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Effect of long-term storage on the hatchability of red-legged partridge (Alectoris rufa) eggs
Research Note Effect of long-term storage on the hatchability of red-legged partridge (Alectoris rufa) eggs P. González-Redondo1 Departamento de Ciencias Agroforestales, Escuela Universitaria de Ingeniería Técnica Agrícola, Universidad de Sevilla, 41013 Sevilla, Spain Storage period had a significant effect on hatchability (P < 0.05). Storage of red-legged partridge eggs up to 28 d does not affect subsequent hatchability, but a significant decline in hatchability occurs when the eggs are stored for 35 d. This research confirms, as occurs in other Alectoris species, that long-term storage of redlegged partridge eggs (to 28 d) does not have a negative effect on hatchability. These findings will be useful in terms of successful hatchery management, mainly by allowing prolonged storage of eggs while gathering a sufficient-sized batch to be incubated, and shipment of long shelf life hatching eggs at game farms while losing little hatchability until further incubation.
Key words: red-legged partridge, Alectoris rufa, hatchability, egg storage length, egg weight loss 2010 Poultry Science 89:379–383 doi:10.3382/ps.2009-00408
INTRODUCTION
the time recommended so that the eggs do not lose their viability, which ranges from 7 to 15 d in A. rufa (Almendro, 1979; Beer and Jenkinson, 1981; Pérez y Pérez, 1981; Cancho, 1991; Torres and Garcés, 1995). This maximum duration of time for storing eggs, however, is recommended in informative publications that do not provide experimental evidence. Despite the fact that there are many red-legged partridge farms, there is a lack of scientific studies concerning the hatchability of A. rufa eggs under long-term storage conditions. In order for farmers to improve handling of hatching eggs, reference values of the hatchability of long-term stored red-legged partridge eggs are necessary. These values will be useful in allowing prolonged storage of eggs while a sufficient-sized batch to be incubated is collected and for shipment of long shelf life hatching eggs. The present study investigated the effect of 0-, 7-, 14-, 21-, 28-, and 35-d storage periods on weight loss during the storage period, weight loss during the incubation, and hatchability values of red-legged partridge (A. rufa) eggs.
The red-legged partridge (Alectoris rufa) is a game species raised on farms in countries such as France, Portugal, England, Italy (Coles, 1971; González-Redondo, 2004), and, particularly, Spain, where there are well over 669 farms (Sánchez García-Abad et al., 2009). Medium and large-size farms, which obtain a high yield of hatching eggs, usually load the incubator on a weekly or, at most, fortnightly basis (Almendro, 1979; Pérez y Pérez, 1981; Torres and Garcés, 1995). There are, however, many farms that, having few breeding pairs, store the hatching eggs for longer periods because of the need to assemble a sufficiently large quantity of eggs to fully load the incubator and, subsequently, to raise a batch of chicks (Beer and Jenkinson, 1981; Cancho, 1991). Moreover, due to the remarkable reproductive seasonality of the red-legged partridge (Pérez y Pérez, 1981; Bagliacca et al., 1988; González-Redondo et al., 2003; González-Redondo, 2006), often the period these farms store the eggs at the beginning and at the end of the reproductive season, when the laying frequency is low (Beer and Jenkinson, 1981), far exceeds
MATERIALS AND METHODS Birds and Husbandry
©2010 Poultry Science Association Inc. Received August 18, 2009. Accepted October 26, 2009. 1 Corresponding author: [email protected]
A total of 180 hatching eggs, divided into 6 batches of 30, from a red-legged partridge farm located in Santa 379
Downloaded from http://ps.oxfordjournals.org/ at National Institute of Education Library, Serials Unit on May 31, 2015
ABSTRACT The effect of 0-, 7-, 14-, 21-, 28-, and 35-d storage periods on hatchability and weight loss during storage and incubation of red-legged partridge (Alectoris rufa) eggs stored at 15°C and 80% RH was studied. There was a significant effect of storage period on egg weight loss during storage (P < 0.001), a significant increase occurring in weight loss for each additional week the eggs were stored, and this weight loss amounted to more than 3% for the eggs stored for 35 d. Storage period affected egg weight loss during incubation (P < 0.05). An increase in egg weight loss during incubation occurred, increasing from 21 d of storage and amounting to more than 10% for the eggs stored for 35 d.
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Data Recorded After the 24-d incubation period, the number of hatched chicks and unhatched eggs was recorded. To determine their fertility, nonhatched eggs were analyzed via breakout examination (Ernst et al., 2004). All eggs were weighed before and after storage and after 21 d of incubation. Weight losses during the storage period and after 21 d of incubation were calculated for each individual egg, as a percentage of the initial weight in each phase.
Statistical Methods Statistical differences in the fertility, hatchability of the incubated eggs, and the hatchability of the fertile eggs, as a function of the duration of the storage period, were analyzed using contingency tables on which Pearson’s χ2 tests were performed, and the standardized residuals were calculated. In the interpretation of the standardized residuals, 1.96 was considered to be the discriminant value for a confidence level of 95%. Statistical differences in the initial and final weights and weight losses of the fertile eggs during storage and incubation periods, as a function of the duration of the storage period, were analyzed by 1-way ANOVA. When differences among storage periods were significant, means were separated using Duncan’s multiple range tests at the 0.05 level of significance. Pearson
correlations were performed to analyze the relationship between weight losses of the fertile eggs during storage and incubation periods. The analyses were conducted using SPSS 15.0 software (SPSS Inc., 2006).
