- Email: [email protected]
Triple-yolked eggs in domestic ducks: a rare occurrence
Triple-yolked eggs in domestic ducks: a rare occurrence Attila Salamon∗,†,1 and John P. Kent† ∗
School of Biology and Environmental Science, University College Dublin, Belfield, Dublin 4, Ireland; and † Ballyrichard House, Arklow, Co. Wicklow, Ireland
Key words: duck, fertility, incubation, triple-yolked egg, yolk position 2016 Poultry Science 00:1–3 http://dx.doi.org/10.3382/ps/pew004
INTRODUCTION
On day 2 of incubation (E2), the eggs were weighed on a digital scale (±0.1 g); length and width were measured with a digital caliper (±0.01 mm). Egg shape was determined according to the scale devised by Roberts (1997). Yolk position was recorded on E2 and E8 by individual candling. Fertility was recorded on E8, and further weighing and candling took place on E12, E15, E19, E22, and E25 of incubation. Dead eggs were removed when identified, stored overnight, and opened the next day to estimate the day of embryonic death using Kaltofen (1971) as a guide.
Multiple-yolked avian eggs are rare, with an estimated one in every 500 eggs being double-yolked (DY), and one in every 5,000 to 6,000 is triple-yolked (TY) (Romanoff and Romanoff, 1949). Studies on TY eggs are also rare, with Romanoff and Romanoff (1949) reporting studies on a total of four TY hen (Gallus gallus domesticus) eggs including a very large one, all containing proportionately more total yolk, but less albumen and shell than single-yolked (SY) eggs (Curtis, 1914; Clark, 1932; reviewed in Romanoff and Romanoff, 1949). Here, TY eggs were identified during a larger study that compared DY and SY duck eggs (Salamon and Kent, 2014, 2016) through the incubation process. The objective of this study was to describe the incubation of TY eggs.
RESULTS Seven (0.0145%) TY eggs were identified, i.e., approximately one in every 6,900 eggs. Physical parameters are shown in Table 1. TY egg weight varied (93.2 to 136.5 g), with three lighter than 100 g, and four over 109 g. Length ranged from 70.27 to 82.35 mm, while the range of width was 49.25 to 56.21 mm and three different egg shapes were identified: ideal (n = 3), conical (n = 2) and biconical (n = 2). Three yolk positions were identified in TY eggs (see Fig. 1): type A (Eggs 1, 2, 4, and 6), B (Eggs 5 and 7), and C (Egg 3). During incubation (from E2 to E8), yolk position remained the same in eggs with three infertile yolks (Eggs 2 and 7), while it changed in Egg 1 (from type A to B) and in Egg 5 (from type B to C) with the fertile yolks positioned close to the airspace. The yolk movement suggests the absence of chalazae between the yolks. However, in 42.86% (3/7) of eggs (Eggs 2, 4, and 6) it was not possible to identify yolk position on E8, as those eggs were infected and their yolks were disintegrated. In TY eggs, 33.33% of all yolks (7/21) were
MATERIALS AND METHODS A total of 48,224 eggs from a flock of ducks of the Aylesbury breed over a 2-year period (2008–2010) were studied at Ballyrichard (Arklow, Ireland; 52◦ 50 5 N, 6◦ 7 49 W). The flock was managed as described by Salamon and Kent (2016). TY eggs from 42 batches were identified before setting by individual candling. Eggs were set and managed as described in Salamon and Kent (2014).
C 2016 Poultry Science Association Inc. Received September 17, 2015. Accepted December 1, 2015. 1 Corresponding author: [email protected]
1
Downloaded from http://ps.oxfordjournals.org/ at University of Pittsburgh on February 17, 2016
sions were greater than for single-yolked duck eggs. Yolk fertility in the TY eggs was low (33.33%), and this was attributed to smaller yolk size and early ovulation and/or follicle immaturity. By day 8 of incubation, fertile yolks were positioned next to the airspace. Egg 5 contained one fertile yolk, and the embryo developed to enter the airspace, was consuming all three yolks, but failed to hatch.
