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Article

Effects of Sibling Eggs Contact on Incubation Length and Hatching Synchrony in Red-Legged Partridge (Alectoris rufa)

by
Pedro González-Redondo
* and
Fátima Quesada-Pérez
Departamento de Agronomía, Universidad de Sevilla, Carretera de Utrera km 1, 41013 Seville, Spain
*
Author to whom correspondence should be addressed.
Appl. Sci. 2022, 12(11), 5586; https://doi.org/10.3390/app12115586
Submission received: 1 May 2022 / Revised: 26 May 2022 / Accepted: 30 May 2022 / Published: 31 May 2022
(This article belongs to the Section Agricultural Science and Technology)
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Abstract

:
Hatching synchrony is a desirable trait in the artificial incubation of eggs because it permits the simultaneous extraction of all the chicks from the hatcher, thus minimizing extraction queues. This study aimed at evaluating the effects on egg performance, incubation length, and hatching synchrony of different sibling contact regimes during the incubation in red-legged partridge (Alectoris rufa) eggs. To achieve these objectives, 196 eggs were arranged in four treatments according to the sibling eggs contact regime: (a) eggs without contact during the whole incubation process; (b) eggs in contact during the incubation phase (from day 1 to 20 of incubation); (c) eggs in contact during the hatching phase (from day 20 of incubation to hatching); (d) eggs in permanent contact throughout the incubation process (from day 1 of incubation to hatching). Development stage at embryonic mortality, hatchability, and egg weight loss during incubation were not affected, but incubation length was shortened and hatching synchrony was increased in eggs in contact during the hatching phase. The main conclusion was that keeping red-legged partridge eggs in close contact during the hatching stage in the artificial incubation does not affect hatchability but allows hatching synchrony to be maximized, facilitating the handling of 1 day old chicks.

1. Introduction

The red-legged partridge (Alectoris rufa Linnaeus, 1758) is a wild species raised in game farms in several European countries such as France, Italy, Portugal, the United Kingdom, and especially Spain, where, in 2020, there were 2736 registered farms and a well-developed market [1,2,3,4]. This palearctic partridge is mainly raised for two purposes related to hunting management: to increase hunting bags and to provide birds for population re-establishment [2,5]. Most of the red-legged partridge game farms are complete-cycle farms [3] that incubate the eggs obtained during the laying season through artificial incubation, a technique that is key to their productivity. Hatching eggs management and artificial incubation technology in A. rufa are recently receiving attention from the research community [6,7,8,9,10,11,12]. However, in spite of the relevance of the red-legged partridge game farm subsector, various aspects of the artificial incubation remain to be rigorously investigated.
One aspect that has not received sufficient attention in red-legged partridge is related to incubation length and hatching synchrony under artificial incubation. It is known that several factors, e.g., egg storage length and temperature [9] and incubation temperature regime [10], modify incubation length and hatching synchrony in this species. However, scientific research concerning A. rufa eggs hatching synchrony under artificial incubation as a function of the contact regime among eggs is lacking. As a precocial bird, the red-legged partridge brood hatches synchronously in the wild in order to leave the nest quickly after hatching, as an efficient strategy to minimize predation losses [13]. Hatching synchrony is achieved in precocial phasianids through mechanisms involving sibling contact and sound emission among the embryos of the clutch [14,15]. This pattern is maintained in the artificial incubation [8,16], although the timing of the mechanism via which hatching synchrony is achieved remains uninvestigated. Practical guidelines on how to operate hatching synchrony in the artificial incubation of A. rufa eggs will be useful for farmers to better manage hatching eggs and 1 day old chick batches. In this context, the present research was aimed at investigating the effects on egg performance, incubation length, and hatching synchrony of different sibling contact regimes during the incubation and hatching phases in red-legged partridge (A. rufa) eggs under artificial incubation.