RESULTS AND DISCUSSION The number of incubated eggs, fertile eggs, and hatched eggs; the fertility and hatchability of the incubated eggs; as well as the hatchability of the fertile eggs, according to their storage time before incubation, are shown in Table 1. The average fertility of the eggs recorded in this study (85.6%) was slightly higher than in previous reports on A. rufa under farming conditions (73.5 to 81.6%; Bagliacca et al., 1988; Paci et al., 1992; González-Redondo, 2006). The average hatchability of the incubated eggs (65%) was within the range of values found in the literature (53.4 to 84.1%; Mori et al., 1985; Paci et al., 1992; González-Redondo et al., 2003; González-Redondo, 2006). The average hatchability of the fertile eggs we recorded (76%) showed a value similar to those reported for this species (72.6 to 91.6%; Bagliacca et al., 1988; Paci et al., 1992; González-Redondo, 2006). No differences were found in the fertility of the incubated eggs among the experimental batches (χ2 = 1.978, df = 5, P = 0.852). Marginal differences were found in the hatchability of the total of the incubated eggs (χ2 = 10.769, df = 5, P = 0.056), but significant differences were found in the hatchability of the fertile eggs (χ2 = 13.420, df = 5, P = 0.020) according to the duration of the storage period before the incubation. No significant effect of storage time was found on hatchability of eggs stored up to 28 d before incubation, but eggs stored for 35 d showed a significant decrease in hatchability (Table 1), amounting to more than onethird when the eggs were held beyond 28 d. Previous scientific reports have not evaluated the variation in hatchability of the red-legged partridge (A. rufa) eggs under long-term storage conditions. Interestingly, our results coincide with findings of Woodard and Morzenti (1975) in Alectoris graeca, a species whose eggs have no appreciable loss in hatchability when held up to 28 d under similar conditions (egg storage at 16°C and 70% RH) to our experiment. In addition, Özbey and Esen (2007) and Çağlayan et al. (2009) found that hatchability of A. graeca eggs is not affected when stored up to 14 d at 14°C and 75% RH. Our findings also partly coincide with Beer and Jenkinson (1981), who found that placing the red-legged partridge (A. rufa) eggs in plastic bags that were folded underneath to form a partial seal during storage improves hatchability when the eggs were stored up to 3 to 5 wk at 13 to 15°C and 70 to 80% RH. The length of time hatching eggs can be held without impairment to the potential embryo may depend upon several factors, such as genotype, age and performance of the breeders, and temperature, humidity, and turning and small end position of the eggs during
Downloaded from http://ps.oxfordjournals.org/ at National Institute of Education Library, Serials Unit on May 31, 2015
Cruz (province of Córdoba, Southern Spain) were used. The breeding partridges, with ages of 2 and 3 yr old, were fed with commercial feed (20% CP and 2,800 kcal/ kg of ME) and were housed in pairs in outdoor cages measuring 40 × 100 cm. The partridges were initially subjected to natural lighting, but from December 15, artificial lighting was added, increasing the photoperiod by a quarter of an hour every 3 d until, in the first week of February, a complete photoperiod (natural light + artificial light) of 16 h of light was reached. Egg laying commenced during the first week of February. From March 19 onward, 6 batches of eggs were collected at weekly intervals and were kept small end down at 15°C and 80% RH, being turned 2 times per day at regular intervals. Sampling was carried out in this intermediate date to avoid low fertility of eggs laid at the beginning and at the end of the laying period, given the reproductive seasonality of this species (González-Redondo, 2006). The storage periods of the egg batches were as follows: batch 1, 35 d; batch 2, 28 d; batch 3, 21 d; batch 4, 14 d; batch 5, 7 d; and batch 6, 0 d. Twelve hours before being loaded in the incubator, the eggs were prewarmed at 23°C and 65% RH by maintaining them in the room where the incubator itself was located. All of the eggs were loaded into the incubator on the same date. The eggs were incubated at 37.8°C and 55% RH during the first 21 d, being turned every hour, and thereafter were incubated at 37.5°C and 80% RH without turning them until the hatch.