ABSTRACT Multiple-yolked avian eggs, and especially triple-yolked (TY) eggs, are rare. Over two years, 48,224 duck eggs (Anas platyrhynchos domesticus) were individually candled and seven (0.0145%) TY eggs were identified in a commercial breeding and incubation environment. When compared with double-yolked eggs (Salamon and Kent, 2016) their mean weight, length, width and shape index did not differ, but their dimen-
2
SALAMON AND KENT Table 1. Physical parameters of triple-yolked (TY) eggs: egg weight on E2, length, width, shape index, shape; and the fertility of TY eggs on E8. Egg number
TY egg weight on E2 (g)
Length (mm)
Width (mm)
Shape index (length/width)
Egg shape
Fertility on E8
1 2 3 4 5 6 7
131.7 136.5 97.2 109.6 93.2 96.7 120.4
82.35 79.2 76.94 74.42 70.27 72.09 78.85
54.15 56.21 48.84 51.15 49.25 49.28 53
1.52 1.41 1.58 1.45 1.43 1.46 1.49
conical ideal biconical ideal ideal biconical conical
3 3 1 1 1 1 3
Mean (±SD)
112.19 (±17.66)
76.30 (±4.27)
51.70 (±2.84)
1.48 (±0.06)
fertile yolks (2 alive, 1 dead) infertile yolks fertile, 2 infertile yolks fertile (dead), 2 infertile yolks fertile, 2 infertile yolks fertile (dead), 2 infertile yolks infertile yolks
fertile. In the egg with three fertile yolks (Egg 1), two yolks with live embryos were closer to the airspace at E8 (type B position). In the two eggs with one fertile yolk (Eggs 3 and 5), the fertile yolk was next to the airspace, on E8 (type C position; see Fig. 1). Blood rings were observed on the fertile but dead yolks in Eggs 1, 4, and 6 at candling on E8, suggesting death on E3-4 of incubation (see Kaltofen, 1971). Infertile (Eggs 2 and 7) or fertile but dead (Eggs 4 and 6) eggs were removed at candling on E8. Three eggs remained in the incubator after fertility check on E8. Egg 3 became infected and was removed on E12. Egg 1 was incubated up to E17, when the two remaining live embryos died. Egg 5 was incubated and transferred to the hatcher on E26. The one embryo of Egg 5 entered the airspace, but did not hatch and was examined post-mortem on E30 of incubation. The embryo was relatively large compared those from SY eggs with a larger abdomen and two yolk sacs attached, one about pea sized and the other about three times pea size.
DISCUSSION The finding that one in every 6,900 duck eggs was TY is comparable to findings in domestic fowl (Curtis, 1914; reviewed in Romanoff and Romanoff, 1949), and
the relatively small egg size suggests that they were produced at the onset of laying (Curtis, 1914; Clark, 1932, reviewed in Romanoff and Romanoff, 1949). Variation in egg weight has been observed in DY duck eggs. However, 41.73% of such DY eggs were similar in weight to SY eggs (Salamon and Kent, 2016). Interestingly, the mean egg weight, length, width, and shape index of TY duck eggs did not differ from those of DY duck eggs, but were greater than those of SY duck eggs (for means of DY and SY duck eggs, see Salamon and Kent, 2016). Further, TY duck eggs were ideal, conical, and biconical shaped and these were the most common shapes in DY eggs (Salamon and Kent, 2016). Curtis (1914) also showed that the proportions of the internal contents of the TY hen eggs did not differ from those in DY eggs, but differed from SY eggs by having proportionally more yolk and less albumen. However, the individual yolks in the TY eggs were smaller than those in SY and DY eggs (Curtis, 1914), which complements the finding of Salamon and Kent (2013) comparing the internal contents of SY and DY duck eggs and further strengthens the view that DY and TY eggs are produced by young birds at the onset of laying (Romanoff and Romanoff, 1949; Salamon and Kent, 2016). The fertility in the TY egg yolks was only 33.33% and is similar to that of DY hen eggs (27.3%;
Downloaded from http://ps.oxfordjournals.org/ at University of Pittsburgh on February 17, 2016
Figure 1. Yolk positions as identified in triple-yolked eggs. AS: airspace.
