Blood profile, egg laying performance, egg external and internal qualities of guinea fowls raised in three different housing systems

DOI: https://doi.org/10.21203/rs.3.rs-2472428/v1

Abstract

This study evaluated the impact of different housing systems on the blood profile, egg production, egg external and internal characteristics of guinea fowl. Two hundred and thirty-four 24 week- old Helmeted guinea fowl pullets were used of which 78 were assigned to each housing system; cage, deep litter and deep litter with access to run. Each housing system had six replicate groups of 13 birds each. Data were collected on egg laying performance and characteristics. Blood sampling and analyses were carried out at the 16th week of the experiment. All data collected were subjected to analysis of variance in a Completely Randomized Experimental Layout. The result indicated that the average final weight, weight gain, feed intake, feed per dozen egg and total egg were significantly (p < 0.05) influenced across the housing systems. Interestingly, egg weight, shell thickness and yolk colour were observed to be more in deep litter with free run housing system. Hens in the deep litter with free run had the highest (p < 0.05) total serum protein (4.27g/dl), albumin (2.57g/dl) and glucose (208.33mg/dl) values compared to other systems. White blood cell count was significantly (p < 0.05) higher in deep litter and deep litter with free run than cage system. It was concluded that hens in deep litter housing with free run had better growth and egg quality traits, suggesting that this housing type was more beneficial to guinea fowl under tropical conditions than cage and deep litter housing types.

Introduction

An appropriate housing type has been an issue of concern in the domestication and commercial production of guinea fowl eggs and meat in the tropics, of which the most important species is Numidia meleagris Production, management and housing systems, nutrition, purpose of egg and meat production, control of mortality of young guinea fowl and level of breeding activity are the main factors that affect the productive performance of the Guinea fowl (Portillo-Salgado et al. 2022). However, factors such as nutrition, genotype, and pre-incubation and incubation conditions have permanent long term influence on productive performance of Guinea fowl (Portillo-Salgado et al., 2022). The evaluation (Oke et al., 2015) of the effects of housing systems (open air, deep-bed, and battery cage) showed that the body weight of the birds kept in the open air was similar to that of the deep-bed reared hens, but was significantly higher than those of birds reared in battery cages. The low performance shown by Guinea fowl kept in battery cages was linked to cage induced stress levels, which significantly influenced rectal temperature, breathing rate, and blood glucose levels of birds (Oke et al., 2015). It was also observed that conventional battery cage systems are not suitable for housing guinea fowl. However, Sánchez-Casanova et al., (2020) observed positive effect of open-air housing and production systems on the well-being of chickens; however, mortality rate was compromised to some extent. There is a need to further establish the appropriate housing system fit for the optimal performance of pearl helmet guinea fowl in the tropical environments. This study is aimed to assess laying production, eggs’ external and internal characteristics, and blood profile of guinea fowl reared in varying housing systems.

Materials And Methods

Experimental birds, design and management

A total of 234 twenty-four-week-old, Pearl helmeted guinea fowl pullets were used for this research and were randomly assigned to three experimental housing systems namely; cage, deep litter, and deep litter with free run. Each housing system had 78 pullets arranged in 6 replications of 13 birds each. The cages had 1m2 of floor area per bird. The deep litter floor also had a stock density of 1 m2 per bird. The deep litter with run had 2.5 m2 per bird outdoor run area (in addition to deep litter floor of 1 m2 per bird) covered with grass and small bushes, which enabled pullets to supplement their diets using vegetation and small creatures living outdoors. The birds were subjected to lighting programme of 16 hours of light: 8 hours of darkness (12L: 8D) because the houses were open sided to provide sufficient light intensity to support egg production according to Kyere et al. (2017). The deep litter pen floor was bedded with wood shavings. Housing systems were equipped with wooden nest boxes for egg laying and were naturally ventilated and equipped with feeders and drinkers. The cage housing was a wire net supported by metal bars. Each housing type was equipped with galvanized feeder and linear drinker. Experimental treatments (housing systems) and data collected were arranged in a Completely Randomized Experimental Design. Standard feed and water were provided ad libitum throughout the experimental period of 16 weeks. The composition of the diet is given in Table 1.

Data Collection And Parameters Considered

Data were collected on bodyweight gain, feed consumption and survivability. For egg quality analyses, six eggs per replicate pen were sampled weekly. External and internal egg quality assessments were done within 24 hours of egg lay. The eggs were randomly collected weekly from each replicate pen and weekly data pooled to obtain mean values for stastical analysis.