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RESEARCH NOTE Table 1. Fertility and hatchability of red-legged partridge eggs according to the length of the storage period Number of eggs Storage period (d) 0 7 14 21 28 35 Total P-value
Incubated
Fertile
Hatched
30 30 30 30 30 30 180
27 25 27 25 24 26 154
22 19 24 21 18 13 117
Fertility1 (%)
Hatchability2 (%)
Hatchability of the fertile eggs3 (%)
90.0 83.3 90.0 83.3 80.0 86.7 85.6 NS
73.3a 63.3a 80.0a 70.0a 60.0a 43.3b 65.0 †
81.5x 76.0x 88.9x 84.0x 75.0x 50.0y 76.0 *
a,b
storage (Bowman, 1969; Woodard and Morzenti, 1975; Beer and Jenkinson, 1981; Lapão et al., 1999; Fasenko, 2007). Because these variables were held constant in the present experiment, the observed reduction in viability of eggs stored more than a month was probably caused in part by the deterioration of embryo quality due to aging, as occurs in other poultry species (Woodard and Morzenti, 1975; Fasenko, 2007), and seemed to be related to the egg weight loss (Hassan et al., 2005; Romao et al., 2008). To illustrate this, the initial and final weights during the storage period, the weight at 21 d of incubation, and weight losses of the fertile eggs during storage and incubation periods, as a function of the length of time hatching eggs were stored before incubation, are shown in Table 2. No differences were found in the initial weight of the fertile eggs before their storage (χ2 = 297.97, df = 7, P < 0.607). Recently laid egg weight matches well with that described for A. rufa (Beer and Jenkinson, 1981; Pérez y Pérez, 1981) and other species of the Alectoris genus (Kırıkçı et al., 2004; Tilki and Saatci, 2004;
Çağlayan et al., 2009). Highly significant differences were found in fertile egg weight loss during the storage period as a function of its length (χ2 = 183.02, df = 7, P < 0.001). The fertile egg weight loss progressively increased with storage time before incubation, the eggs stored for 35 d showing the maximum weight loss (more than 3%). The egg weight loss observed during storage in the present research followed the expected pattern and was slightly higher than that found by Beer and Jenkinson (1981) for red-legged partridge (A. rufa) bagged eggs when stored at 13 to 15°C and 70 to 80% RH and by Tilki and Saatci (2004) for rock partridge (A. graeca) eggs when stored at room temperature (15 to 18°C) and unspecified RH. Our observations in the sense that long-term stored eggs may lose weight due to water loss, something that can affect viability of the eggs, confirm the findings of other authors for A. graeca. When storage period is lengthened, internal quality in rock partridge eggs (yolk ratio, yolk index, albumen ratio, albumen index, and Haugh unit) progressively deteriorate, something that is related with losing mois-
Table 2. Egg weight and egg weight losses during storage and incubation periods in red-legged partridge fertile eggs according to the length of the storage period1 Storage period (d) 0 7 14 21 28 35 Total P-value a–d
Number of eggs 27 25 27 25 24 26 154
Egg weight before storage (g)
Egg weight after storage (g)
Egg weight loss during storage2 (%)
19.46 ± 0.23 19.30 ± 0.18 19.75 ± 0.21 19.18 ± 0.23 19.48 ± 0.26 19.41 ± 0.27 19.43 ± 0.09 NS
19.46 ± 0.23 19.22 ± 0.18 19.54 ± 0.21 18.91 ± 0.22 19.09 ± 0.27 18.81 ± 0.29 19.18 ± 0.10 NS
0.00 0.39 1.07 1.42 2.02 3.13 1.33
± 0.00d ± 0.05d ± 0.21c ± 0.08c ± 0.12b ± 0.29a ± 0.11 ***
Egg weight at 21 d of incubation (g) 17.77 17.59 17.89 17.10 17.32 16.89 17.43
± 0.21a ± 0.19ab ± 0.22a ± 0.25ab ± 0.28ab ± 0.36b ± 0.11 *
Values in the same column with different superscripts are significantly different (P < 0.05). Mean ± SEM. 2 Values are expressed as a percentage of egg weight at the beginning of storage period. 3 Values are expressed as a percentage of egg weight at the beginning of incubation. 4 Pearson correlations between weight losses during storage and incubation periods. *P < 0.05; ***P < 0.001. 1
Egg weight loss after 21 d of incubation3 (%) 8.67 8.50 8.50 9.58 9.31 10.40 9.15
± 0.21bc ± 0.40bc ± 0.28bc ± 0.53ab ± 0.46ab ± 0.81a ± 0.20 *
Weight loss correlation4 r r r r r r r
= = = = = = =
0.000; 0.308; 0.133; 0.811; 0.858; 0.983; 0.599;
P P P P P P P
= = = < < < <
1.000 0.134 0.507 0.001 0.001 0.001 0.001
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Values in the same column with different superscripts are marginally different (P < 0.1). Values in the same column with different superscripts are significantly different (P < 0.05). 1 Percentage of incubated eggs that were fertile. 2 Percentage of incubated eggs that hatched. 3 Percentage of fertile eggs that hatched. †P < 0.1; *P < 0.05. x,y
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is of considerable importance to the farmer, who may store eggs for many days to accumulate greater numbers, mainly for 2 reasons. The first reason is to hatch, at the beginning and at the end of the laying season, a useful-sized batch of chicks for rearing and release, reducing the need to incubate small batches or to discard the earliest and latest eggs (Beer and Jenkinson, 1981), which are laid at a low rate because the egg production increases and decreases slowly in these periods of the laying season, given the remarkable reproductive seasonality of this species (González-Redondo, 2006). The second reason is for shipment of long shelf life hatching eggs, one of the commercial products in countries with a well-developed market for red-legged partridge game farms (González-Redondo, 1999, 2006) while losing little hatchability until further incubation.