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TRIPLE-YOLKED DUCK EGGS
REFERENCES Burke, W. H., M. H. Henry, and I. Elezaj. 1997. Comparison of embryos and chicks that developed as single individuals in double yolk eggs with those developed in single yolk eggs. Poult. Sci. 76:901–907. Clark, T. B. 1932. A triple-yolk egg. Poult. Sci. 11:176. Curtis, M. R. 1914. Studies on the physiology of reproduction in the domestic fowl. VI. Double- and triple-yolked eggs. Biol. Bull. 26:55–83. Fasenko, G. M., F. E. Robinson, B. L. Danforth, and I. Zelter. 2000. An examination of fertility, hatchability, embryo mortality, and chick weight in double versus single-yolked broiler breeder eggs. Can. J. Anim. Sci. 80:489–493. Fechheimer, N. S., and W. P. Jaffe. 1966. Fertility and embryo death in double-yolked eggs. J. Reprod. Fert. 12:363–364. Kaltofen, R. S. 1971. Embryonic Development in the Eggs of the Pekin Duck. Center for Agricultural Publishing and Documentation, Wageningen, The Netherlands. Monkman, M. 1963. A study of the development of double-yolked eggs. MSc Thesis, Northern Illinois University, DeKalb, Illinois. Roberts, V. 1997. Standard for eggs. Pages 359–362 in British Poultry Standards. 5th ed. V. Roberts, ed. Blackwell Science Ltd., Oxford, UK. Romanoff, A. L., and A. J. Romanoff. 1949. The Avian Egg. John Wiley & Sons Inc., New York. Salamon, A. 2015. Maternal investment – and its constraints – in the egg of domestic waterfowl. PhD Diss. University College Dublin, Dublin, Ireland. Salamon, A., and J. P. Kent. 2013. Double and single yolked duck eggs: their contents and dimensions compared and the mechanical stimulation hypothesis for albumen secretion is supported. Int. J. Poult. Sci. 12:254–260. Salamon, A., and J. P. Kent. 2014. Changes during incubation within double-yolked duck (Anas platyrhynchos domesticus) eggs: yolk position, mortality, hatchability and the importance of an optimal egg size. Int. J. Poult. Sci. 13:695–702. Salamon, A., and J. P. Kent. 2016. Yolk size and ovulation order determine fertility within double yolked duck (Anas platyrhynchos domesticus) eggs. Reprod. Fert. Dev. 28:440–445.
Downloaded from http://ps.oxfordjournals.org/ at University of Pittsburgh on February 17, 2016
Fechheimer and Jaffe, 1966), but lower than yolk fertility in DY (51.9%) and SY duck eggs (89.98%; Salamon and Kent, 2016), and DY (62.5%) and SY broiler breeder eggs (98.44%; Fasenko et al., 2000). Yolks in DY duck eggs are smaller than in SY duck eggs (Salamon and Kent, 2013) and have a lower chance of achieving fertilization that was attributed to early ovulation and / or follicle immaturity (Salamon and Kent, 2016). The small size–within the normal SY duck egg weight range (75 to 104.9 g; Salamon and Kent, 2016)–of TY duck eggs and an associated small yolk size should explain the low fertility of TY duck eggs found here. Two TY eggs were incubated long enough to record egg weight-loss data that was similar to that of DY duck eggs (Salamon, 2015). The one live embryo in Egg 5 entered the airspace on E26 and was transferred to the hatcher. It did not hatch and the post-mortem examination showed that the embryo was internalizing all three yolks, but did not complete this process. Thus, it is possible that a single embryo in TY eggs may reach the point of hatching, as found in DY eggs (domestic fowl, Monkman, 1963; Burke et al., 1997; Fasenko et al., 2000; duck, Salamon and Kent, 2014). It was suggested that there may be an optimal egg weight range to facilitate successful hatching in DY and SY eggs (Monkman, 1963; Salamon and Kent, 2014) and this may also apply to the rare TY duck egg, as Egg 5 was within the ‘optimal’ weight range. However, the relative excess of yolk and/or lack of albumen in DY and TY eggs must also be considered in the context of embryo development and as a constraint on successful hatching.
