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PRODUCTION, MODELING, AND EDUCATION
2009 Poultry Science 88 :2712–2717
doi: 10.3382/ps.2009-00069
Key words: oviposition time , egg storage , broiler breeder , egg weight loss , hatchability
ABSTRACT An experiment was conducted to determine
the effect of time of oviposition, generally representing
different positions in the normal egg laying sequence,
on egg weight loss during storage and incubation, and
on fertility and fertile hatchability of eggs from mid-lay
(42 wk) and old (67 wk) broiler breeders. A total of
1,800 eggs (900 eggs per flock age) were collected dur-
ing 10 consecutive days between 0830 and 1830 h each
day. The eggs were individually marked, weighed, and
stored for 1 to 10 d before incubation was initiated. Egg
weight remained less from collection through incuba-
tion for eggs from the mid-lay flock than those from the
old flock. Fresh weight of early laid (first-in-sequence;
C1) eggs was significantly greater than that for the
middle-of-day laid (mid-sequence; Cs), or late-in-day
laid eggs (terminal-in-sequence; Ct). Percentage of egg
weight loss during storage did not differ significantly
between the mid-lay and old flocks but percentage of
weight loss in the mid-lay flock was greater during incu-
bation. Egg weight loss during storage of eggs from the
middle-of-day laid (Cs) eggs was significantly greater
than for early laid (C1) eggs, which was greater than
for the late-in-day laid (Ct) eggs. Fertility was signifi-
cantly decreased due to flock age but not due to ovi-
position time. Fertile hatchability was also significantly
decreased due to flock age, but there was no significant
effect of oviposition time. Early and late dead embryos
increased with flock age, but there was no significant
effect of oviposition time. It was concluded that there
was no effect of oviposition time on fertility or fertile
hatchability even though there were significant differ-
ences in egg weight and egg weight loss during storage
due to oviposition time.
The effects of oviposition time on egg weight loss during storage
and incubation, fertility, and hatchability of broiler hatching eggs
1
A. H. Zakaria ,* P. W. Plumstead ,† H. Romero-Sanchez ,‡ N. Leksrisompong ,† and J. Brake †2
* Department of Animal Science, Faculty of Agriculture, Damascus University, Damascus 30621, Syria;
† Department of Poultry Science, North Carolina State University, Raleigh 27695-7608;
and ‡ Grupo Grica, Faculty of Agriculture, University of Antioquia, AA 1226, Medellin, Colombia
INTRODUCTION
Domestic hens lay eggs on successive days, followed
by a pause of one or more days during which no eggs
will be laid. Eggs laid on successive days have been
called a sequence or clutch of variable length. Further-
more, the time interval between successive ovipositions
in each sequence has been reported to vary from about
24 to 29 h depending on the sequence length, with lon-
ger sequences attributed to a shorter interval between
eggs. In this respect, it has been commonly observed
that the sequence length was longer in younger hens
that laid smaller eggs. This implied that as the hen
aged, the length of the sequence was shortened and
egg weight increased (Etches and Schoch, 1984; Bahr
and Palmer, 1989; Zakaria, 2001; Johnston and Gous,
2003).
In a previous report (Zakaria et al., 2005), the ma-
jority of eggs from a relatively young (34 wk) broiler
breeder flock were produced primarily between 0700
and 1300 h when feeding was at 0800 h, with the great-
est numbers for a single hour being between 0900 and
1000 h. In an older (59 wk) flock under similar condi-
tions, eggs were more evenly distributed between 0700
and 1500 h. Furthermore, egg weight of early laid (C1)
eggs was significantly greater than mid-sequence (Cs)
and late laid (Ct) eggs in the young broiler breeder
flock, whereas the late (Ct) eggs were significantly
smaller than early (C1) and middle (Cs) eggs in the old
broiler breeder flock. Similarly, egg weight of the first-
in-sequence (C1) eggs was reported to be greater than
that of subsequent eggs in a sequence in broiler breed-
ers (Robinson et al., 1991; Novo et al., 1997).
The first-in-sequence (C1) eggs have been associated
with reduced fertility in individually caged and arti-
Received February 6, 2009.