REFERENCES Almendro, F. 1979. Cría industrial de la perdiz roja. Hojas Divulgadoras del Ministerio de Agricultura 11–12:1–24. Arnold, T. W., F. C. Rohwer, and T. Armstrong. 1987. Egg viability, nest predation, and the adaptive significance of clutch size in prairie ducks. Am. Nat. 130:643–653. Bagliacca, M., B. Mori, and L. Gualterio. 1988. Egg laying under artificial photo-regulation in the red partridge. Pages 657–659 in Proc. 18th World’s Poultry Congress, Nagoya, Japan. Japan Poultry Science Association, Nagoya, Japan. Beer, J., and G. Jenkinson. 1981. The storage of red-legged partridge eggs. A suggestion for trials. Game Conservancy Annu. Rev. 12:80–82. Bowman, J. C. 1969. Storage of hatching eggs. 2. Evidence of genotype × environment interactions. Br. Poult. Sci. 10:19–28. Çağlayan, T., S. Alaşahan, K. Kırıkçı, and A. Günlü. 2009. Effect of different egg storage periods on some egg quality characteristics and hatchability of partridges (Alectoris graeca). Poult. Sci. 88:1330–1333. Cancho, M. 1991. Incubación. Equipo y técnicas de manejo. Control. Pages 21–27 in La Perdiz Roja. Fundación La Caixa. AEDOS, Barcelona, Spain. Casas, F. 2008. Gestión agraria y cinegética: Efectos sobre la perdiz roja (Alectoris rufa) y aves esteparias protegidas. PhD Thesis. Universidad de Castilla-La Mancha (UCLM) e Instituto de Investigación en Recursos Cinegéticos (IREC-CSIC), Albacete, Spain. Coles, C. 1971. The Complete Book of Game Conservation. Barrie & Jenkins Ltd., London, UK. Ernst, R. A., F. A. Bradley, U. K. Abbott, and R. M. Craig. 2004. Egg candling and breakout analysis. ANR Publication 8134. http:// anrcatalog.ucdavis.edu/pdf/8134.pdf Accessed Mar. 2007. Fasenko, G. M. 2007. Egg storage and the embryo. Poult. Sci. 86:1020–1024. González-Redondo, P. 1999. Marketing y comercialización de la producción en las granjas cinegéticas de perdiz roja. Selecciones Avícolas 41:494–508. González-Redondo, P. 2004. Un caso de cambio en el manejo de los recursos cinegéticos: La historia de la cría en cautividad de la perdiz roja en España. Rev. Esp. Estud. Agrosoc. Pesq. 204:179–203. González-Redondo, P. 2006. Influence of the laying date on the fertility and hatchability of red-legged partridge (Alectoris rufa) eggs. J. Appl. Poult. Res. 15:579–583. González-Redondo, P., M. Delgado, and M. Reina. 2003. Caracterización de la puesta y su viabilidad en una granja cinegética de perdiz roja (Alectoris rufa). Pages 182–183 in Proc. 2nd Jornadas Ibéricas de Razas Autóctonas y sus Productos Tradicionales: Ganadería Ecológica, Sevilla, Spain. Consejería de Agricultura y Pesca, Junta de Andalucía, Sevilla, Spain..
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ture from the egg (Tilki and Saatci, 2004; Çağlayan et al., 2009). Significant differences were found in fertile egg weight loss at 21 d of incubation as a function of the storage time (χ2 = 183.02, df = 7, P = 0.037). The weight loss of the fertile eggs during incubation progressively increased for batches of eggs stored for longer periods before their incubation, the eggs stored for 35 d showing the maximum weight loss, whereas these losses remained invariable for eggs stored up to 21 d. Egg weight loss during the 21 first days of incubation was clearly linked to egg weight loss during the storage period (r = 0.599; P < 0.001). The weight loss during incubation, potentiated in batches of eggs stored for longer periods, was responsible for the decrease in hatchability that we observed and partly coincides with that observed for the rock partridge, a species showing low hatchability for eggs with extreme percentage mass loss during incubation (Kırıkçı et al., 2004). The nesting behavior of red-legged partridges in the wild can help to explain the longevity of eggs from this species. In most precocial birds, when eggs are exposed to natural microclimates, hatching success declines markedly (Arnold et al., 1987). Alectoris rufa is an exception because egg viability in the wild remains high for about 25 d and declines sharply thereafter (Green, 1984; Casas, 2008), this being consistent with our findings under farming conditions. Two mechanisms explain this adaptive pattern. First, this species seems to prefer a warm, dry climate over most of its range (Pérez y Pérez, 1981), where red-legged partridge, which has a long laying interval, often broods a clutch of eggs that has been left for 3 wk, and some of the eggs must be 5 or 6 wk old before brooding starts (Coles, 1971). Under these conditions A. rufa eggs stand continual exposure to full sun, often alternating with frosty nights on a bare, dry fallow or chalk down (Coles, 1971). Second, red-legged partridges often produce double clutches, and males delay brooding the first until females complete the second clutch (Green, 1984; Casas, 