Animal Bioscience

Asian Australasian Association of Animal Production Societies (아세아태평양축산학회)
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The interaction effects of the naked neck gene and housing system on egg production, egg quality, blood biochemical parameters and immunity of laying hens under hot climate

  • Osama Abou-Emera (Department of Animal and Poultry Production, College of Agriculture and Food, Qassim University) ;
  • Ibrahim Al-Homidan (Department of Animal and Poultry Production, College of Agriculture and Food, Qassim University) ;
  • Gamal Rayan (Department of Animal and Fish Production, College of Agricultural and Food Sciences, King Faisal University) ;
  • Moataz Fathi (Department of Animal and Poultry Production, College of Agriculture and Food, Qassim University)
  • Received : 2024.12.04
  • Accepted : 2025.05.27
  • Published : 2025.12.01
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Abstract

Objective: Poultry producers use alternative housing arrangements, such as free-range systems, to allow birds to express their natural behaviors and to enhance consumer confidence in poultry products. Free-range systems provide hens with access to open spaces and better airflow, offering opportunities for thermoregulation through natural behaviors such as seeking shade or dust bathing. Compared to confined cage conditions, this can help reduce the negative effects of heat stress. In this study, we examined the productivity of laying hens segregated for the naked neck gene (Na) and raised in two distinct housing systems. Methods: A total of 540 laying hens, 24 weeks of age, were randomly assigned to a 2×3 factorial design consisting of three genotypes (NaNa, Nana, and nana) and two housing systems (wire cages and free-range pens). Productive performance, egg quality characteristics, immune response, and blood parameters were evaluated over a three-month period during the hot summer season. Results: The results showed that introducing the Na gene into chickens raised under hot climate conditions improved egg production, cell-mediated immunity, and eggshell strength. A significant reduction in blood cholesterol levels and the cumulative percentage of broken eggs was observed in naked neck genotypes (NaNa and Nana) compared to the normally feathered genotype (nana). Hens kept in cages produced significantly heavier eggs compared to those in the free-range system. Laying hens kept in a free-range system exhibited a higher relative yolk weight and an increased shell percentage. Additionally, a significant decrease in plasma cholesterol levels was found in layers raised in free-range systems compared to those in wire cages. Eggs produced by hens reared in free-range systems also had a darker yellow yolk color compared to those from caged hens. Conclusion: Introducing the Na gene into laying hens raised in free-range housing could be beneficial for improving egg production, immunity, and egg quality under high ambient temperatures.

Keywords

Acknowledgement

The researchers would like to thank the Deanship of Graduate Studies and Scientific research at Qassim University for financial support (QU-APC-2025).