Accepted August 13, 2009.
1 The use of trade names in this publication does not imply endorse-
ment of the products mentioned nor criticism of similar products not
mentioned.
2 Corresponding author: jbrake@ncsu.edu
© 2009 Poultry Science Association Inc.
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ficially inseminated broiler breeders (Robinson et al.,
1991; Goerzen et al., 1996) and in artificially insemi-
nated turkeys (Bacon and Nestor, 1979). Although Fa-
senko et al. (1992) did not find differences in fertility
relative to egg position in a sequence, they reported
lower fertile hatchability in first-in-sequence eggs com-
pared with subsequent eggs in a sequence in individu-
ally caged and artificially inseminated broiler breed-
ers. On the other hand, Zakaria et al. (2005) found no
differences in fertility and fertile hatchability among
eggs of different sequence positions in naturally mated
broiler breeders.
Brake et al. (1997) reviewed the changes in egg com-
ponents associated with egg handling and storage and
concluded that the factors that could affect hatchability
varied by age of flock, age of egg, ambient temperature,
strain, and handling procedures. Fasenko et al. (1991)
further stated that nest holding time and method of
egg storage affected postoviposition and preincubation
embryonic growth. Oviposition time may also affect
hatchability. The objective of the present study was to
examine the effect of breeder flock age and oviposition
time on egg weight, egg weight loss during both storage
and incubation, fertility, hatchability, and embryonic
mortality of broiler hatching eggs.
MATERIALS AND METHODS
Birds and Management
Two flocks of Ross 344 male × Ross 308 slow-feath-
ering female broiler breeders at 42 wk of age (mid-lay)
and 67 wk of age (old) were housed in 15 pens each
of 2 adjacent two-thirds slat curtain-sided houses and
were subjected to the same nutrition and management
programs. An average of 54 females with 6 males or
46 females with 5 males was present in each pen of
the mid-lay and old flocks, respectively, at the time
of experiment. Incandescent lights operated from 0330
to 1930 h (daylight saving time) each day with ad-
ditional natural daylight entering each house through
open or translucent curtains, depending upon ambient
temperature. The birds were fed at 0800 h daily and
water was available for ad libitum consumption from
0700 to 1500 h daily.
Experimental Design
All eggs were removed from the nest boxes in each
of the 15 pens at 1900 h on the day before the first egg
collection and during each day of the experiment. A to-
tal of 1,800 eggs (900 eggs per flock age) were collected
during 10 consecutive days starting at 0830 h and ter-
minating at 1830 h each day. Two eggs were randomly
selected from all of those collected from each of the 15
pens at 0830, 1100, and 1800 h each day from the mid-
lay flock to be used for incubation. Eggs collected at
1030 and 1300 h were not used. Thus, the 30 eggs col-
lected at 0830, 1100, and 1800 h generally represented
early (C1), middle (Cs), and late (Ct) eggs, respec-
tively. In a similar manner, eggs were collected at 0930,
1130, and 1830 h each day from the old flock to be used
for incubation. Eggs collected at 1100 and 1330 h were
not used. Thus, the 30 eggs collected at 0930, 1130, and
1830 h generally represented early (C1), middle (Cs),
and late (Ct) eggs, respectively, in the old flock. The
slight modification of time of collection between the
2 flock age groups was required to provide sufficient
numbers of eggs in the old flock based upon knowledge
of the pattern of egg production and the actual count
of eggs present during the first 2 d of this experiment.
A 10-d period was selected so as to include the full
range of egg storage periods that might reasonably be
encountered during normal commercial practice. Thus,
eggs collected during the first day were stored for 10 d
and those collected on the 10th day were stored for 1
d. All eggs were individually identified by pen number,
flock age, and date of collection before being weighed to
the nearest 0.01 g. Eggs from each day of egg collection
were transferred to a cooler (14 to 16°C and 65% RH)
2 h after collection.
