1/1/23, 1:18 AM Effects of housing system and plumage colour on egg quality characteristics of indigenous naked-neck chickens

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Effects of housing system and plumage colour on egg quality

characteristics of indigenous naked-neck chickens
L Dahloum, A Yakubu1 and M Halbouche
Laboratoire de Physiologie Animale Appliquée, Université Abdelhamid Ibn Badis, 27000,
Mostaganem, Algeria.
abdulmojyak@gmail.com
1 Department of Animal Science, Faculty of Agriculture, Nasarawa State University, Keffi, Shabu-
Lafia Campus, Nasarawa State, Nigeria.

Abstract

The aim of the present study was to examine some egg characteristics of Naked neck indigenous
layers (NNL) with different plumage colours (White layers, WL; Black layers, BL and Brown
layers, BrL) kept in two different housing systems (conventional cages vs deep litter). The birds
were randomly allocated in a 2 (Housing system) x 3 (Genotype) factorial arrangement. In total,
592 fresh eggs from 150 adult NNL (ranging from 32 and 35 weeks old) were analyzed for both
internal and external egg characteristics using the General Linear Model (GLM) procedure.

There were pronounced effects of both housing system and feather colour on egg weight, egg shape
index, albumen weight, albumen height, haugh units, yolk weight and yolk index. Housing system
by plumage colour analysis of variance revealed great interactions on egg weight, yolk weight, yolk
index and on all albumen quality traits studied. The heaviest eggs [56.9±0.44 and 58.5±0.53 (g),
respectively] were laid by BrL in both housing systems. BrL and WL raised on litter system tended
to deposit markedly more albumen compared to their caged counterparts. There was also positive
effect of litter system on WL in terms of yolk production (+1.16g). The present results provide
useful information on the performance of Naked neck layers which can be exploited favourably to
boost poultry production under hot environmental conditions.

Key words: cage, egg indices, interaction, litter, major gene

Introduction

Eggs are one of the most common foods available worldwide as they play important role in human
diet as a source of protein and several essential nutrients, particularly vitamin D, vitamin B12,
selenium and choline (Ruxton et al 2010). They also provide growth factors required by the
developing embryo, as well as a number of defense factors to protect against bacterial and viral
infections (Tolik et al 2014). However, poor egg quality causes economic losses at all production
stages. Egg quality characteristics are influenced by many factors, including genetic and
environmental ones. It is evident that heat stress is one of the major challenges in poultry
production worldwide as it has a direct impact on birds’ performance. The detrimental effects of
heat stress on broilers and laying hens range from reduced growth and egg production to decreased
poultry and egg quality and safety.

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1/1/23, 1:18 AM Effects of housing system and plumage colour on egg quality characteristics of indigenous naked-neck chickens

Genetic approaches that aid in reducing or altering the extent of plumage cover have, as a result,
been adopted in many hot regions (Fathi et al 2013). Some particular major genes such as the
frizzled plumage (F ), naked neck (Na), and sex-linked slow-feathering (K) gene have been
identified to have positive effects on heat tolerance (Sharifi et al 2010). Naked neck chickens have
good heat dissipation mechanism and are highly resistant to diseases and superior to indigenous
full-feathered and exotic egg-type or exotic naked neck counterparts in terms of growth rate, egg
production, egg quality and meat yield (Islam and Nishibori 2009; Dahloum 2017). In Algeria, a
great phenotypic and phaneroptic diversity of local poultry genetic resources found in the rural
areas has been reported (Dahloum et al 2016; Dahloum 2017). However, to the best of our
knowledge, there is not much detailed information available on the egg production potentials of any
of these breeds or genotypes under either extensive or intensive rearing system. There is also dearth
of information on the egg quality characteristics of the indigenous chickens with regard to plumage
colour. Taking these facts into consideration, this study aimed to evaluate the impact of housing
system (Cage vs Litter) and feather colour on some external and internal egg characteristics of
indigenous Naked neck layers.

Materials and methods

Experimental site

The study was carried out from May-June, 2017 at a privately-owned farm in Sayada village
located in Mostaganem province (Algeria). Mostaganem is a littoral zone found at 35°55' 52'' N, 0'
05' 21'' E, at an altitude of 85 m. It has an area of 2269 km2 large, and is characterized by a
Mediterranean climate. The average yearly temperature and total precipitation amount are 17.4°C
and 375mm, respectively with highest average temperature of 25.5°C recorded in the month of
August (www.fr.climate-data.org.).