Egg Traits Assessed

Egg, albumen and the yolk weights were carefully measured and the dried empty shell was weighed in grams; eggshell thickness was also measured after the egg was broken. The shell thickness (mm) without inner and outer shell membranes was measured. Egg shape index was calculated by dividing the egg width by the egg length and the ratio multiplied by 100. Albumen height measured with an accuracy of 0.01mm. Haugh Unit was also calculated as :

HU = 100 log (H + 7.5–1.7W0.37)

Where HU = Haugh unit ; H = Albumen height in mm; W = egg weight (g)

Number of eggs/week was counted as the total number of eggs laid by individual hen in each group per week.

Blood Sample Collection For Haematological And Serum Parameters

At the sixteenth week of feeding trial, four hens were randomly selected from each replicate for blood test. Blood samples were collected via left wings into vials containing Ethylene Diamine Tetra Acetate (EDTA) for haematological parameters according to (Van et al., 2001). Another 2.5ml of blood was collected into a sample bottle (without anticoagulant) for serum determination and was centrifuged at 3000U/min for ten minutes to separate the cell from the plasma and fractionated blood separated serum was evaluated using an automated blood chemistry analyser Hitachi, Japan with DIAS (Diagnostics Systems GmbH, Germany) reagents.

Table 1

Composition (g/kg) of basal experimental diet for guinea hens

Ingredient

Composition

Maize

440.00

Soybean meal

80.00

Fish meal (72% CP)

20.00

Groundnut cake

75.00

Wheat offal

265.50

Bone meal

40.00

Oyster shell

71.00

Lysine

1.50

Methionine

2.00

*Vit./Mineral Premix

2.50

Salt (NaCl)

2.50

Total

1000.00

Chemical Composition

 

Metabolizable Energy (MJ/g/kg)

10.61

Crude Protein (g/kg)

16.76

Crude Fibre (g/kg)

4.27

Ether Extract (g/kg)

3.85

Calcium (g/kg)

3.77

Available Phosphorus (g/kg)

0.79

*1 Kg contains: Vit A: 10,000,000 IU; Vit D3: 2,500,000 IU; Vit E:20,000mg; Vit K3: 3,000mg; Vit B 3 :3,000mg; Vit B2: 7,000mg; Vit B6: 5000mg; Vit B12: 25mg; Biotin: 20mg: Niacin: 15,000mg; Panthotenic Acid: 10,000mg; Folic Acid:8500mg; Manganese:80,000mg; Zinc:60,000mg; Iron:40,000mg; Copper:8,000mg; Iodine: 1,000mg; Selenium (1%): 150mg; Cobalt:250mg; Choline:200,000mg and Antioxidant: 100,000mg.

Statistical model and data analysis

The statistical model adopted was : Yij = µ + Bi +Eij

Where, Yij is Individual Observation, µ is the population mean, Bi is the effect of housing systems and Eijk is the residual error. Data analysis was done using Analysis of Variance in a Completely Randomized Experimental Design. Significant (P < 0.05) differences among means were separated using Duncan’s Multiple Range Test as contained in Statistical Analyst System (SAS, 2003) package.

Results

The results of the laying performance of guinea fowl reared in the three housing system as presented in Table 2 showed significant (p < 0.05) effect of housing system on weight gain, feed intake, feed per kg egg, body weight at 1st egg lay and hen day egg production. Birds in deep litter with free run had highest total egg produced per group per week (209.00 ± 6.03) and hen-day egg production of 15.58 ± 0.05 compared to cage’s 81.67 ± 3.17 and 6.64 ± 0.10 and those of deep litter, 197.00 ± 4.51 and 14.67 ± 0.78 respectively. Statistical similarities were observed in values obtained for guinea fowls raised in deep litter and deep litter with free run in terms of weight gain, feed intake, feed per kg egg, total number of eggs, body weight at 1st egg lay, daily egg laid and hen day egg production. The Table 3 showed significant effect of housing system on egg weight, shell thickness and shape index. Guinea fowl reared in cage house had a significantly highest shell thickness. Yolk colour was most intense in eggs from guinea fowl kept in deep litter with free run housing (Table 3).

There was significant (p < 0.05) difference in white blood cell and lymphocytes (Table 4). The white blood cell counts were significantly (p < 0.05) higher in deep litter and deep litter with free run housing systems than cage. The white blood cell counts were significantly (p < 0.05) higher in deep litter and deep litter with free run housing systems than cage. The values of some serum chemistry indices of guinea fowl are also presented in Table 5. The values of albumin showed that guinea fowl on deep litter and deep litter with run were significantly higher than caged fowls, the same trend was observed in glucose values, the values obtained were within the stipulated range for laying birds.