A total of 1,800 eggs representing the 3 daily oviposi-
tion times from 10 d of egg collection from the mid-lay
(900 eggs) and old (900 eggs) broiler breeders were dis-
tributed randomly among 10 incubator trays (180 eggs
per tray), with both flock ages and all oviposition times
uniformly represented in each tray. The 10 trays were
randomly placed into a single Natureform NMC-2000
incubator (Natureform International, Jacksonville, FL)
to 18 d of incubation at an internal egg temperature
of 37.8°C for the first 24 h of incubation and 37.5 to
37.8°C thereafter as determined by the method of Lek-
srisompong et al. (2007). Relative humidity was au-
tomatically controlled at 55% and eggs were turned
through a 90° angle 48 times daily through 18 d of incu-
bation. At 18 d of incubation, all eggs were weighed in-
dividually and then transferred to hatching baskets and
returned to the same machine at 36.8°C to complete
the hatching process. The number of chicks hatched
from each tray was counted at 21.5 d of incubation. All
unhatched eggs were then opened and examined mac-
roscopically by a single experienced individual to deter-
mine fertility or stage of embryonic mortality, or both.
Eggs were classified as cracked (11 eggs were excluded
from calculations), infertile, early dead (embryos died 1
to 7 d of incubation), and late dead (embryos died 8 to
21 d of incubation). For purposes of statistical analysis,
the middle dead, late dead, and pipped embryos were
combined into the 8 to 21 d late dead group.
Statistical Analysis
The effects of flock age and time of oviposition on
egg weight and egg weight loss during storage and in-
cubation were analyzed by ANOVA using the GLM
procedure of SAS Institute (1991) with day of collec-
tion as a block. Differences among means were sepa-
rated using least squares mean analysis. Fertility, fertile
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hatchability, and embryo mortality data were subjected
to categorical analyses using the odds ratio method to
estimate relative treatment differences of the effects of
flock age, time of oviposition [early (C1), middle (Cs),
and late (Ct)], and their interactions on fertility, fertile
hatchability, and embryonic mortality (SAS Institute,
1991). Unless otherwise indicated, statements of statis-
tical significance were based upon P < 0.01.
RESULTS AND DISCUSSION
The effects of flock age, oviposition time, and their
interaction on egg weight at collection, during stor-
age before setting, and during incubation are shown in
Table 1. As expected, egg weight at collection, during
storage before setting, and during 18 d of incubation
was less for the mid-lay than for the old flock. Weight
of early laid (C1) eggs was significantly greater than for
the middle (Cs) eggs or late (Ct) eggs. However, there
was an interaction between flock age and oviposition
time for egg weight at collection, during storage before
setting, and during incubation for early (C1), middle
(Cs), and late (Ct) oviposition times. Inspection of the
data of Table 1 revealed this interaction to have been
due to the late laid (Ct) eggs from the old flock being
smaller than the middle laid (Cs) eggs of the older flock,
but this was not the case for the mid-lay flock, whereas
early laid eggs were the largest in all cases. These data
confirmed and extended previous findings (Zakaria et
al., 2005) that egg weight decreased as time of oviposi-
tion (position in a sequence) advanced in 2 Ross 308
flocks aged 34 and 59 wk. This was consistent with the
results obtained by Robinson et al. (1991), who used
Indian River broiler breeder hens at 45 wk of age and
reported that early (C1) eggs were significantly greater
in weight than subsequent eggs in a sequence. Similarly,
Novo et al. (1997) utilized eggs produced by Cobb 500
broiler breeder hens at 46 and 65 wk of age and found
egg weight to decrease with later time of oviposition.
The effect of aging and the relationships of sequence
length and egg position on ovarian follicular develop-
ment of commercial layers has been studied in detail by
Zakaria et al. (1983, 1984a,b) and Zakaria (1999a,b).