Experimental birds and their management

Data were obtained from a total of 150 adult indigenous Naked neck layers [60 White layers (WL);
50 Brown layers (BrL) and 40 Black layers (BL)] ranging from 32 and 35 weeks of age. In the
same poultry house, each layer group was maintained in conventional cages of 550cm2 (5
birds/cage) and on deep litter (10 birds/m2) without outdoor access in a 2 (Housing system) x 3
(Genotype) factorial arrangement. All birds were fed with a commercial diet (2722 Kcal kg-1 ME;
16% crude protein; 0.65% available Phosphorus; 3.5% Calcium; 0.71% Lysine and 0.29%
Methionine). Water and feed were provided ad libitum twice daily (at 7h30 and 17h00). The light
schedule was 15L:9D (7h00 to 22h00). Housing temperature and relative humidity were 23±2°C
and 65-75%, respectively. The birds used in this experiment were reared in accordance with the
recommendations of the "Guide for the Care and Use of Laboratory Animals, French version" and
those of ITELV (Institut Technique des élevages) de Baba Ali (Algeria) for layer hens.

Egg quality analysis

A total of 592 fresh eggs (301 from cages and 291 from litter) were analyzed for internal and
external quality within 24 hours after laying. The eggs showing any macroscopic abnormalities
(broken egg, dirty egg, misshaped egg, bloody egg, double-yolk egg) were removed from the
analysis. The external egg traits recorded were: whole egg weight (WEW, g), egg width (EWd,
mm) and egg lenght (EL, mm): These values were used for egg shape index calculation [ESI=

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(EWd/EL x 100)] and eggshell weight (ESW, g). As regards the internal egg quality, the parameters
investigated were: albumen weight (AW, g), albumen height (AH, g), albumen pH (ApH), Haught
units (HU = [100 × log (AH + 7.7 – 1.7 × EW0.37)], yolk weight (YW, g), yolk pH (YpH), yolk
height (YH, mm) and yolk diameter ( YD, mm) for yolk index calculation (YI = YH/ YD) and yolk
by albumen ratio (Y/A). WEW was determined to the nearest 0.01g using electronic scale. EWd,
EL and YD were determined with a digital caliper (Mitutoyo Corp., Aurora, IL, USA) while AH
and YH were determined using a tripod micrometer with a precision of 0.01mm.

Statistical analysis

The main effects of housing system and plumage colour and the interaction between them on
internal and external egg characteristics were determined using the General Linear Model (GLM)
procedure in SPSS software (IBM, version 21.0). Where the interaction was significant, Duncan's
Multiple Range Test (DMRT) was performed to compare means. The model used was:

Yijk = μ + Hi + Gj + (HG)ijk + eijk

where,

Yijk = observation per individual

μ = population mean

Hi = fixed ith housing system effect (i = cage, litter)

Gj = fixed jth genotype effect (j = white, brown, black layers)

(HG)ijk = interaction effect of housing system and genotype

eijk = error term

Results

External egg quality

Egg weight, egg shape and eggshell weight

There was an interaction between housing system and plumage colour for whole egg weight (Table
1). Brown-feathered hens produced the heaviest eggs in both housing system while the lightest eggs
were produced by White hens in cages. For birds on litter, however, Black hens and White hens
seemed to have the same ranking in terms of egg weight. In addition, significant egg
conformational change was observed depending on both fixed factors. Eggs from caged hens were
rounder compared to those produced in litter system which were more elongated. Black-feathered
layers produced the biggest eggs compared to those from the white layers (+1.62), while eggs from
Brown feathered layers seemed to be of intermediate size. However, no significant housing system
by plumage colour interaction occurred for this parameter. Regarding eggshell weight (ESW), there
was pronouced effect of genotype on this trait. Brown-feathered layer produced more shell amount
(+1.46g) compared to its counterparts. However, there were no effects of housing system and
housing system by plumage colour interaction on ESW.
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1/1/23, 1:18 AM Effects of housing system and plumage colour on egg quality characteristics of indigenous naked-neck chickens
Table 1. Effects of housing system and plumage colour on whole egg weight, shape index and eggshell weight
of indigenous naked neck (Least square means±standard error)
Housing system Genotype1 WEW (g) ESI ESW (g)
54.0±0.27 75.4±0.27 8.29±0.09
WL 50.8±0.47d 74.6±0.46b 7.71±0.16b
Cage b ab
BrL 56.9±0.44 75.2±0.43 9.21±0.15a
BL 54.3±0.51c 76.3±0.51a 7.98±0.18b
55.7±0.28 74.2±0.28 8.21±0.10
WL 54.3±0.44c 73.8±0.42b 7.46±0.16b
Litter
BrL 58.4±0.53a 73.3±0.50b 9.25±0.20a
BL 54.4±0.49c 75.4±0.46a 7.92±0.18b
Source of variation ANOVA significance level [p (F)]
Housing system, H ≤0.001 0.002 0.51
Genotype, G ≤0.001 ≤0.001 ≤0.001
HxG ≤0.001 0.46 0.65
abcd Within columns, Least squares means with different superscripts differ at p ≤ 0.05 ;
1 WL (White layers, n= 217); BrL (Brown layers, n= 195); BL (Black layers, n= 180); WEW = whole egg
weight; ESI = egg shape index; ESW = eggshell weight.