2. Materials and Methods

2.1. Birds, Husbandry, and Sample Gathering

A total of 196 red-legged partridge hatching eggs, gathered from a farm located at Hinojosa del Duque (province of Córdoba in Southern Spain with geographic coordinates: 38°27′45.9″ N, 5°0.6′22.0″ W), were used. The breeding partridges were fed commercial feed (20% CP, 5.0% EE, 4.0% CF and 11.5% Ash) and were housed in pairs in outdoor cages measuring 40 × 90 cm, under a natural lighting regime. Egg laying started in mid-March, and sampling was carried out at the beginning of May, an intermediate date of the laying season, to avoid lower fertility of eggs laid when the laying season begins and ends, as A. rufa shows reproductive seasonality [1,16]. All eggs were gathered from breeding partridges aged 2 and 3 years to avoid the influence of breeder age on fertility and hatchability. Eggs were laid within a 3 day interval before the incubation loading. Meanwhile, they were stored in the farm under natural environmental conditions (15 to 20 °C and 60% RH), as this was the time needed to gather the required number of hatching eggs in the farm, and because a 3 day gathering interval does not jeopardize performance of Alectoris eggs [7,9,17]. The eggs were stored small end down without turning until incubation.

2.2. Experimental Design

The 196 eggs were arranged in four treatments of 49 eggs integrated by seven replications of seven hatching eggs each. The experimental batches were established according to the sibling contact regime of the eggs in different phases of the incubation process: (a) eggs without contact during the whole incubation process; (b) eggs in contact during the incubation phase (from the beginning to day 20 of incubation); (c) eggs in contact during the hatching phase (from day 20 of incubation to hatching); (d) eggs in permanent contact throughout the incubation process (from the beginning of incubation to hatching). Such sibling contact regimes were conceived to test the hypothesis that hatching synchrony is modified when the eggs are in close contact during late stages of embryonic development. The nodal point to define the experimental treatments was chosen at day 20 of incubation because (i) the literature reports that hatching synchrony is achieved when eggs remain in close contact in the last 20% of incubation (reviewed in Reyna [18]), and (ii) in A. rufa eggs, the whole incubation lasts 23–24 days [8,9,10,11,12] while transference from incubator to hatcher is usually carried out on day 20 of incubation [1,8,16].
In order to keep the eggs in contact, two types of experimental containers were built. For eggs to be kept in contact until day 20 of incubation, when the eggs needed to be turned, boxes made of rigid plastic grid were built. These boxes consisted of 4 cm in height and 10 cm in diameter cylinders provided with two lids. In each box, eggs were placed small end down and immobilized, when necessary, with small spongy plastic pieces to prevent the eggs from moving and falling when the incubator turned the trays on which the boxes were fixed.
For eggs to be kept in contact from day 20 of incubation during the hatching phase, artificial nests made of rigid plastic grids were built. These artificial nests were 15 cm in diameter and 15 in height to prevent chicks from escaping. To keep the eggs in contact, their base consisted of a 5 cm deep conic nest made of felt, which forced the eggs to remain grouped in the center of the nest. These artificial nests were loaded into the hatcher and allowed the chicks to easily hatch while the eggs remained in close contact.
Both container models received seven eggs, and each egg directly contacted at least other three eggs, thus ensuring the potential effect of sibling contact on hatching synchrony.
In order to keep the eggs without contact during the incubation phase, the eggs were put in incubator trays, consisting of individual cells measuring 3.5 × 3.5 cm, which prevented the eggs from coming into contact. To prevent the eggs from coming into contact during the hatching phase, they were placed in hatching trays divided in individual 10 cm side triangular cells delimited by rigid plastic grid walls.

2.3. Egg Incubation

The eggs from all treatments were loaded into the incubator (HS-25 model, Masalles, Ripollet, Spain) on the same date (3 May). The eggs were incubated at 55% RH and 37.8 °C during the first 20 days, being turned 45° every hour. On day 20 of incubation, the eggs were transferred to a hatcher (1-2 SA model, Maino Enrico-Adriano S.n.c., Oltrona di San Mamette, Italy) set at 80% RH and 37.5 °C, without turning them until hatching.

2.4. Data Recorded

To determine egg weight losses, eggs were weighed before loading in the incubator and at day 20 of incubation. For each individual egg, weight loss during the first 20 days of the incubation process was obtained as a percentage of egg weight before incubation. In order to determine hatchability of the incubated eggs, the numbers of unhatched eggs and hatched chicks were recorded once the incubation finished. To determine true egg fertility, non-hatched eggs were analyzed throughout breakout examination [19]. Hatchability of the fertile eggs was also determined. Fertile eggs were classified into the following categories: fertile without development (FND), positive development (PD), early embryonic mortality (EEM), late embryonic mortality (LEM), or pipped but not out of shell (P) [19,20]. Incubation length was calculated by carrying out hatching controls every 12 h, as the difference between the hatching date (when the partridge chick becomes out of the shell) and the date when the incubation started.