These studies indicated 1) there was a continuous in-
crease in follicular (yolk) volume at ovulation (and thus
egg weight) with increasing age, 2) the average follicu-
lar growth period increased as sequence size decreased
(flock aged), 3) the follicular growth period decreased
as egg position in a sequence increased from second to
sixth, 4) follicular (yolk) volume tended to be less in
terminal (Ct) follicles in sequences of 2 to 5 eggs, and
5) the follicular growth period of the C1 egg was longer
than for Ct follicles. Based on these considerations, it
could be suggested that the rapid growth phase of Ct
follicles was shorter and the rapid growth phase of C1
follicles was longer to account for the differences in the
egg weight among the more numerous and smaller eggs
Table 1. Egg weight at collection, after storage before setting, and at transfer after 18 d of incubation
from early, middle, and late oviposition times of 42-wk-old and 67-wk-old broiler breeder flocks
Variable
Egg weight (g)
Collection1Setting2Transfer3
Flock age (wk)
42 63.7 ± 0.2B63.4 ± 0.2B57.4 ± 0.2B
67 68.2 ± 0.2A67.9 ± 0.2A61.7 ± 0.2A
Oviposition time
Early467.8 ± 0.2A67.5 ± 0.2A61.3 ± 0.2A
Middle565.1 ± 0.2B64.8 ± 0.2B58.7 ± 0.2B
Late665.0 ± 0.2B64.7 ± 0.2B58.7 ± 0.2B
Age × oviposition time
42 wk
Early 65.9 ± 0.3D65.6 ± 0.3D59.5 ± 0.3D
Middle 62.3 ± 0.3E62.0 ± 0.3E56.1 ± 0.3E
Late 62.9 ± 0.3E62.6 ± 0.3E56.7 ± 0.3E
67 wk
Early 69.7 ± 0.3A69.4 ± 0.3A63.2 ± 0.3A
Middle 67.9 ± 0.3B67.5 ± 0.3B61.4 ± 0.3B
Late 67.1 ± 0.3C66.8 ± 0.3C60.6 ± 0.3C
A–EMeans ± SE for 900 eggs from each flock age in a column with different superscripts differ significantly (P
< 0.01).
1Egg weight at collection.
2Egg weight before setting at the end of storage period of 1 to 10 d at 14 to 16°C and 65% RH.
3Egg weight at 18 d of incubation before transfer to hatching baskets.
4Early oviposition time of 0830 to 0930 h generally represented first-in-sequence (C1) eggs in a laying se-
quence.
5Middle oviposition time of 1100 to 1130 h generally represented mid-sequence (Cs) eggs in a laying sequence.
6Late oviposition time of 1400 to 1800 h generally represented terminal-in-sequence (Ct) eggs in a laying se-
quence.
ZAKARIA ET AL.
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of the young flock in the present study. In contrast, the
larger eggs from the shorter sequence lengths of the
older flock, the Cs and Ct eggs, were smaller.
The effects of flock age, oviposition time, and their
interaction on percentage of egg weight loss during stor-
age before setting, incubation, and total (combined) are
shown in Table 2. Percentage of egg weight loss during
storage before setting did not differ significantly be-
tween the mid-lay and the old flocks, but percentage
of weight loss in the mid-lay flock was greater during
incubation as reflected by the transfer and total egg
weight loss. Egg weight loss in relation to oviposition
time differed during egg storage before setting but did
not differ during incubation. In this respect, weight loss
during storage of eggs from the middle (Cs) oviposition
time was significantly greater than for eggs from the
early (C1) oviposition time, which was, in turn, greater
than for eggs from the late (Ct) oviposition time. There
were no significant interactions.
According to Peebles and Brake (1987), shell thick-
ness was the lowest and porosity the greatest during
the mid-lay age period. It has been well documented
that mid-sequence eggs (Cs) comprise most of the eggs
produced by mid-lay hens (Etches and Schoch, 1984;
Bahr and Palmer, 1989; Zakaria, 2001). Higher relative
porosity may explain, in general, why egg weight loss of
the mid-lay flock or mid-sequence eggs (Cs) was greater
than that of the old flock. Weight loss may be explained
by liberation of water as a result of deterioration of the
albumen with subsequent passage of unbound water
through the eggshell as influenced by variation in albu-
men quality due to flock age, storage time, and storage
conditions (Brake et al., 1997; Lapao et al., 1999; Tona
et al., 2003).