Internal egg quality

Albumen characteristics

Data describing the effects of housing system and plumage colour on some albumen parameters are
presented in Table 2. Both housing system and plumage colour affected all albumen quality
characteristics, with the exception of albumen pH. Important interactions between both factors were
also found for all albumen quality traits. Brown layers and white layers raised on litter system
tended to deposit more albumen compared to their caged counterparts while the albumen weight
from black layers remained constant regardless of housing system.The highest values for albumen
height and HU score were found in eggs from white layers kept on litter system. In cage rearing,
white and brown layers were similar in terms of Albumen height and HU score. The lowest values
for both traits were found in black layers. With respect to albumen pH, the mean values ranged
between 8.55 and 8.72. In white layers, this parameter tended to decrease notably in litter system
while the opposite was observed for black layers.

Table 2. Effects of plumage colour and housing on albumen weight, albumen height, haught units and albumen
pH of indigenous naked neck (Least square means±standard error)
Housing system Genotype 1 AW (g) AH (mm) HU ApH
Cage 28.2±0.22 7.27±0.01 85.4±0.55 8.62±0.02
WL 26.2±0.38c 8.01±0.01b 91.4±0.95ab 8.72±0.04a
BrL 29.4±0.35b 7.97±0.01b 89.3±0.89b 8.56±0.03b
BL 28.9±0.41b 5.82±0.02d 75.6±1.03d 8.59±0.04b
Litter 29.3±0.22 6.96±0.01 83.3±0.56 8.62±0.02
WL 28.4±0.35b 8.54±0.01a 93.3±0.88a 8.58±0.03b
BrL 31.1±0.42a 5.65±0.02d 73.4±1.06d 8.56±0.04b
BL 28.4±0.39b 6.68±0.02c 83.1±0.98c 8.72±0.04a
Source of variation ANOVA significance level [p (F)]
Housing, H ≤0.001 ≤0.01 0.006 0.98
Plumage colour, C ≤0.001 ≤0.001 ≤0.001 ≤0.01
HxC ≤0.001 ≤0.001 ≤0.001 ≤0.001
abcd Within columns. Least squares means with different superscripts differ atp≤0.05;
1 WL (White layers, n= 217); BrL (Brown layers, n= 195); BL (Black layers, n=180); AW = albumen weight;
AH = albumen height; ApH = albumen pH; HU = Haught units.

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Yolk characteristics and Y/A ratio

The effects of housing system and plumage colour on some yolk characteristics as well as Yolk by
Albumen ratio are presented in Table 3. The mean yolk weight varied between 16. 9g and 18.4g.
This trait was highly influenced by both housing system and plumage colour as well as their
interaction, indicating positive effect of litter system on yolk production especially in white layers
(+1.61g) in comparison with black layers. In contrast, in brown layers, the yolk weight seemed to
decrease in litter system. Even though the yolk index was influenced by housing system and
plumage colour as well, no interaction was observed. Additionally, housing system and plumage
colour had no effect on yolk pH and Y/A ratio. However, there was significant impact of interaction
on Y/A ratio.