2008). Both ecological constraint and breeding system in the wild have acted as selection mechanisms for prolonged egg viability before incubation. When comparisons are made with figures published in the literature, the length of time red-legged partridge (A. rufa) hatching eggs can be held without decline in hatchability is higher than that for most poultry species (Woodard and Morzenti, 1975; Wilson et al., 1997; Fasenko, 2007; Romao et al., 2008) and, as Woodard and Morzenti (1975) stated, apparently resulted from genetic variability among species. In conclusion, the red-legged partridge (A. rufa) eggs store well with little deterioration for 1 mo in contrast to the lesser durability of eggs from other poultry species. After this initial period, however, hatchability is liable to decline rapidly even under a steady cool temperature, high humidity, and regular turning during storage before incubation. The length of time hatching eggs can be held without impairment to the potential embryo
RESEARCH NOTE
Pérez y Pérez, F. 1981. La perdiz roja española. Editorial CientíficoMédica, Barcelona, Spain. Romao, J. M., T. G. V. Moraes, R. S. C. Teixeira, W. M. Cardoso, and C. C. Buxade. 2008. Effect of egg storage length on hatchability and weight loss in incubation of egg and meat type Japanese quails. Braz. J. Poult. Sci. 10:143–147. Sánchez García-Abad, C., M. E. Alonso, R. Prieto, V. Eguren, and V. Gaudioso. 2009. Una visión sobre la avicultura para la producción de caza en España. ITEA 105:169–183. SPSS Inc. 2006. Manual del Usuario de SPSS Base 15.0. SPSS Inc., Chicago, IL. Tilki, M., and M. Saatci. 2004. Effects of storage time on external and internal characteristics in partridge (Alectoris graeca) eggs. Rev. Méd. Vét. 155:561–564. Torres, A., and C. Garcés. 1995. La explotación de la perdiz. Pages 345–363 in Zootecnia. Bases de Producción Animal. Vol. 5. Mundi-Prensa, Madrid, Spain. Wilson, H. R., A. R. Eldred, and C. J. Wilcox. 1997. Storage time and ostrich egg hatchability. J. Appl. Poult. Res. 6:216–220. Woodard, A. E., and A. Morzenti. 1975. Effect of turning and age of egg on hatchability in the pheasant, chukar, and Japanese quail. Poult. Sci. 54:1708–1711.
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Green, R. E. 1984. Double nesting of the red-legged partridge Alectoris rufa. Ibis 126:332–346. Hassan, S. M., A. A. Siam, M. E. Mady, and A. L. Cartwright. 2005. Egg storage period and weight effects on hatchability of ostrich (Struthio camelus) eggs. Poult. Sci. 84:1908–1912. Kırıkçı, K., D. C. Deeming, and A. Günlü. 2004. Effects of egg mass and percentage mass loss during incubation on hatchability of eggs of the rock partridge. Br. Poult. Sci. 45:380–384. Lapão, C., L. T. Gama, and M. C. Soares. 1999. Effects of broiler breeder age and length of egg storage on albumen characteristics and hatchability. Poult. Sci. 70:640–645. Mori, B., M. Bagliacca, M. Chiarcossi, and I. Romboli. 1985. Performances riproduttive della pernice rossa allevata in Liguria. Riv. Avic. 54:27–32. Özbey, O., and F. Esen. 2007. The effect of storage period on hatchability characteristics of rock partridges (Alectoris graeca). J. Anim. Vet. Adv. 6:466–469. Paci, G., M. Marzoni, N. Benvenuti, and M. Bagliacca. 1992. Breeding technology of red partridges: Colonies or couples. Pages 351– 352 in Proc. 19th World’s Poultry Congress, Amsterdam, the Netherlands. World’s Poultry Science Association, Netherlands Branch, Wageningen, the Netherlands
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Key words: red-legged partridge, Alectoris rufa, hatchability, egg storage length, egg weight loss 2010 Poultry Science 89:379–383 doi:10.3382/ps.2009-00408
INTRODUCTION
the time recommended so that the eggs do not lose their viability, which ranges from 7 to 15 d in A. rufa (Almendro, 1979; Beer and Jenkinson, 1981; Pérez y Pérez, 1981; Cancho, 1991; Torres and Garcés, 1995). This maximum duration of time for storing eggs, however, is recommended in informative publications that do not provide experimental evidence. Despite the fact that there are many red-legged partridge farms, there is a lack of scientific studies concerning the hatchability of A. rufa eggs under long-term storage conditions. In order for farmers to improve handling of hatching eggs, reference values of the hatchability of long-term stored red-legged partridge eggs are necessary. These values will be useful in allowing prolonged storage of eggs while a sufficient-sized batch to be incubated is collected and for shipment of long shelf life hatching eggs. The present study investigated the effect of 0-, 7-, 14-, 21-, 28-, and 35-d storage periods on weight loss during the storage period, weight loss during the incubation, and hatchability values of red-legged partridge (A. rufa) eggs.