The effects of flock age, oviposition time, and their
interaction on fertility, fertile hatchability, and embryo
mortality are shown in Table 3. As expected, fertility
was significantly decreased due to flock age but not
due to oviposition time, or the interaction of flock age
and oviposition time. Fertile hatchability was also sig-
nificantly decreased due to flock age, as expected, but
there was no significant effect of oviposition time or
the age × oviposition time interaction (Table 3). As
was the case for fertile hatchability, late dead embry-
os increased with flock age, whereas early dead em-
bryos exhibited a similar numerical trend (P < 0.10)
but there was no significant effect of oviposition time.
This was consistent with the report of Elibol and Brake
(2004), who found that fertile hatchability was much
better from a 29-wk-old broiler breeder flock than from
a 68-wk-old flock because of decreased mortality at all
stages of embryo development. However, in the present
study, there was a significant interaction of flock age ×
oviposition time for percentage early dead, which was
due to increased early dead embryos during the early
C1 oviposition time of the mid-lay flock but a decrease
in early dead embryos during the same period in the
old flock (Table 3). Albumen quality varies with flock
Table 2. Percentage of egg weight loss after storage before setting, after 18 d of incubation, and the
combined total loss from early, middle, and late oviposition times of 42-wk-old and 67-wk-old broiler
breeder flocks
Variable
Egg weight loss (%)
Setting1Transfer2Total3
Age (wk)
42 0.45 ± 0.01 9.45 ± 0.07A9.86 ± 0.07A
67 0.47 ± 0.01 9.14 ± 0.07B9.57 ± 0.07B
Oviposition time
Early40.47 ± 0.01B9.17 ± 0.09 9.59 ± 0.09
Middle50.52 ± 0.01A9.31 ± 0.09 9.79 ± 0.09
Late60.41 ± 0.01C9.41 ± 0.09 9.78 ± 0.09
Age × oviposition time
42 wk
Early 0.43 ± 0.02 9.37 ± 0.13 9.76 ± 0.13
Middle 0.53 ± 0.02 9.48 ± 0.13 9.96 ± 0.13
Late 0.41 ± 0.02 9.49 ± 0.14 9.87 ± 0.14
67 wk
Early 0.50 ± 0.02 8.96 ± 0.13 9.42 ± 0.13
Middle 0.51 ± 0.02 9.16 ± 0.13 9.69 ± 0.13
Late 0.41 ± 0.02 9.32 ± 0.13 9.62 ± 0.13
A–CMeans ± SE for 900 eggs from each flock age in a column with different superscripts differ significantly (P <
0.01). The absence of superscripts indicates the absence of significant effects.
1Egg weight loss at the end of the storage period at 14 to 16°C and 65% RH for 1 to 10 d before setting in the
incubator.
2Egg weight loss at 18 d of incubation before transfer to hatching baskets.
3Total egg weight loss relative to egg weight at collection.
4Early oviposition time of 0830 to 0930 h generally represented first-in-sequence (C1) eggs in a laying se-
quence.
5Middle oviposition time of 1100 to 1130 h generally represented mid-sequence (Cs) eggs in a laying sequence.
6Late oviposition time of 1400 to 1800 h generally represented terminal-in-sequence (Ct) eggs in a laying se-
quence.
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age and length of egg storage (Brake at al., 1997) and
probably played some role in this interaction.
Reports have previously stated that hatchability de-
creased with increased egg weight (Wilson, 1991; Ogun-
shile and Sparks, 1995; French, 1997), but the signifi-
cantly larger early (C1) eggs of the present study did
not exhibit a significant decrease in fertile hatchability.
Elibol and Brake (2008) found that fertile hatchability
was decreased in larger eggs, about 69 g in comparison
with about 63 to 66 g, obtained from a flock of 51- to
57-wk-old Ross 308 broiler breeders. Perhaps the differ-
ence in egg weight due to time of oviposition found in
the present study was not sufficiently great to induce
the effect. Increased embryonic mortality associated
with greater egg weight, especially late deads, has been
explained on the basis of difficulties in losing embryonic
metabolic heat during the latter stages of incubation
(French, 1997; Elibol and Brake, 2008). This may ex-
plain the increased late deads in the considerably larger
eggs (~4.5 g) of the older flock versus mid-lay flock of
the present study as opposed to the slightly larger eggs
(~2.7 g) due to early oviposition time. Evidently, there
may be a threshold difference in egg weight required to
observe a significant difference in hatchability and this
may depend upon egg management, incubation condi-
tions, and age of flock.