Table 3. Effects of plumage colour and housing on yolk weight, yolk index, yolk pH and yolk by albumen ratio
of indigenous naked neck (Least square means±Standard error)
Housing system Genotype1 YW (g) YI YpH Y/A
Cage 17.6±0.17 0.47±0.01 6.73±0.13 0.47±0.01
WL 16. 9±0.29 b 0.47±0.01 ab 6.92±0.22 0.66±0.02
BrL 18.4±0.27 a 0.49±0.01 a 6.62±0.21 0.67±0.02
BL 17.5±0.31 ab 0.44±0.01 b 6.65±0.24 0.61±0.02
Litter 18.2±0.17 0.49±0.01 6.77±0.13 0.63±0.01
WL 18.5±0.27 a 0.50±0.01 a 6.56±0.20 0.66±0.02
BrL 18.1±0.33 a 0.49±0.01 ab 7.14±0.25 0.59±0.02
BL 18.0±0.30 a 0.47±0.01 b 6.63±0.23 0.64±0.02
Source of variation ANOVA significance level [p (F)]
Housing, H 0.009 0.007 0.79 0.38
Plumage colour, C ≤0.001 ≤0.001 0.59 0.17
HxC 0.007 0.18 0.13 0.03
ab Within columns. Least squares means with different superscripts differ atp≤ 0.05;
1 WL (White layers, n= 217); BrL (Brown layers, n= 195); BL (Black layers, n= 180; YW = yolk weight; YI =
Yolk index; YpH= yolk pH; Y/A = yolk by albumen ratio.

Discussion

The mean egg weight obtained from naked neck chickens in this study varied from 50.8±0.47g to
58.4 ± 0.53g, with an average egg weight of 54.3 ± 0.21g and coefficient of variation of 10%.
These values for egg weights are similar to those reported by earlier workers (Dahloum 2017).
However, Rajkumar et al (2015) reported higher egg weight in broiler-based naked neck chicken at
different ages which ranged from 56.3 to 60g at 32 and 40 weeks, respectively. Dahloum et al
(2017) also reported highest mean egg weight of 58.6g in Naked neck-frizzled chickens kept in
litter system at 35 weeks of age. Contrastingly, Yakubu et al (2008) reported lower values of 43.0g
and 40.8g in free range homozygous naked neck and full-feathered chickens, while Wambui et al
(2018) and Gikunju et al (2018) reported values of 46.5 and 46.3g, respectively.

Egg weight has significant effects on total hatchability, hatchability of fertile eggs, egg weight loss,
embryonic death, and egg breakout analysis in broiler breeder chickens (Alsobayel et al 2013).
Generally, larger eggs produce larger chicks and a good-quality egg improves the probability of
optimal hatchability and chick quality (Yoho et al 2008). The differences observed in egg weight in
this current study under housing system are in concordance with the findings of other investigators
(Jones et al 2014). Conversely, Ismoyowati et al (2010) reported that egg weight was not different
among Kedu chickens with different feather colours.

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The mean egg shape index of 74.7±4.73 with a coefficient of variation of 6% obtained in this study
falls within the normal range of 72-76 and confirms our previous studies (Dahloum 2017).
Comparable values for shape index were also reported by Yakubu et al (2008) for Nigerian Naked
neck chickens but higher than that obtained by the same authors for normal feathered chickens.
Generally, it is well known that indigenous chickens laid smallest sized eggs in comparison with
commercial strains. According to Rajavindra et al (2015), the higher shape index value indicates
better uniformity in the eggs which is essential for good hatchability and healthy chick production.
In this study, important effects of housing system and plumage colour on egg shape index were
found. With respect to housing system, our results are in agreement with the reports of earlier
authors (Van Den Brand et al 2004), but inconsistent with those of Svobodova et al (2014).

Shell breakage has always been a financial drain on the poultry industry (Solomon 2010). Thus,
selecting the hen genotype which provides better eggshell quality characteristics is a very important
issue to be considered (Ketta and Tumova 2018). In the present study, the mean eggshell weight
was 8.23±1.78g with a coefficient of variation of 22%. Similar mean eggshell weights were
recorded for commercial hybrids Hy-Line Brown in extensive rearing system (Batkowska and
Brodacki 2017). Current estimate on shell weight was higher than the 5.02g found in heterozygous
Naked neck birds (Rajkumar et al 2009). In this study, eggshell weight differed according to
plumage colour. Nevertheless, Ketta and Tumova (2016) reported that eggshell thickness is
probably a more reliable indicator of eggshell quality than eggshell weight. In the present study, the
effect of housing system on eggshell weight was not found which corresponds to the findings of
Svobodova et al (2014). On the other hand, the impact of housing system on the shell
characteristics was clearly visible and statistically significant in the study of Batkowska and
Brodacki (2017). Overall, research findings have not provided a clear indication of which
production system maintains eggs with the best shell quality.