Table 2

Effect of housing system on laying performance of guinea fowl hens (24 to 40 weeks of age).

Parameters

Housing systems

 

Deep litter

Cage

Deep litter with run

Weight gain(g/bird)

395.33 ± 33.75ab

415.33 ± 14.01a

375.00 ± 2.33b

Feed intake (g/bird/day)

75.59 ± 0.24a

75.09 ± 0.12b

75.32 ± 0.13ab

Feed/kg egg laid

6.71 ± 0.14a

6.12 ± 0.62b

6.31 ± 0.17a

Hen-housed per replicate (no)

13.00

13.00

13.00

Age at 1st lay (wk)

27.67 ± 0.33

25.33 ± 1.67

27.33 ± 0.33

Body wt. at 1st egg lay(g)

1387.08 ± 0,07b

1423.04 ± 0.15a

1413.20 ± 0.07ab

Hen-day egg production(%)

14.67 ± 0.78a

6.64 ± 0.10b

15.58 ± 0.50a

Total egg production per week (no)

197.00 ± 4.51a

81.67 ± 3.17b

209.00 ± 6.03a

Survivability (%)

92.31 ± 10.33

84.62 ± 10.58

92.31 ± 10.33

a,b Means on the same row with different superscipts are significantly different (p < 0.05)

Table 3

Egg quality traits of guinea fowl hens raised in different housing systems

Parameters

Housing systems

 

Deep litters

Cage

Deep litters with run

External egg quality

Egg weight (g)

35.66 ± 0.13ab

35.11 ± 0.82b

37.02 ± 0.17a

Egg length (mm)

42.69 ± 0.22a

37.23 ± 2.89b

41.94 ± 0.17ab

Egg breadth (mm)

33.95 ± 0.23

28.53 ± 3.04

34.11 ± 0.30

Egg shape index (%)

78.63 ± 0.27ab

73.91 ± 2.89b

80.24 ± 0.56a

Shell weight (g)

5.66 ± 0.23

5.51 ± 0.04

5.58 ± 0.08

Shell thickness (mm)

0.58 ± 0.01b

0.64 ± 0.03a

0.53 ± 0.01b

Shell weight (%)

15.87 ± 0.24

15.69 ± 0.44

15.07 ± 0.12

Internal egg quality

Albumen height (mm)

6.15 ± 0.06

6.48 ± 0.29

6.59 ± 0.11

Albumen weight (g)

18.63 ± 0.35

18.20 ± 0.25

18.24 ± 0.08

Albumen index %

50.33 ± 0.87

50.99 ± 0.49

51.13 ± 0.13

Albumen pH

8.76 ± 0.03

8.49 ± 0.13

8.50 ± 0.01

Yolk weight (g)

10.60 ± 0.12

10.43 ± 0.17

10.41 ± 0.09

Yolk weight (%)

28.68 ± 0.18

29.33 ± 0.35

29.24 ± 0.24

Yolk height (mm)

13.17 ± 0.11

13.78 ± 0.37

13.25 ± 0.15

Yolk colour

1.54 ± 0.07b

1.74 ± 0.13b

5.51 ± 0.07a

Haugh unit

87.93 ± 0.64

87.55 ± 1.40

87.98 ± 0.37

a,b = Means on the same row with different superscipts are significantly different (p < 0.05)

Table 4

Effect of housing system on haematological indices of guinea fowl hens

Parameters

Housing Systems

 

Deep litter

Cage

Deep litter with run

Packed cell volume (%)

37.00 ± 4.73

40.67 ± 5.78

37.00 ± 1.53

Haemoglobin (g/dl)

12.30 ± 1.27

13.10 ± 2.06

12.28 ± 0.66

Red blood cells (x1012/L)

2.73 ± 0.35

3.0 ± 0.40

2.73 ± 0.12

White blood cells (x109/L)

21.20 ± 1.73a

13.70 ± 1.01b

20.20 ± 1.10a

Lymphocytes (%)

67.00 ± 1.53b

74.00 ± 1.15a

66.00 ± 2.08b

Eosinophils (%)

0.67 ± 0.67

0.33 ± 0.33

0.33 ± 0.33

Basophils (%)

0.00 ± 0.00

0.33 ± 0.33

0.00 ± 0.00

Monocytes (%)

