59.2 1.6 6.0 0.0 7.0 8.6 36.0

All embryos (n) Normal (%) MalpositionsB (%) I II III IV V VI

A All embryos = total embryos examined; Normal = normally positioned embryos; Malpositions = malpositioned embryos: I = head between thighs, II = head in small end, III = head to left, IV = beak away from air cell, V = feet over head, and VI = beak over right wing. B Distribution of malposition incidence in eggs set small end up and large end up—not turned differed significantly from that of eggs set large end up and turned (P ≤ 0.05).

bryonic malpositions (Table 7). Overall incidence of malpositions was low in comparison to experiment 5, especially positions V and VI. However, the incidence of malposition I was higher with eggs stored 4 wk having 9.5% of the embryos with malposition I, whereas the incidence increased to 23.9% in eggs stored 5 or 6 wk. The increase in malposition I may reflect the delaying effect of prolonged egg storage on embryonic development [13, 29], which is consistent with the negative effects of long-term storage on hatchability of quail eggs [30].

Experiment 7 Neither strain (flight or jumbo) nor breeder flock age (young: 35, 46, and 50 wk; old: 87, 98, and 102 wk) significantly altered the incidence of malpositions in bobwhite embryos (Table 8). Overall, malpositions were relatively low: 6.6, 5.5, 8.7, and 5.3% for young flight, old flight, young jumbo, and old jumbo, respectively. Most of the observed malpositions were classified as head over the right wing (VI). Many factors have been shown to affect the incidence of embryonic malpositions including

TABLE 7. Incidence of embryonic malpositions of bobwhite quail embryos in eggs stored 1 to 6 wk (experiment 6) Pre-incubation storage time (wk) Position

A

1

2

3

4

5–6

732 91.4

969 94.1

1,009 92.8

1,092 88.6

180 72.2

MalpositionsB (%) I II III IV V VI

8.6 5.7 0.0 0.7 0.0 0.0 2.2

5.9 4.4 0.0 0.3 0.0 0.0 1.2

7.2 5.0 0.0 0.6 0.0 0.0 1.6

11.4 9.5 0.0 0.4 0.0 0.0 1.5

27.8 23.9 0.0 1.1 0.0 0.0 2.8

Pipped (%) Yolk internalized (%)

2.4 1.5

2.0 1.3

0.7 0.4

0.1 0.0

0.0 0.0

All embryos (n) Normal (%)

A All embryos = total embryos examined; Normal = normally positioned embryos; Malpositions = malpositioned embryos: I = head between thighs, II = head in small end, III = head to left, IV = beak away from air cell, V = feet over head, and VI = beak over right wing. B Distribution of malposition incidence in eggs stored 5 to 6 wk differed significantly from those stored 1 wk (P ≤ 0.05).

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Large end up

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TABLE 8. Incidence of embryonic malpositions in eggs of two strains and agesA of bobwhite quail (experiment 7) PositionB

Old flight

Young jumbo

Old jumbo

Total embryos (n) Normal (%)

49 93.9

307 94.5

69 91.3

150 94.7

MalpositionsC (%) I II III IV V VI

6.1 2.0 0.0 0.0 0.0 0.0 4.1

5.5 0.0 0.0 0.0 0.0 0.0 5.5

8.7 1.4 0.0 0.0 0.0 0.0 7.2

5.3 1.3 0.0 0.0 1.3 0.0 2.7

A

Young breeders were 35, 46, and 50 wk of age; old breeders were 87, 98, and 102 wk of age. Total embryos = total embryos examined; Normal = normally positioned embryos; Malpositions = malpositioned embryos: I = head between thighs, II = head in small end, III = head to left, IV = beak away from air cell, V = feet over head, and VI = beak over right wing. C Distribution of malposition incidence in eggs did not significantly differ due to strain or age of breeders (P > 0.05). B

egg orientation and turning frequency [13, 31, 32], tilting instead of turning the egg [33], plane of turning [34], and related factors [1, 35, 36]. However, others [37] found no effect due to turning frequency or due to turning or lack of turning during the third week of incubation [31]. The incidence of malpositions in quail eggs in the present study was not significantly influenced by breeder age, although an age effect has been observed in commercial broiler eggs [16]. Egg size and shape are influenced by breeder age, and the incidence of malpositions is increased in large eggs [38] and with abnormal orientation of the early embryo [39], which is in turn influenced by egg shape [40, 41]. A breeder age effect on incidence of malpositions has been observed in chickens [21]. The incidence of malpositions has been reported to be affected by nutritional factors such as dietary protein [20], vitamin A deficiency [42], and vitamin B12 deficiency [43], whereas others [44] report no influence due to allowance of dietary protein or energy. Genetic strains and lines did not have significant effects on the incidence of malpositions in these studies, which is in agreement with one study [21] in which genetics was not an influencing factor but was not in agreement with others which reported a genetic