2.5. Statistical Analyses

Fertility, hatchability of the incubated eggs, and hatchability of the fertile eggs, according to the sibling contact regime during the incubation process, were analyzed by means of contingency tables on which Pearson’s χ2 tests were performed. Egg weights before incubation and at day 20 of incubation, as well as weight loss at day 20 of incubation, were analyzed for the fertile eggs by one-way analysis of variance. Embryonic mortality of fertile eggs was analyzed by Kruskal–Wallis tests. The descriptive statistics mean, minimum, maximum, coefficient of variation, variance, kurtosis (g2), and skewness (g1) coefficients were obtained for the length of incubation period. Differences in mean incubation length among treatments were analyzed through one-way analysis of variance. When differences among sibling eggs contact regimes for the incubation length were significant, treatment means were separated using Dunnett’s C multiple range tests at the 0.05 level of significance. Differences in the variance of the incubation length among treatments were also analyzed [21]. For all comparisons, statistical significance was accepted when p < 0.05. The analyses were conducted using SPSS 15.0 software [22].

3. Results and Discussion

Table 1 shows the number of incubated, fertile, and hatched eggs, the fertility and hatchability of the incubated eggs, and the hatchability of the fertile eggs, according to the sibling contact regime during artificial incubation of red-legged partridge eggs. The mean fertility of the eggs found in this trial (89.8%) was higher than in previous reports on A. rufa under game farming conditions (50.2% to 85.6%) [9,11,12,23,24,25]. Higher fertility found in this trial with respect to average values described in the literature might be explained by the eggs being gathered in the center of the breeding season in this trial, a period in which fertility of red-legged partridge peaks [1,16,26]. Good quality and fertility selection in the breeding flock could also have influenced the outcome [16]. No differences were found in fertility among the experimental batches (p > 0.05), which evidences that eggs were randomly distributed among treatments.
The mean hatchability of the incubated eggs (70.4%; Table 1) was within the range of values reported in the literature in red-legged-partridge under game farm conditions (31.0% to 84.1%) [7,9,11,12,24,25,27]. No differences (p > 0.05) were found in the hatchability of all incubated eggs according to the sibling contact regime of the eggs during incubation (p > 0.05). The mean hatchability of the fertile eggs (78.4%; Table 1) showed an intermediate value with respect to the interval reported for this species (57.6% to 91.6%) [7,9,11,12,23,24]. This means that incubation conditions set in this trial were suitable for the specific requirements of this species. Moreover, no significant differences were observed in hatchability of fertile eggs in function of the sibling contact regime of the eggs (p > 0.05). Previous scientific reports did not test the variation in hatchability of the red-legged partridge (A. rufa) eggs submitted to different sibling contact regimes of the eggs during artificial incubation. Our results agree with those obtained by Proudfoot [28,29] in chicken eggs, as well as those by Pani et al. [30] in Bobwhite quail (Colinus virginianus) eggs, for which no effect on hatchability was observed when eggs were kept in contact in the hatching trays from days 18 and 21 of incubation, respectively.
No difference was found among sibling eggs contact regimes during incubation for embryo development stages at embryonic mortality (Table 2). In general terms, development stages at which embryo mortality occurs coincided with the pattern and values reported for A. rufa by Gómez-de-Travecedo et al. [10] and were lower than mortalities reported at positive development, early embryonic, and late embryonic development when red-legged partridge eggs were submitted to pre-storage incubation [9]. In the present trial, however, eggs pipped but not out of shell were higher (6.3%, Table 2) than in the aforementioned studies (0.0% to 0.5%) [9,10]. In our experiment, a lower incidence of fertile eggs not developed and positive development was observed than in a trial on A. rufa eggs submitted to different turning regimes during storage before incubation [12]. To our knowledge, there has been no study investigating embryonic mortality in relation to sibling contact regime in red-legged partridge eggs during artificial incubation.
No differences were found among treatments in the initial weight of the fertile eggs before their incubation (19.2 g; p > 0.05), in the egg weight after 20 days of incubation (17.3 g; p > 0.05), and in the egg weight loss after 20 days of incubation (9.5 g; p > 0.05) (Table 3). Recently laid egg weights fit those described for A. rufa [3,9,10,11,12,25,31] and other species of the Alectoris genus [17,32,33]. The mean weight loss of the fertile eggs during the first 20 days of incubation was similar to the value found by González-Redondo [7] (9.2%) and slightly lower than the values reported by Gómez-de-Travecedo et al. [9,10] (10.2% to 11.1%) for A. rufa eggs submitted to several temperature regimes during storage and incubation, as well as the value (10.0%) reported by González-Redondo and Martínez Domínguez [12] for red-legged partridge eggs submitted to different turning regimes during storage before incubation. No reference was found in the literature describing, in this species, the potential effect of egg contact on weight loss during incubation.