0.33 ± 0.33

0.67 ± 0.33

0.00 ± 0.00

Mean cell volume (fl)

135.33 ± 0.33

135.33 ± 1.45

135.67 ± 0.33

Mean cell haemoglobin (pg)

47.67 ± 2.91

43.67 ± 1.20

44.67 ± 1.20

MCHC (g/d)

33.47 ± 0.79

32.07 ± 0.52

33.13 ± 0.78

a, b Means on the same row with different superscipts are significantly different (p < 0.05)

Table 5

Effect of housing system on serum chemistry of guinea fowl hens

Parameters

Housing Systems

 

Deep litter

Cage

Deep litter with run

Total protein (g/dl)

3.93 ± 0.30

3.60 ± 0.12

4.27 ± 0.18

Albumin (g/dl)

2.50 ± 0.06a

1.67 ± 0.09b

2.57 ± 0.12a

Globulin (g/dl)

Uric acid (mg/dl)

1.43 ± 0.28

4.23 ± 0.45

1.93 ± 0.09

4.57 ± 0.32

1.70 ± 0.06

4.23 ± 0.56

Glucose (mg/dl)

205.00 ± 6.81a

182.33 ± 5.55b

208.33 ± 4.41a

Cholesterol (mg/dl)

102.67 ± 2.91

104.33 ± 6.69

99.67 ± 3.18

a, b Means on the same row with different superscipts are significantly different (p < 0.05)

Discussion

The higher (p > 0.05) weight gain obtained in the cage guinea fowl was a spetacle that cannot be explained however the value not statistically diffrent from deep litter with run values. However, litter floor housing may provide the bird with non-digestible structural particles that, upon ingestion, have remarkable effects on digestibility, feed efficiency, growth and meat yield (Santos et al., 2012). Traditionally, DF has been considered as an antinutritional factor and a diluent in poultry diets. Several reports show a strong negative correlation between the fiber content of the diet and the digestibility of protein and fats. Those reports also indicate that increased fibrous components of the diet reduce growth performance and impair nutrient retention in turkeys and broiler chickens. These DF cannot be hydrolyzed by the digestive enzymes in the small intestine but can be fermented to a certain degree by the microflora in the GIT. It was reported by Santos et al. (2012) that broilers reared in a conventional litter-based house had superior growth performance results when compared to those raised in a non-litter cage-based housing system. Birds in the three housing systems investigated were fed the same commercial diet and the fowls reared in cage consumed less (p < 0.005) feed and gained more body weight with less kilogramme egg laid compared to fowls reared in deep litter and deep litter with free run house. This affirms the fact that housing system is an external factor that influences growth and production. Sekeroglu et al. (2009) concluded that free-range housing system significantly decreased the total feed intake and body weight of broilers. Current findings about feed intake comply with the results of previous studies indicating higher feed consumption for the deep litter or floor system than for the cage system. Layers kept in litter system consumed more feed than the layers housed in cage systems. Feed consumption her was higher for the floor system (deep litter and deep litter with free run) than for the cage system. This was in the line with the findings of Preisinger (2000) who reported that birds in floor system ate more feed than those in cage systems.

Heavier (p < 0.05) eggs obtained in the deep litter with free run housing system can be associated with access to open-free run, where fowls could supplement their diet from vegetation and invertebrates. According to Sokołowicz et al. (2018) free runs inhabited by soil invertebrates, including earthworms are rich in nutrients which can be an additional source of protein for fowls. Also green forage consumed in the run can supply additional nutrients to fowl rear in the deep litter with free run housing system (Sokołowicz et al., 2018). There are diverse reports on effects of housing on egg weight and egg production. The values of egg weight (37.02 ± 0.17, 35.11 ± 0.82, 35.66 ± 0.13g) reported for guinea fowls in this study were lower than the egg weight of the grey guinea fowl reported in most studies particularly for the indigenous pearl and black guinea fowls reported by Obike et al. (2011). The reason for this disparity in reports could be due to environmental and genetic variations that affect egg weight. Egg weight values of the three-housing system were in the range reported by Oke et al. (2004) who obtained a mean egg weight of 37.67g and 36.24g in Pearl strain of guinea fowl. Cage housing system physically shortenned age at 1st lay but with concomittant increase in body weight at 1st egg lay relative to other housing treatments used in this study. Also guinea fowl raised in deep litter with free run housing system had a better egg laying performance in terms of total number of egg laid and hen day egg production when compared with batttery cage and deep litter housing systems respectively. Hen day egg production was 120% better in both deep litter and deep litter with run housing compared to cage reared fowls. The hen day egg production of guinea fowl in deep litter with free run was 6% a lot better than those reared in deep litter house.