There was a significant impact of plumage colour on all albumen traits studied. However, the pH
albumen did not differ between housing systems which is inconsistent with the submission of Van
Den Brand et al (2004). The overall mean values of 28.6g obtained for albumen weight in this study
was found to be about 2g and 6g smaller than those recorded by Batkowska and Brodacki (2017)
and Rajkumar et al (2009), respectively, but was about 7g higher than those recorded in Nigerian
locally adapted chickens (Adedeji et al 2015). The albumen heights as well as HU score in the
present study were greater than those reported by Lewko and Gornowicz (2011) (7.3mm vs
4.52mm and 85.33 vs 63.71, respectively) but lower in terms of albumen pH values (8.62 vs 9.2).
However, similar results for albumen height, Haugh units and albumen pH were found in other
studies (Lewko and Gornowicz 2011). Garba et al (2010) noted that HU of high quality eggs falls
within the range of 57.9-61.8. However, the albumen pH is a more reliable measure of egg
freshness than albumen height since it was not affected by the age or strain of hen (Silversides and
Scott 2001). Furthermore, Albumen pH is useful for describing changes in quality of albumen over
time during storage (Chatterjee et al 2007).

The overall mean of 17.9g obtained in the present study for yolk weight was comparable with those
reported in previous studies (Lewko and Gornowocz 2011; Chatterjee et al 2007) but greater than
those reported in other studies (Batkowska and Brodacki 2017; Yilmaz-Dikmen et al 2017).
However, slightly highest values of 18.5g and18.6g were found by Mahrous and El-Dlebshany
(2011) in Naked neck and Naked neck-Frizzled chickens, respectively. The present study revealed
significant effect of housing system on yolk weight with highest values recorded for birds kept on
litter. These results are in agreement with those reported by Pistekova et al (2006). In another study
by Yilmaz-Dikmen et al (2017), the yolk weight was higher in the free-range system than in
conventional-cage and enriched-cage systems. In contrast, Lewko and Gornowocz (2011) reported
that eggs laid by caged birds were characterized by yolks with the highest values for weight and pH
compared to eggs from litter and free-range system. The average yolk index of 0.48 found in the
present study is higher than those reported by Tabidi et al (2011) and Sreenivas et al (2013). As for
yolk weight, the present study revealed remarkable effect of both housing system and plumage

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colour on yolk index. The housing system impact on yolk index was reported by several
investigators (Svobodová et al 2014; Ledvinka et al 2012). Contrastingly, Ahammed and Ohh
(2013) and Jones et al (2014) found no difference in yolk index between housing treatments. In the
present study, the overall mean value of Yolk pH was 6.74 which is slightly higher than 6.42 found
in Tswana naked neck chickens (Kgwatalala et al 2016). Regarding the Y/A ratio, the mean value of
0.64 obtained in the present study is lower than those reported by Marcos et al (2017) ranging from
0.68 to 0.75 in three Ethiopian indigenous chicken ecotypes. However, they are higher than the
0.39 and 0.52 reported in eggs from commercial breeds’ and Korean native chickens, respectively
(Suk and Park 2001). It is evident that the volume of egg yolk used by food companies in their
formulations is constantly increasing (Miranda et al 2015) due to the excellent functional properties
of its lipoproteins such as flavor, aroma, colour, viscosity, emulsifying, and foaming (Lai et al
2010). However, eggs with heavier yolk and larger Yolk: albumen ratio are likely to contain more
cholesterol (Suk and Park 2001). Wang et al (2009) reported that the outdoor layers produce eggs
with lower cholesterol content than caged layers (8.64 vs 0.32 mg/g). Furthermore, Mahrous and
El-Dlebshany (2011) stated that the presence of Na gene may lead to the development of low-
cholesterol chicken eggs as demanded by health-conscious consumers. In the present study, housing
system and plumage colour effects were not enough to detect differences in both yolk pH and Y/A
ratio. These findings are partially consistent with other studies. Thus, Chodová et al (2013) reported
no effect of housing system on yolk pH whilst Van Den Brand et al(2004) observed no effect of HS
on Y/A ratio. Overall, the reasons for diverse opinions between researchers regarding some external
egg characteristics are certainly multifactorial such as the used breeds, layers' age, and other
experimental conditions (nutrition, temperature and lighting).

Conclusions

The results of the present study clearly indicated significant housing system by feather colour
interactions on some egg quality traits, showing a remarkable change in the ranking of
genotypes studied.

The potential interest of further research is stressed to understand the basis of feather colour
on egg quality traits of Naked neck layers reared in cages and to better exploit positive
interaction effects in the selection of high-performance genotypes.

Acknowledgment

This experiment was supported by Abdelhamid Ibn Badis University of Mostaganem, Algeria.

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Received 9 November 2018; Accepted 14 November 2018; Published 2 December 2018

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