The red-legged partridge (Alectoris rufa) is a game species raised on farms in countries such as France, Portugal, England, Italy (Coles, 1971; González-Redondo, 2004), and, particularly, Spain, where there are well over 669 farms (Sánchez García-Abad et al., 2009). Medium and large-size farms, which obtain a high yield of hatching eggs, usually load the incubator on a weekly or, at most, fortnightly basis (Almendro, 1979; Pérez y Pérez, 1981; Torres and Garcés, 1995). There are, however, many farms that, having few breeding pairs, store the hatching eggs for longer periods because of the need to assemble a sufficiently large quantity of eggs to fully load the incubator and, subsequently, to raise a batch of chicks (Beer and Jenkinson, 1981; Cancho, 1991). Moreover, due to the remarkable reproductive seasonality of the red-legged partridge (Pérez y Pérez, 1981; Bagliacca et al., 1988; González-Redondo et al., 2003; González-Redondo, 2006), often the period these farms store the eggs at the beginning and at the end of the reproductive season, when the laying frequency is low (Beer and Jenkinson, 1981), far exceeds
MATERIALS AND METHODS Birds and Husbandry
©2010 Poultry Science Association Inc. Received August 18, 2009. Accepted October 26, 2009. 1 Corresponding author: [email protected]
A total of 180 hatching eggs, divided into 6 batches of 30, from a red-legged partridge farm located in Santa 379
Downloaded from http://ps.oxfordjournals.org/ at National Institute of Education Library, Serials Unit on May 31, 2015
ABSTRACT The effect of 0-, 7-, 14-, 21-, 28-, and 35-d storage periods on hatchability and weight loss during storage and incubation of red-legged partridge (Alectoris rufa) eggs stored at 15°C and 80% RH was studied. There was a significant effect of storage period on egg weight loss during storage (P < 0.001), a significant increase occurring in weight loss for each additional week the eggs were stored, and this weight loss amounted to more than 3% for the eggs stored for 35 d. Storage period affected egg weight loss during incubation (P < 0.05). An increase in egg weight loss during incubation occurred, increasing from 21 d of storage and amounting to more than 10% for the eggs stored for 35 d.
380
González-Redondo
Data Recorded After the 24-d incubation period, the number of hatched chicks and unhatched eggs was recorded. To determine their fertility, nonhatched eggs were analyzed via breakout examination (Ernst et al., 2004). All eggs were weighed before and after storage and after 21 d of incubation. Weight losses during the storage period and after 21 d of incubation were calculated for each individual egg, as a percentage of the initial weight in each phase.
Statistical Methods Statistical differences in the fertility, hatchability of the incubated eggs, and the hatchability of the fertile eggs, as a function of the duration of the storage period, were analyzed using contingency tables on which Pearson’s χ2 tests were performed, and the standardized residuals were calculated. In the interpretation of the standardized residuals, 1.96 was considered to be the discriminant value for a confidence level of 95%. Statistical differences in the initial and final weights and weight losses of the fertile eggs during storage and incubation periods, as a function of the duration of the storage period, were analyzed by 1-way ANOVA. When differences among storage periods were significant, means were separated using Duncan’s multiple range tests at the 0.05 level of significance. Pearson
correlations were performed to analyze the relationship between weight losses of the fertile eggs during storage and incubation periods. The analyses were conducted using SPSS 15.0 software (SPSS Inc., 2006).
RESULTS AND DISCUSSION The number of incubated eggs, fertile eggs, and hatched eggs; the fertility and hatchability of the incubated eggs; as well as the hatchability of the fertile eggs, according to their storage time before incubation, are shown in Table 1. The average fertility of the eggs recorded in this study (85.6%) was slightly higher than in previous reports on A. rufa under farming conditions (73.5 to 81.6%; Bagliacca et al., 1988; Paci et al., 1992; González-Redondo, 2006). The average hatchability of the incubated eggs (65%) was within the range of values found in the literature (53.4 to 84.1%; Mori et al., 1985; Paci et al., 1992; González-Redondo et al., 2003; González-Redondo, 2006). The average hatchability of the fertile eggs we recorded (76%) showed a value similar to those reported for this species (72.6 to 91.6%; Bagliacca et al., 1988; Paci et al., 1992; González-Redondo, 2006). No differences were found in the fertility of the incubated eggs among the experimental batches (χ2 = 1.978, df = 5, P = 0.852). Marginal differences were found in the hatchability of the total of the incubated eggs (χ2 = 10.769, df = 5, P = 0.056), but significant differences were found in the hatchability of the fertile eggs (χ2 = 13.420, df = 5, P = 0.020) according to the duration of the storage period before the incubation. No significant effect of storage time was found on hatchability of eggs stored up to 28 d before incubation, but eggs stored for 35 d showed a significant decrease in hatchability (Table 1), amounting to more than onethird when the eggs were held beyond 28 d. Previous scientific reports have not evaluated the variation in hatchability of the red-legged partridge (A. rufa) eggs under long-term storage conditions. Interestingly, our results coincide with findings of Woodard and Morzenti (1975) in Alectoris graeca, a species