In this study, percentage egg weight loss at 18 d of
incubation before transfer and total egg weight loss
during storage and incubation from old hens was sig-
nificantly less than for eggs from mid-lay hens (Table
2). The fact that weight loss was higher in the mid-lay
flock would be consistent with greater porosity (Peebles
and Brake, 1987) and better fertile hatchability (Table
3). The percentage weight loss approached 10% (Table
2) under conditions of this study, which was slightly less
than the weight loss of 10.9 to 11% associated with the
highest hatchability in 27- to 60-wk-old Cobb broiler
breeders (Tona et al., 2001), but the fertile hatchability
was acceptable in the present study nonetheless (Table
3).
The fertility of early laid eggs (C1) was not reduced
in this study with naturally mated hens in contrast
to artificially mated turkeys (Bacon and Nestor, 1979)
and broiler breeders (Robinson et al., 1991) but was
in close agreement with other findings (Zakaria et al.,
2005). It was important to note that the previous study
of Robinson et al. (1991) used an individual cage sys-
tem where about 38% of the eggs were first-in-sequence
(C1) eggs, which clearly demonstrated a high incidence
of short sequence lengths (poor egg production). Rob-
inson et al. (1991) reported 87.0% fertility for the first-
in-sequence eggs versus 89.6% fertility for eggs in other
sequence positions. Similarly, Bacon and Nestor (1979)
classified eggs as “first of the clutch,” including clutch
lengths of only one egg, and “other clutch position.” In
agreement with the present findings, Novo et al. (1997)
collected eggs at 2-h intervals between 0800 and 1800
h from 13,900 commercially housed hens and did not
find significant differences in fertility and embryonic
mortality relative to time of oviposition at 46 and 65
wk of age, or differences in hatchability at 46 wk of age.
Thus, although poor fertility may be observed in early
Table 3. Fertility, fertile hatchability, and embryonic mortality of eggs from 42-wk-old and 67-wk-old
broiler breeders that were stored for 1 to 10 d before incubation
Variable Fertility1 (%) Fertile hatchability (%) Early dead (%) Late dead (%)
Age (wk)
42 96.0A91.9A4.1y3.1B
67 77.3B85.7B5.9x8.4A
Oviposition time
Early286.6 88.2 4.6 6.5
Middle387.4 90.3 4.9 4.4
Late485.9 87.5 5.8 6.2
Age × oviposition time
42 wk
Early 95.3 89.4 6.0A3.2
Middle 97.3 93.2 3.4B2.7
Late 95.3 92.9 2.8B3.2
67 wk
Early 77.8 86.9 3.2B9.9
Middle 77.6 87.5 6.4A6.1
Late 76.4 82.1 8.8A9.1
x,yMeans for 900 eggs from each flock age in a column with different superscripts approach significance (P <
0.10). There is no SE with categorical analysis. The absence of superscripts indicates the absence of significant
effects.
A,BMeans for approximately 900 eggs from each flock age in a column with different superscripts differ signifi-
cantly (P < 0.01). There is no SE with categorical analysis. The absence of superscripts indicates the absence of
significant effects.
1Percentage of fertile hatchability, early, and late dead embryos calculated based on number of fertile eggs.
2Early oviposition time of 0830 to 0930 h generally represented first-in-sequence (C1) eggs in a laying se-
quence.
3Middle oviposition time of 1100 to 1130 h generally represented mid-sequence (Cs) eggs in a laying sequence.
4Late oviposition time of 1400 to 1800 h generally represented terminal-in-sequence (Ct) eggs in a laying se-
quence.
ZAKARIA ET AL.
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laid (C1) eggs under some conditions, especially with
artificial insemination, this effect was not observed in
the natural mating conditions of the present study. It
was concluded that there was no effect of oviposition
time on fertility or fertile hatchability even though
there were significant differences in egg weight and egg
weight loss during storage due to oviposition time.
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