The mean incubation period lasted 23.08 days (Table 4), a slightly lower value than the 23.20–23.70 day period reported for the red-legged partridge under artificial incubation [8,9,10,11,12]. It was in close agreement with the 23 day modal duration for the incubation length reported by González-Redondo et al. [8]. Incubation length was influenced by the sibling contact regime during the incubation process (p < 0.001), being shortened when the eggs were in contact during the incubation with respect to the eggs without contact (Table 4). Thus, eggs without contact during the whole incubation process had an incubation length (23.50 days) within the interval described in literature for the artificial incubation of red-legged partridge eggs. This can be explained by the typical handling of A. rufa fertile eggs during artificial incubation in most game farms, which involves incubating them without contact until the transference from the incubator machine to the hatcher usually on day 20 or 21 of incubation [34], and then placing them in the hatcher trays without paying specific attention to whether they are in close contact or not. In the present trial, eggs kept in contact during either of the two phases of incubation (1–20 days and 21 days–hatching) showed a shorter incubation length, hatching earlier (22.74 days) in the treatment in which eggs were in permanent contact throughout the entire incubation.
Furthermore, eggs kept in contact during the hatching phase hatched within a brief interval of 24 h, during a narrow window between days 22.5 and 23.5 of incubation (Table 4 and Figure 1), and with shorter dispersion than that observed for eggs from the other treatments, showing the minimum variance (0.097; p < 0.01) and the lowest coefficient of variation (1.35) for the incubation length. Studies on the artificial incubation of A. rufa eggs demonstrate that hatching can begin on day 21.5 and end on day 26 from the start of incubation, within a variable interval that might last up to 4 days as a function of the incubation conditions [8]. Accordingly, the shorter hatching dispersion interval displayed by the eggs maintained in contact during the hatching phase is an interesting finding because it could allow red-legged game farms to improve hatching synchronization, a desirable situation to simultaneously extract the whole 1 day old chick batch from the hatcher, thus minimizing extraction queues. This mechanism optimizes 1 day old chick batch management, so that chicks that hatch earlier would not have to wait for a long period of time for extraction, thus minimizing their dehydration risk.
Previous reports have shown that incubation length and hatching synchrony are affected by several factors in the artificial incubation of red-legged partridge eggs, such as the length of the storage period before incubation [9], the egg turning regime during storage before incubation [12], the time to shift from first phase of incubation to hatching phase temperature [10], or the temperature set during the hatching period [11]. However, to our knowledge, the current study is the first to demonstrate in A. rufa that the close contact of the eggs during the hatching phase of the artificial incubation shortens its duration and increases hatching synchrony. In other poultry species, it has been reported that proximity or contact among eggs during the hatching period of the artificial incubation affects the time of hatch, accelerating it in Japanese quail (Coturnix japonica) [35] and Bobwhite quail [30].
In precocial birds, the contact among eggs favors hatching synchronization, reducing its dispersion, through mechanisms that involve inter-embryonic communication. Thus, embryos that are close to hatching emit more stimuli than those that are in a less advanced state of development [36]. The sources of stimulation are various, but those produced by the embryos themselves, when they are close to hatching, are clicks, sounds of embryo body movements, and breakage of the shell, as well as vocalizations [14]. In fact, it has been studied in pheasants (Phasianus colchicus) and mallards (Anas platyrhynchos) that eggs in contact during the hatching phase synchronize hatching more intensely, which shows that contact of the eggs in the final phase is more effective [15], as occurred in the present study. In Japanese quail, it was found that almost all embryos emit clicks, with a maximum level in pipped eggs, that all eggs emit sounds of body movements, and that vocalizations occur to a lesser extent but increase as hatching approaches [14]. In the present investigation, the close physical contact between the eggs achieved thanks to the artificial nests used in both the incubation and the hatching phases contributed not only to the adequate transmission of the sounds emitted by the embryos, but also to the movements and clicks that led to the maximum possible hatching synchrony.
The evolutionary explanation of the findings in this research is related to the fact that, in precocial birds, physical contact of the eggs in the nest favors communication between embryos, favoring synchronized hatching in a short period of time [15,37]. This favors the female partridge promptly leaving the nest with the nidifugous chicks even if there are eggs left unhatched [13,38], to avoid the risk of being predated, which would be increased by a dilation of the hatching time [8,39].
As a practical implication arising from this study, we propose that the bottom of the hatcher trays be built with a slight slope toward their central part, so that the eggs can roll to stay in contact, while having enough space for hatching. To develop this proposal, the most suitable design and slope of the bottom of the hatcher trays would require a specific investigation.