whose eggs have no appreciable loss in hatchability when held up to 28 d under similar conditions (egg storage at 16°C and 70% RH) to our experiment. In addition, Özbey and Esen (2007) and Çağlayan et al. (2009) found that hatchability of A. graeca eggs is not affected when stored up to 14 d at 14°C and 75% RH. Our findings also partly coincide with Beer and Jenkinson (1981), who found that placing the red-legged partridge (A. rufa) eggs in plastic bags that were folded underneath to form a partial seal during storage improves hatchability when the eggs were stored up to 3 to 5 wk at 13 to 15°C and 70 to 80% RH. The length of time hatching eggs can be held without impairment to the potential embryo may depend upon several factors, such as genotype, age and performance of the breeders, and temperature, humidity, and turning and small end position of the eggs during
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Cruz (province of Córdoba, Southern Spain) were used. The breeding partridges, with ages of 2 and 3 yr old, were fed with commercial feed (20% CP and 2,800 kcal/ kg of ME) and were housed in pairs in outdoor cages measuring 40 × 100 cm. The partridges were initially subjected to natural lighting, but from December 15, artificial lighting was added, increasing the photoperiod by a quarter of an hour every 3 d until, in the first week of February, a complete photoperiod (natural light + artificial light) of 16 h of light was reached. Egg laying commenced during the first week of February. From March 19 onward, 6 batches of eggs were collected at weekly intervals and were kept small end down at 15°C and 80% RH, being turned 2 times per day at regular intervals. Sampling was carried out in this intermediate date to avoid low fertility of eggs laid at the beginning and at the end of the laying period, given the reproductive seasonality of this species (González-Redondo, 2006). The storage periods of the egg batches were as follows: batch 1, 35 d; batch 2, 28 d; batch 3, 21 d; batch 4, 14 d; batch 5, 7 d; and batch 6, 0 d. Twelve hours before being loaded in the incubator, the eggs were prewarmed at 23°C and 65% RH by maintaining them in the room where the incubator itself was located. All of the eggs were loaded into the incubator on the same date. The eggs were incubated at 37.8°C and 55% RH during the first 21 d, being turned every hour, and thereafter were incubated at 37.5°C and 80% RH without turning them until the hatch.
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RESEARCH NOTE Table 1. Fertility and hatchability of red-legged partridge eggs according to the length of the storage period Number of eggs Storage period (d) 0 7 14 21 28 35 Total P-value
Incubated
Fertile
Hatched
30 30 30 30 30 30 180
27 25 27 25 24 26 154
22 19 24 21 18 13 117
Fertility1 (%)
Hatchability2 (%)
Hatchability of the fertile eggs3 (%)
90.0 83.3 90.0 83.3 80.0 86.7 85.6 NS
73.3a 63.3a 80.0a 70.0a 60.0a 43.3b 65.0 †
81.5x 76.0x 88.9x 84.0x 75.0x 50.0y 76.0 *
a,b
storage (Bowman, 1969; Woodard and Morzenti, 1975; Beer and Jenkinson, 1981; Lapão et al., 1999; Fasenko, 2007). Because these variables were held constant in the present experiment, the observed reduction in viability of eggs stored more than a month was probably caused in part by the deterioration of embryo quality due to aging, as occurs in other poultry species (Woodard and Morzenti, 1975; Fasenko, 2007), and seemed to be related to the egg weight loss (Hassan et al., 2005; Romao et al., 2008). To illustrate this, the initial and final weights during the storage period, the weight at 21 d of incubation, and weight losses of the fertile eggs during storage and incubation periods, as a function of the length of time hatching eggs were stored before incubation, are shown in Table 2. No differences were found in the initial weight of the fertile eggs before their storage (χ2 = 297.97, df = 7, P < 0.607). Recently laid egg weight matches well with that described for A. rufa (Beer and Jenkinson, 1981; Pérez y Pérez, 1981) and other species of the Alectoris genus (Kırıkçı et al., 2004; Tilki and Saatci, 2004;
Çağlayan et al., 2009). Highly significant differences were found in fertile egg weight loss during the storage period as a function of its length (χ2 = 183.02, df = 7, P < 0.001). The fertile egg weight loss progressively increased with storage time before incubation, the eggs stored for 35 d showing the maximum weight loss (more than 3%). The egg weight loss observed during storage in the present research followed the expected pattern and was slightly higher than that found by Beer and Jenkinson (1981) for red-legged partridge (A. rufa) bagged eggs when stored at 13 to 15°C and 70 to 80% RH and by Tilki and Saatci (2004) for rock partridge (A. graeca) eggs when stored at room temperature (15 to 18°C) and unspecified RH. Our observations in the sense that long-term stored eggs may lose weight due to water loss, something that can affect viability of the eggs, confirm the findings of other authors for A. graeca. When storage period is lengthened, internal quality in rock partridge eggs (yolk ratio, yolk index, albumen ratio, albumen index, and Haugh unit) progressively deteriorate, something that is related with losing mois-
Table 2. Egg weight and egg weight losses during storage and incubation periods in red-legged partridge fertile eggs according to the length of the storage period1 Storage period (d) 0 7 14 21 28 35 Total P-value a–d
Number of eggs 27 25 27 25 24 26 154
Egg weight before storage (g)
Egg weight after storage (g)
Egg weight loss during storage2 (%)