In this study, eggs from deep litter with or without free run were characterized by a higher shape index than eggs from cage system. Dalle Zotte et al. (2013) observed no siginficant effect of rearing system on egg shape index compared to what was obtained in this study. According to Sarica and Erensayin (2009) classification, eggs shape index in cage (73.91%), deep litter (78.63%) and deep litter with free run (80.24%) best fit round shape class contrary to fact that guinea fowl eggs have small end that are more pointed than those of chicken egg(Obike et al., 2011). The typical elliptic egg shape has been considered as a beneficial trait because it reduces breaking losses during transport, as suggested by Nedomová et al. (2009) that egg shape index influences eggshell strength. The higher mean shell thickness values obtained in this study may be due to fatigue or stress associated with cage housing wherein birds are unable to exercise or exhibit their natural behaviour. The shell formation is by activities of cells of the oviduct and uterus and under stress conditions, the secretions of these cells may become acidic which may damage or destroy these cells and can induce the formation of eggshells that have high or excess deposit of calcium. The observation of more golden yolk in eggs from the guinea fowls reared in the deep litter with free run compared to the eggs from other housing systems corroborated the claims of Sokołowicz et al. (2018). This was so because the fowls on free run had access to green plants which are abundant in the pigment xanthophyl. The Haugh unit value obtained in this study is higher than the 70% benchmark noted for quality eggs.

A significant (p < 0.05) difference was noticed in the white blood cell count and lymphocytes. The white blood cell count was significantly higher in the deep litter with run and deep litter than those in cage. These values are signals that the birds were in a perpetual state of well-being for the interval of the research. The WBCs are responsible for defending the body against infections Adedibu (2014). Insignificant difference noted in blood serum biochemistry indices across housing systems seems to suggest that birds are healthy and underwent varying housing systems without any stress.Based on the results of this study, laying guinea fowl hens show a better egg production potential when riased in the deep litter with free run housing system and raising them in either deep litter or deep litter with free run housing systems will give them optimum health compare to rearing them in cage housing.

Declarations

Data availability

The data that support the findings of this study are available from the corresponding author upon request. 

Code availabilty

Not applicable

Funding (Not applicable)

No funds, grants, or other support were received.

Conflict of Interest

The authors declared that they have no conflict of interest

Ethical statement

Animal experimental studies conducted in this manuscript was performed in accordance with the laid down ethical standards and approved by the Ethics Committee of the Federal University of Agriculture, Abeokuta, Nigeria and  the Animal Welfare Group Nigeria

Consent to participate/publish (All authors after reading agreed to paticipate and publish the manuscript)

Code availability ( Post Graduate School Repository, Federal   University of Agriculture, Abeokuta, Nigeria)

Authors’ contribution

All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Olubukola Precious Adepeju Idowu, Olajide Mark Sogunleand Olusegun Mark Obafemi Idowu. The first draft of the manuscript was written by Olubukola Precious Adepeju Idowu and all authors commented on draft versions of the manuscript. All authors read and approved the final manuscript for publishing

Authors and affiliations:

Agricultural Media Resources and Extension Centre, Federal University of Agriculture, P.M.B 2240, Abeokuta, Ogun State, Nigeria

Olubukola Precious Adepeju  Idowu    (ORCID ID   0000-0002-5591-3523)

Department of Animal Production and Health, Federal University of Agriculture, P.M.B 2240, Abeokuta, Ogun State, Nigeria

Olubukola Precious Adepeju  Idowu, (ORCID ID  0000-0002-5591-3523)

Olajide Mark Sogunle, (ORCID ID  0000-0001-9661-0089 )

Olajide A. Adeyemi(ORCID ID  0000-0003-3419-2402)

Kemi Ruth  Idowu (ORCID ID  0000-0003-4019-9387)

Department of Animal Nutrition, Federal University of Agriculture, P.M.B 2240, Abeokuta, Ogun State, Nigeria

Adedoyin Titi Amos, (ORCID ID   0000-0001-5926-7314)

Damilola Uthman Kareem, (ORCID ID   0000-0002-6986-876X)

Adeyemi Mustapha Bamgbose (ORCID ID   0000-0002-5000-2798)

Olusegun Mark Obafemi Idowu (ORCID ID   0000-0002-1200-3909)