4. Conclusions

Maintaining red-legged partridge eggs in close contact during the hatching phase in artificial incubation does not affect hatchability but allows hatching synchrony to be maximized, facilitating the management of 1 day old chicks.

Author Contributions

Conceptualization, P.G.-R.; methodology, P.G.-R. and F.Q.-P.; investigation, P.G.-R. and F.Q.-P.; resources, P.G.-R.; data curation, P.G.-R. and F.Q.-P.; writing—original draft preparation, P.G.-R.; writing—review and editing, P.G.-R. and F.Q.-P. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

The study was conducted in accordance with Directive 2010/63/EU of the European Parliament and of the Council of 22 September 2010 on the protection of animals used for scientific purposes (Official Journal of the European Union, L276, pp. 33–79). Ethical review and approval were waived for this study because the eggs used were handled in conditions similar to those of the commercial hatcheries, and the 1 day old chicks obtained were reintegrated into the farm from which the eggs were gathered.

Informed Consent Statement

Not applicable.

Data Availability Statement

Data are available from the corresponding author upon request.

Acknowledgments

The authors thank Casto Aparicio, owner of Granja Belagarda (Hinojosa del Duque, Cordova, Spain), for providing the hatching eggs used in the trial.

Conflicts of Interest

The authors declare no conflict of interest.