19.46 ± 0.23 19.30 ± 0.18 19.75 ± 0.21 19.18 ± 0.23 19.48 ± 0.26 19.41 ± 0.27 19.43 ± 0.09 NS
19.46 ± 0.23 19.22 ± 0.18 19.54 ± 0.21 18.91 ± 0.22 19.09 ± 0.27 18.81 ± 0.29 19.18 ± 0.10 NS
0.00 0.39 1.07 1.42 2.02 3.13 1.33
± 0.00d ± 0.05d ± 0.21c ± 0.08c ± 0.12b ± 0.29a ± 0.11 ***
Egg weight at 21 d of incubation (g) 17.77 17.59 17.89 17.10 17.32 16.89 17.43
± 0.21a ± 0.19ab ± 0.22a ± 0.25ab ± 0.28ab ± 0.36b ± 0.11 *
Values in the same column with different superscripts are significantly different (P < 0.05). Mean ± SEM. 2 Values are expressed as a percentage of egg weight at the beginning of storage period. 3 Values are expressed as a percentage of egg weight at the beginning of incubation. 4 Pearson correlations between weight losses during storage and incubation periods. *P < 0.05; ***P < 0.001. 1
Egg weight loss after 21 d of incubation3 (%) 8.67 8.50 8.50 9.58 9.31 10.40 9.15
± 0.21bc ± 0.40bc ± 0.28bc ± 0.53ab ± 0.46ab ± 0.81a ± 0.20 *
Weight loss correlation4 r r r r r r r
= = = = = = =
0.000; 0.308; 0.133; 0.811; 0.858; 0.983; 0.599;
P P P P P P P
= = = < < < <
1.000 0.134 0.507 0.001 0.001 0.001 0.001
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Values in the same column with different superscripts are marginally different (P < 0.1). Values in the same column with different superscripts are significantly different (P < 0.05). 1 Percentage of incubated eggs that were fertile. 2 Percentage of incubated eggs that hatched. 3 Percentage of fertile eggs that hatched. †P < 0.1; *P < 0.05. x,y
382
González-Redondo
is of considerable importance to the farmer, who may store eggs for many days to accumulate greater numbers, mainly for 2 reasons. The first reason is to hatch, at the beginning and at the end of the laying season, a useful-sized batch of chicks for rearing and release, reducing the need to incubate small batches or to discard the earliest and latest eggs (Beer and Jenkinson, 1981), which are laid at a low rate because the egg production increases and decreases slowly in these periods of the laying season, given the remarkable reproductive seasonality of this species (González-Redondo, 2006). The second reason is for shipment of long shelf life hatching eggs, one of the commercial products in countries with a well-developed market for red-legged partridge game farms (González-Redondo, 1999, 2006) while losing little hatchability until further incubation.
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ture from the egg (Tilki and Saatci, 2004; Çağlayan et al., 2009). Significant differences were found in fertile egg weight loss at 21 d of incubation as a function of the storage time (χ2 = 183.02, df = 7, P = 0.037). The weight loss of the fertile eggs during incubation progressively increased for batches of eggs stored for longer periods before their incubation, the eggs stored for 35 d showing the maximum weight loss, whereas these losses remained invariable for eggs stored up to 21 d. Egg weight loss during the 21 first days of incubation was clearly linked to egg weight loss during the storage period (r = 0.599; P < 0.001). The weight loss during incubation, potentiated in batches of eggs stored for longer periods, was responsible for the decrease in hatchability that we observed and partly coincides with that observed for the rock partridge, a species showing low hatchability for eggs with extreme percentage mass loss during incubation (Kırıkçı et al., 2004). The nesting behavior of red-legged partridges in the wild can help to explain the longevity of eggs from this species. In most precocial birds, when eggs are exposed to natural microclimates, hatching success declines markedly (Arnold et al., 1987). Alectoris rufa is an exception because egg viability in the wild remains high for about 25 d and declines sharply thereafter (Green, 1984; Casas, 2008), this being consistent with our findings under farming conditions. Two mechanisms explain this adaptive pattern. First, this species seems to prefer a warm, dry climate over most of its range (Pérez y Pérez, 1981), where red-legged partridge, which has a long laying interval, often broods a clutch of eggs that has been left for 3 wk, and some of the eggs must be 5 or 6 wk old before brooding starts (Coles, 1971). Under these conditions A. rufa eggs stand continual exposure to full sun, often alternating with frosty nights on a bare, dry fallow or chalk down (Coles, 1971). Second, red-legged partridges often produce double clutches, and males delay brooding the first until females complete the second clutch (Green, 1984; Casas, 2008). Both ecological constraint and breeding system in the wild have acted as selection mechanisms for prolonged egg viability before incubation. When comparisons are made with figures published in the literature, the length of time red-legged partridge (A. rufa) hatching eggs can be held without decline in hatchability is higher than that for most poultry species (Woodard and Morzenti, 1975; Wilson et al., 1997; Fasenko, 2007; Romao et al., 2008) and, as Woodard and Morzenti (1975) stated, apparently resulted from genetic variability among species. In conclusion, the red-legged partridge (A. rufa) eggs store well with little deterioration for 1 mo in contrast to the lesser durability of eggs from other poultry species. After this initial period, however, hatchability is liable to decline rapidly even under a steady cool temperature, high humidity, and regular turning during storage before incubation. The length of time hatching eggs can be held without impairment to the potential embryo
RESEARCH NOTE
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