School of Biology and Environmental Science, University College Dublin, Belfield, Dublin 4, Ireland; and † Ballyrichard House, Arklow, Co. Wicklow, Ireland
Key words: duck, fertility, incubation, triple-yolked egg, yolk position 2016 Poultry Science 00:1–3 http://dx.doi.org/10.3382/ps/pew004
INTRODUCTION
On day 2 of incubation (E2), the eggs were weighed on a digital scale (±0.1 g); length and width were measured with a digital caliper (±0.01 mm). Egg shape was determined according to the scale devised by Roberts (1997). Yolk position was recorded on E2 and E8 by individual candling. Fertility was recorded on E8, and further weighing and candling took place on E12, E15, E19, E22, and E25 of incubation. Dead eggs were removed when identified, stored overnight, and opened the next day to estimate the day of embryonic death using Kaltofen (1971) as a guide.
Multiple-yolked avian eggs are rare, with an estimated one in every 500 eggs being double-yolked (DY), and one in every 5,000 to 6,000 is triple-yolked (TY) (Romanoff and Romanoff, 1949). Studies on TY eggs are also rare, with Romanoff and Romanoff (1949) reporting studies on a total of four TY hen (Gallus gallus domesticus) eggs including a very large one, all containing proportionately more total yolk, but less albumen and shell than single-yolked (SY) eggs (Curtis, 1914; Clark, 1932; reviewed in Romanoff and Romanoff, 1949). Here, TY eggs were identified during a larger study that compared DY and SY duck eggs (Salamon and Kent, 2014, 2016) through the incubation process. The objective of this study was to describe the incubation of TY eggs.
RESULTS Seven (0.0145%) TY eggs were identified, i.e., approximately one in every 6,900 eggs. Physical parameters are shown in Table 1. TY egg weight varied (93.2 to 136.5 g), with three lighter than 100 g, and four over 109 g. Length ranged from 70.27 to 82.35 mm, while the range of width was 49.25 to 56.21 mm and three different egg shapes were identified: ideal (n = 3), conical (n = 2) and biconical (n = 2). Three yolk positions were identified in TY eggs (see Fig. 1): type A (Eggs 1, 2, 4, and 6), B (Eggs 5 and 7), and C (Egg 3). During incubation (from E2 to E8), yolk position remained the same in eggs with three infertile yolks (Eggs 2 and 7), while it changed in Egg 1 (from type A to B) and in Egg 5 (from type B to C) with the fertile yolks positioned close to the airspace. The yolk movement suggests the absence of chalazae between the yolks. However, in 42.86% (3/7) of eggs (Eggs 2, 4, and 6) it was not possible to identify yolk position on E8, as those eggs were infected and their yolks were disintegrated. In TY eggs, 33.33% of all yolks (7/21) were
MATERIALS AND METHODS A total of 48,224 eggs from a flock of ducks of the Aylesbury breed over a 2-year period (2008–2010) were studied at Ballyrichard (Arklow, Ireland; 52◦ 50 5 N, 6◦ 7 49 W). The flock was managed as described by Salamon and Kent (2016). TY eggs from 42 batches were identified before setting by individual candling. Eggs were set and managed as described in Salamon and Kent (2014).
C 2016 Poultry Science Association Inc. Received September 17, 2015. Accepted December 1, 2015. 1 Corresponding author: [email protected]
1
Downloaded from http://ps.oxfordjournals.org/ at University of Pittsburgh on February 17, 2016
sions were greater than for single-yolked duck eggs. Yolk fertility in the TY eggs was low (33.33%), and this was attributed to smaller yolk size and early ovulation and/or follicle immaturity. By day 8 of incubation, fertile yolks were positioned next to the airspace. Egg 5 contained one fertile yolk, and the embryo developed to enter the airspace, was consuming all three yolks, but failed to hatch.