effect [10, 20]. Gender of the embryo did not affect incidence of malpositions in quail, which is similar to results reported for chicken-pheasant hybrid embryos [45]. Data from the present studies and previous reports indicate that genetic strains or lines and embryo gender are not major factors influencing the incidence of embryonic malpositions. Factors such as egg handling, egg orientation and turning, incubation conditions, and breeder nutrition are likely to be more important. The high incidence of malposition VI (head over right wing) in these studies might have been influenced by the eggs being maintained in the setter at setter temperature until removal for examination. However, Waters [12] reported that the incidence of VI increased after 18 DOI in a manner parallel to and essentially equal with the increase in normally positioned embryos. The high incidence of malposition VI may simply reflect a normal variant position as suggested by others [9, 11, 12]. Although a high incidence of embryonic malpositions is often observed in situations of low hatchability, with all of the known influencing factors and potential for interactions among them, malpositions will not usually be definitive in identifying the cause of embryonic losses.

CONCLUSIONS AND APPLICATIONS 1. A background level of embryonic malpositions was observed in broiler and bobwhite quail eggs. 2. The incidence of embryonic malpositions was not significantly different due to gender of the embryo or to broiler strains (lines); thus, these factors are not major causes of malpositions.

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Young flight

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REFERENCES AND NOTES 1. Landauer, W. 1967. The hatchability of chicken eggs as influenced by environment and heredity. Storrs Agric. Exp. Sta. Monograph 1 (rev.). University of Connecticut, Storrs, CT. 2. Orlov, M. V. 1962. Biological principles of incubation. Pages 244–323 in Poultry Science and Practice. Vol. 2. Translated and published (1969) by Israel Program for Scientific Translations Ltd. in cooperation with USDA and National Science Foundation, Washington, DC.

16. Tona, K., F. Bamelis, W. Coucke, V. Bruggeman, and E. Decuypere. 2001. Relationship between broiler breeder’s age and egg weight loss and embryonic mortality during incubation in largescale conditions. J. Appl. Poult. Res. 10:221–227. 17. Bauer, F., S. G. Tullett, and H. R. Wilson. 1990. Effects of setting eggs small end up on hatchability and posthatching performance of broilers. Br. Poult. Sci. 31:715–724.

3. Romanoff, A. L. 1960. Structural and functional development. Pages 141–143 in The Avian Embryo. The Macmillan Co., New York.

18. Fasenko, G. M., F. E. Robinson, S. W. Chapman, and J. R. Higgins. 2000. Determining the hatchability of broiler chicks from eggs set small end up versus eggs set large end up. Poult. Sci. 79(Suppl. 1):3–4. (Abstr.)

4. Kuo, Z. Y. 1932. Ontogeny of embryonic behavior in Aves. II. The mechanical factors in the various stages leading to hatching. J. Exp. Zool. 62:453–487.

19. Wilson, H. R. 1985. University of Florida, Gainesville, FL. Unpublished data.

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7. Hutt, F. B. 1929. Studies in embryonic mortality in the fowl. I. The frequencies of various malpositions of the chick embryo and their significance. Proc. R. Soc. Edinburgh 49:118–131.

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3. Strain and breeder age did not significantly affect the incidence of embryonic malpositions in quail. 4. Long-term pre-incubation storage of quail eggs increased the incidence of embryos with head between the thighs (I), possibly associated with delayed embryonic development. 5. Setting quail eggs with small end up resulted in 75% of the embryos with head in the small end. 6. Not turning quail eggs set with air cell up resulted in increases in head in small end (II), beak away from air cell (IV), and head over right wing (VI) malpositions. 7. The most commonly observed malposition in both broiler and quail embryos was head over right wing (VI). 8. Although higher incidence of malpositions is often associated with low hatchability, while malposition may be a contributing factor, it is not usually definitive of the cause.

WILSON ET AL.: EMBRYONIC MALPOSITIONS 35. Lundy, H. 1969. A review of the effects of temperature, humidity, turning and gaseous environment in the incubator on the hatchability of the hen’s egg. The Fertility and Hatchability of the Hen’s Egg. T. C. Carter and B. M. Freeman, ed. Br. Egg Marketing Board Symp. 5. Oliver and Boyd, Edinburgh, UK. 36. Wilson, H. R. 1991. Physiological requirements of the developing embryo: Temperature and turning. Avian Incubation: Poult. Sci. Symp. 22. S. G. Tullett, ed. Butterworth-Heinemann Ltd., Surrey, UK.

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