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Applsci 12 05586 g001 550
Figure 1. Hatching spread of red-legged partridge eggs according to the sibling eggs contact regime during the incubation process: (a) without contact; (b) contact during incubation phase (1–20 days); (c) contact during hatching phase (21 days–hatching); (d) permanent contact (1 day–hatching).
Figure 1. Hatching spread of red-legged partridge eggs according to the sibling eggs contact regime during the incubation process: (a) without contact; (b) contact during incubation phase (1–20 days); (c) contact during hatching phase (21 days–hatching); (d) permanent contact (1 day–hatching).
Applsci 12 05586 g001
Table
Table 1. Fertility and hatchability of red-legged partridge eggs according to the sibling eggs contact regime during the incubation process.
Table 1. Fertility and hatchability of red-legged partridge eggs according to the sibling eggs contact regime during the incubation process.
Sibling Contact RegimeNumber of EggsFertility 1
(%)		Hatchability 2
(%)		Hatchability of the Fertile Eggs 3
(%)
IncubatedFertileHatched
Without contact49433487.869.479.1
Contact during incubation phase (1–20 days)49433387.867.376.7
Contact during hatching phase (21 days–hatching)49453691.873.580.0
Permanent contact (1 day–hatching)49453591.871.477.8
Total19617613889.870.478.4
p-Value 0.8280.9210.984
1 Percentage of incubated eggs that were fertile; 2 percentage of incubated eggs that hatched; 3 percentage of fertile eggs that hatched.
Table
Table 2. Embryonic mortality of fertile red-legged partridge eggs according to the sibling eggs contact regime during the incubation process.
Table 2. Embryonic mortality of fertile red-legged partridge eggs according to the sibling eggs contact regime during the incubation process.
Sibling Contact RegimeFertile Eggs
(n)		Development Stage at Embryonic Mortality 1
(% of Fertile Eggs)
FNDPDEEMLEMPTotal
Without contact432.30.02.39.37.020.9
Contact during incubation phase (1–20 days)430.09.34.74.74.723.4
Contact during hatching phase (21 days–hatching)450.02.22.28.96.720.0
Permanent contact (1 day–hatching)450.04.46.74.46.722.2
Total1760.64.04.06.86.321.7
SEM 0.61.51.51.91.83.1
p-Value 0.3780.1490.6670.6980.9690.984
1 FND: fertile, no development; PD: positive development; EEM: early embryonic mortality; LEM: late embryonic mortality; P: pipped but not out of shell; SEM: standard error of the mean.
Table
Table 3. Initial weight, weight at 20 days of incubation, and weight loss after 20 days of incubation of red-legged partridge fertile eggs according to the sibling eggs contact regime during incubation (mean).
Table 3. Initial weight, weight at 20 days of incubation, and weight loss after 20 days of incubation of red-legged partridge fertile eggs according to the sibling eggs contact regime during incubation (mean).
Sibling Contact RegimeFertile Eggs
(n)		Initial Weight
(g)		Weight at 20 Days of Incubation
(g)		Weight Loss at 20 Days of Incubation
(%)
Without contact4319.517.510.5
Contact during incubation phase (1–20 days)4318.816.810.3
Contact during hatching phase (21 days–hatching)4519.117.57.3
Permanent contact (1 day–hatching)4519.317.310.1
Total17619.217.39.5
SEM 0.130.130.61
p-Value 0.2060.1970.187
SEM: standard error of the mean.
Table
Table 4. Effects of sibling eggs contact regime during the incubation process on incubation length and hatching synchrony of red-legged partridge eggs.
Table 4. Effects of sibling eggs contact regime during the incubation process on incubation length and hatching synchrony of red-legged partridge eggs.
Sibling Contact RegimeHatched Eggs (n)Incubation Length (Days)
MeanVarianceCV (%)Skewness (g1)Kurtosis (g2)MinMax
Without contact3423.50 a0.318 C2.40−0.8071.95822.0024.50
Contact during incubation phase (1–20 days)3323.02 b,c0.523 A3.140.406−0.59922.0024.50
Contact during hatching phase (21 days–hatching)3623.06 b0.097 D1.35−0.071−0.28122.5023.50
Permanent contact (1 day–hatching)3522.74 c0.358 B2.630.036−1.12922.0024.00
Total13823.080.3872.69−0.016−0.24622.0024.50
p-Value <0.001<0.01
a–c Means in the same column with different superscript letters are significantly different (p < 0.05); A–D variances in the same column with different superscript letters are significantly different (p < 0.01).
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González-Redondo, P.; Quesada-Pérez, F. Effects of Sibling Eggs Contact on Incubation Length and Hatching Synchrony in Red-Legged Partridge (Alectoris rufa). Appl. Sci. 2022, 12, 5586. https://doi.org/10.3390/app12115586

AMA Style

González-Redondo P, Quesada-Pérez F. Effects of Sibling Eggs Contact on Incubation Length and Hatching Synchrony in Red-Legged Partridge (Alectoris rufa). Applied Sciences. 2022; 12(11):5586. https://doi.org/10.3390/app12115586

Chicago/Turabian Style

González-Redondo, Pedro, and Fátima Quesada-Pérez. 2022. "Effects of Sibling Eggs Contact on Incubation Length and Hatching Synchrony in Red-Legged Partridge (Alectoris rufa)" Applied Sciences 12, no. 11: 5586. https://doi.org/10.3390/app12115586

APA Style

González-Redondo, P., & Quesada-Pérez, F. (2022). Effects of Sibling Eggs Contact on Incubation Length and Hatching Synchrony in Red-Legged Partridge (Alectoris rufa). Applied Sciences, 12(11), 5586. https://doi.org/10.3390/app12115586

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