ABSTRACT Multiple-yolked avian eggs, and especially triple-yolked (TY) eggs, are rare. Over two years, 48,224 duck eggs (Anas platyrhynchos domesticus) were individually candled and seven (0.0145%) TY eggs were identified in a commercial breeding and incubation environment. When compared with double-yolked eggs (Salamon and Kent, 2016) their mean weight, length, width and shape index did not differ, but their dimen-
2
SALAMON AND KENT Table 1. Physical parameters of triple-yolked (TY) eggs: egg weight on E2, length, width, shape index, shape; and the fertility of TY eggs on E8. Egg number
TY egg weight on E2 (g)
Length (mm)
Width (mm)
Shape index (length/width)
Egg shape
Fertility on E8
1 2 3 4 5 6 7
131.7 136.5 97.2 109.6 93.2 96.7 120.4
82.35 79.2 76.94 74.42 70.27 72.09 78.85
54.15 56.21 48.84 51.15 49.25 49.28 53
1.52 1.41 1.58 1.45 1.43 1.46 1.49
conical ideal biconical ideal ideal biconical conical
3 3 1 1 1 1 3
Mean (±SD)
112.19 (±17.66)
76.30 (±4.27)
51.70 (±2.84)
1.48 (±0.06)
fertile yolks (2 alive, 1 dead) infertile yolks fertile, 2 infertile yolks fertile (dead), 2 infertile yolks fertile, 2 infertile yolks fertile (dead), 2 infertile yolks infertile yolks
fertile. In the egg with three fertile yolks (Egg 1), two yolks with live embryos were closer to the airspace at E8 (type B position). In the two eggs with one fertile yolk (Eggs 3 and 5), the fertile yolk was next to the airspace, on E8 (type C position; see Fig. 1). Blood rings were observed on the fertile but dead yolks in Eggs 1, 4, and 6 at candling on E8, suggesting death on E3-4 of incubation (see Kaltofen, 1971). Infertile (Eggs 2 and 7) or fertile but dead (Eggs 4 and 6) eggs were removed at candling on E8. Three eggs remained in the incubator after fertility check on E8. Egg 3 became infected and was removed on E12. Egg 1 was incubated up to E17, when the two remaining live embryos died. Egg 5 was incubated and transferred to the hatcher on E26. The one embryo of Egg 5 entered the airspace, but did not hatch and was examined post-mortem on E30 of incubation. The embryo was relatively large compared those from SY eggs with a larger abdomen and two yolk sacs attached, one about pea sized and the other about three times pea size.
DISCUSSION The finding that one in every 6,900 duck eggs was TY is comparable to findings in domestic fowl (Curtis, 1914; reviewed in Romanoff and Romanoff, 1949), and
the relatively small egg size suggests that they were produced at the onset of laying (Curtis, 1914; Clark, 1932, reviewed in Romanoff and Romanoff, 1949). Variation in egg weight has been observed in DY duck eggs. However, 41.73% of such DY eggs were similar in weight to SY eggs (Salamon and Kent, 2016). Interestingly, the mean egg weight, length, width, and shape index of TY duck eggs did not differ from those of DY duck eggs, but were greater than those of SY duck eggs (for means of DY and SY duck eggs, see Salamon and Kent, 2016). Further, TY duck eggs were ideal, conical, and biconical shaped and these were the most common shapes in DY eggs (Salamon and Kent, 2016). Curtis (1914) also showed that the proportions of the internal contents of the TY hen eggs did not differ from those in DY eggs, but differed from SY eggs by having proportionally more yolk and less albumen. However, the individual yolks in the TY eggs were smaller than those in SY and DY eggs (Curtis, 1914), which complements the finding of Salamon and Kent (2013) comparing the internal contents of SY and DY duck eggs and further strengthens the view that DY and TY eggs are produced by young birds at the onset of laying (Romanoff and Romanoff, 1949; Salamon and Kent, 2016). The fertility in the TY egg yolks was only 33.33% and is similar to that of DY hen eggs (27.3%;
Downloaded from http://ps.oxfordjournals.org/ at University of Pittsburgh on February 17, 2016
Figure 1. Yolk positions as identified in triple-yolked eggs. AS: airspace.