References

  1. Adedibu, I.I., Ayorinde, K.L. and Musa, A.A., 2014. Identification of haematology markers suitable for improving productitity of helmeted guinea fowl (Numidia meleagris) American Journal of Experimental Agriculture. 4(10), 1186-1196.
  2. Dalle Zotte, A., Sartori, A.and Bordesan, V. 2013. Physical egg quality from organic versus conventional laying hens. Proc. XV European Symposium on the Quality of Eggs and Egg Products, Bergamo. Bergamo 15–19 September 2013.
  3. Kyere, C. G., Annor, S. Y., Kagya-Agyemang, J. K. and Korankye, O. 2017: Effect of egg size and day length on reproductive and growth performance, egg characteristics and blood profile of the Guinea fowl. Livestock Research for Rural Development. Volume 29, Article #180. Retrieved August 18, 2022, from http://www.lrrd.org/lrrd29/9/kyer29180.html
  4. Nedomová, Š., Severa, L. and Buchar, J. 2009. Influence of hen egg shape on eggshell compres-sive strength. International Agrophysic. 23: 249–256.
  5. Obike, O.M., Oke, U.K. and Azu, K.E., 2011. Comparison of egg production performance and egg quality traits of pearl and black strains of guinea fowl in a Humid rain Forest zone of Nigeria. International Journal of Poultry Science. 10(7), 547-551.
  6. Oke, O.E., Adejuyigbe, A.E., Idowu, O.P., Sogunle, O.M., Ladokun, A.O., Oso, A.O., Abioja, M.O., Abiona, J.A., Daramola, J.O., Whetto, M., Jacobs, E.B., Williams, T.J. and Njoku, C.P., 2015 Effects of housing systems on reproductive and physiological response of guinea fowl (Numida meleagris). Journal of Applied Animal Science, 8(1), pp. 47–55. https://www.thaiscience.info/Journals/Arti cle/JAAS/10972296.pd
  7. Portillo-Salgado, R., Bautista-Ortega, J., Chay-Canul, A.J., Sánchez-Casanova, R.E., Segura-Correa, J.C. and Cigarroa-Vázquez, F.A. 2022. Factors affecting productive performance of guinea fowl: a review . Tropical and Subtropical Agroecosystems 25 : 1-11
  8. Preisinger R. 2000. Lohmann tradition, praxiserfahrung und entwicklungsperspektiven. Lohmann Information 3:13–16
  9. Sánchez-Casanova, R., Sarmiento-Franco, L., Phillips, C.J.C. and Zulkifli, I., 2020. Do free-range systems have potential to improve broiler welfare in the tropics? World’s Poultry Science Journal, https://doi.org/10.1080/00439339.2020.17 07389
  10. Santos, F.B.O., Santos, A.A., Oviedo-Rondon, E.O. and Ferket, P.R. 2012. Influence of Housing System on Growth Performance and Intestinal Health of Salmonella-challenged Broiler Chickens. Current Research in Poultry Science, 2: 1-10. DOI: 10.17311/crpsaj.2012.1.10 URL: https://scialert.net/abstract/?doi=crpsaj.2012.1.10
  11. SAS Institute Inc. (2003). SAS/STAT user’s guide’ version 6, 4 Edition. Vol. 2 SAS inst., Cary; NC.
  12. Sarica, M., Boga, S. and Yamak, U.S., 2008. The effects of space allowance on egg yield, egg quality and plumage condition of laying hens in cages. Czech Journal of Animal Science 53, 346-353.
  13. Sekeroglu, A., Demir, E., Sarica, M. and Ulutas, Z. 2009. Effects of Housing Systems on Growth Performance, Blood Plasma Constituents and Meat Fatty Acids in Broiler Chickens. Pakistan Journal of Biological Sciences, 12: 631-636. DOI: 10.3923/pjbs.2009.631.636 URL: https://scialert.net/abstract/?doi=pjbs.2009.631.636
  14. Sokołowicz, Z,, Krawczyk, J. and Dykiel, M. 2018. The Effect of the type of alternative housing system, genotype and age of laying hens on egg quality. Annals of Animal Science, vol.18, no.2, 2018, pp.541-556. https://doi.org/10.2478/aoas-2018-0004
  15. Van Beekvelt, M.C.P., Colier, W.N.J.M, Weaver, R.A., and Van Engelen, B.G.M., 2001. Performance of near-infrared spectroscopy in measuring muscle consumption and blood flow in skeletal muscle. Journal of Applied Physiology, 90, 511-519.