3
TRIPLE-YOLKED DUCK EGGS
REFERENCES Burke, W. H., M. H. Henry, and I. Elezaj. 1997. Comparison of embryos and chicks that developed as single individuals in double yolk eggs with those developed in single yolk eggs. Poult. Sci. 76:901–907. Clark, T. B. 1932. A triple-yolk egg. Poult. Sci. 11:176. Curtis, M. R. 1914. Studies on the physiology of reproduction in the domestic fowl. VI. Double- and triple-yolked eggs. Biol. Bull. 26:55–83. Fasenko, G. M., F. E. Robinson, B. L. Danforth, and I. Zelter. 2000. An examination of fertility, hatchability, embryo mortality, and chick weight in double versus single-yolked broiler breeder eggs. Can. J. Anim. Sci. 80:489–493. Fechheimer, N. S., and W. P. Jaffe. 1966. Fertility and embryo death in double-yolked eggs. J. Reprod. Fert. 12:363–364. Kaltofen, R. S. 1971. Embryonic Development in the Eggs of the Pekin Duck. Center for Agricultural Publishing and Documentation, Wageningen, The Netherlands. Monkman, M. 1963. A study of the development of double-yolked eggs. MSc Thesis, Northern Illinois University, DeKalb, Illinois. Roberts, V. 1997. Standard for eggs. Pages 359–362 in British Poultry Standards. 5th ed. V. Roberts, ed. Blackwell Science Ltd., Oxford, UK. Romanoff, A. L., and A. J. Romanoff. 1949. The Avian Egg. John Wiley & Sons Inc., New York. Salamon, A. 2015. Maternal investment – and its constraints – in the egg of domestic waterfowl. PhD Diss. University College Dublin, Dublin, Ireland. Salamon, A., and J. P. Kent. 2013. Double and single yolked duck eggs: their contents and dimensions compared and the mechanical stimulation hypothesis for albumen secretion is supported. Int. J. Poult. Sci. 12:254–260. Salamon, A., and J. P. Kent. 2014. Changes during incubation within double-yolked duck (Anas platyrhynchos domesticus) eggs: yolk position, mortality, hatchability and the importance of an optimal egg size. Int. J. Poult. Sci. 13:695–702. Salamon, A., and J. P. Kent. 2016. Yolk size and ovulation order determine fertility within double yolked duck (Anas platyrhynchos domesticus) eggs. Reprod. Fert. Dev. 28:440–445.
Downloaded from http://ps.oxfordjournals.org/ at University of Pittsburgh on February 17, 2016
Fechheimer and Jaffe, 1966), but lower than yolk fertility in DY (51.9%) and SY duck eggs (89.98%; Salamon and Kent, 2016), and DY (62.5%) and SY broiler breeder eggs (98.44%; Fasenko et al., 2000). Yolks in DY duck eggs are smaller than in SY duck eggs (Salamon and Kent, 2013) and have a lower chance of achieving fertilization that was attributed to early ovulation and / or follicle immaturity (Salamon and Kent, 2016). The small size–within the normal SY duck egg weight range (75 to 104.9 g; Salamon and Kent, 2016)–of TY duck eggs and an associated small yolk size should explain the low fertility of TY duck eggs found here. Two TY eggs were incubated long enough to record egg weight-loss data that was similar to that of DY duck eggs (Salamon, 2015). The one live embryo in Egg 5 entered the airspace on E26 and was transferred to the hatcher. It did not hatch and the post-mortem examination showed that the embryo was internalizing all three yolks, but did not complete this process. Thus, it is possible that a single embryo in TY eggs may reach the point of hatching, as found in DY eggs (domestic fowl, Monkman, 1963; Burke et al., 1997; Fasenko et al., 2000; duck, Salamon and Kent, 2014). It was suggested that there may be an optimal egg weight range to facilitate successful hatching in DY and SY eggs (Monkman, 1963; Salamon and Kent, 2014) and this may also apply to the rare TY duck egg, as Egg 5 was within the ‘optimal’ weight range. However, the relative excess of yolk and/or lack of albumen in DY and TY eggs must also be considered in the context of embryo development and as a constraint on successful hatching.