References

  1. He S, Lin J, Jin Q, et al. The relationship between animal welfare and farm profitability in cage and free-range housing systems for laying hens in China. Animals 2022;12:2090. https://doi.org/10.3390/ani12162090
  2. Rodenburg TB, Tuyttens FAM, De Reu K, Herman L, Zoons J, Sonck B. Welfare assessment of laying hens in furnished cages and non-cage systems: an on-farm comparison. Anim Welf 2023;17:363-73. https://doi.org/10.1017/S096272860002786X
  3. Campbell DLM, Bari MS, Rault JL. Free-range egg production: its implications for hen welfare. Anim Prod Sci 2021;61: 848-55. https://doi.org/10.1071/AN19576
  4. Ayoub MA, El-Adel MA, Nossair MA, et al. Impacts of heat stress on some performance parameters of broiler chicken reared under different stocking densities. J Adv Vet Res 2023; 13:577-83.
  5. Rehman MS, Mahmud A, Mehmood S, Pasha TN, Hussian J, Khan MT. Blood biochemistry and immune response in Aseel chicken under free range, semi-intensive, and confinement rearing systems. Poult Sci 2017;96:226-33. https://doi.org/10.3382/ps/pew278
  6. Sokołowicz Z, Krawczyk J, Dykiel M. The effect of the type of alternative housing system, genotype and age of laying hens on egg quality. Ann Anim Sci 2018;18:541-56. https://doi.org/10.2478/aoas-2018-0004
  7. Sharma MK, McDaniel CD, Kiess AS, Loar II RE, Adhikari P. Effect of housing environment and hen strain on egg production and egg quality as well as cloacal and eggshell microbiology in laying hens. Poult Sci 2022;101:101595. https://doi.org/10.1016/j.psj.2021.101595
  8. Bhuiya MSU, Salam MA. Seed production of Sesbania rostrata through vegetative propagation. J Bangaldesh Agric Univ 2003;1:13-7. https://doi.org/10.22004/ag.econ.276302
  9. Spain CV, Freund D, Mohan-Gibbons H, Meadow RG, Beacham L. Are they buying it? United States consumers' changing attitudes toward more humanely raised meat, eggs, and dairy. Animals 2018;8:128. https://doi.org/10.3390/ani8080128
  10. Sărăcilă M, Panaite TD, Tabuc C, et al. Dietary ascorbic acid and chromium supplementation for broilers reared under thermoneutral conditions vs. high heat stress. Sci Pap Anim Sci Ser 2020;73:41-7.
  11. Hasan MN, Chand N, Naz S, et al. Mitigating heat stress in broilers by dietary dried tamarind (Tamarindus indica L.) pulp: effect on growth and blood traits, oxidative status and immune response. Livest Sci 2022;264:105075. https://doi.org/10.1016/j.livsci.2022.105075
  12. Fathi MM, Galal A, Radwan LM, Abou-Emera OK, AlHomidan IH. Using major genes to mitigate the deleterious effects of heat stress in poultry: an updated review. Poult Sci 2022;101:102157. https://doi.org/10.1016/j.psj.2022.102157
  13. Patra B, Choudhary S, Purohit H, et al. Importance of major genes to compensate for the harmful summer climatic effects in fowl. Indian J Anim Health 2025;64:1-5. https://doi.org/10.36062/ijah.2025.01424
  14. Fernandes E, Raymundo A, Martins LL, Lordelo M, de Almeida AM. The naked neck gene in the domestic chicken: a genetic strategy to mitigate the impact of heat stress in poultry production: a review. Animals 2023;13:1007. https://doi.org/10.3390/ani13061007
  15. Duah KK, Essuman EK, Boadu VG, Olympio OS, Akwetey W. Comparative study of indigenous chickens on the basis of their health and performance. Poult Sci 2020;99:2286-92. https://doi.org/10.1016/j.psj.2019.11.049
  16. Rayan GN, El-Attar AH, Fathi MM. Eggshell and bone quality in two different genetic groups of aged layer breeders. Braz J Poult Sci 2020;22:eRBCA-2020-1250. https://doi.org/10.1590/1806-9061-2020-1250
  17. Fathi M, Al-Homidan I, Al-Dokhail A, Ebeid T, Abou-Emera O, Alsagan A. Effects of dietary probiotic (Bacillus subtilis) supplementation on productive performance, immune response and egg quality characteristics in laying hens under high ambient temperature. Ital J Anim Sci 2018;17:804-14. https://doi.org/10.1080/1828051X.2018.1425104
  18. Fathi M, Al-Homidan I, Rayan G, El-Safty S, Ebeid T1,4, Abou-Emera O. Laying performance, immune response and antioxidant properties of hens segregating for naked neck and frizzle genes under low ambient temperature. Czech J Anim Sci 2019;64:216-25. https://doi.org/10.17221/221/2018-CJAS
  19. SAS Institute. JMP 11 multivariate methods. SAS Institute;2013.
  20. Chielo LI, Pike T, Cooper J. Ranging behaviour of commercial free-range laying hens. Animals 2016;6:28. https://doi.org/10.3390/ani6050028
  21. Campbell DLM, Hinch GN, Downing JA, Lee C. Outdoor stocking density in free-range laying hens: effects on behaviour and welfare. Animal 2017;11:1036-45. https://doi.org/10.1017/S1751731116002342
  22. Campbell DLM, Bari MS, Rault JL. Free-range egg production: its implications for hen welfare. Anim Prod Sci 2020;61: 848-55. https://doi.org/10.1071/AN19576
  23. Alig BN, Ferket PR, Malheiros RD, Anderson KE. The effect of housing environment on egg production, USDA egg size, and USDA grade distribution of commercial white egg layers. Poultry 2023;2:204-21. https://doi.org/10.3390/poultry2020017
  24. Ahammed M, Chae BJ, Lohakare J, et al. Comparison of aviary, barn and conventional cage raising of chickens on laying performance and egg quality. Asian-Australas J Anim Sci 2014;27:1196-203. https://doi.org/10.5713/ajas.2013.13394
  25. Karcher DM, Jones DR, Abdo Z, Zhao Y, Shepherd TA, Xin H. Impact of commercial housing systems and nutrient and energy intake on laying hen performance and egg quality parameters. Poult Sci 2015;94:485-501. https://doi.org/10.3382/ps/peu078
  26. Iqbal J, Mukhtar N, Rehman ZU, et al. Effects of egg weight on the egg quality, chick quality, and broiler performance at the later stages of production (week 60) in broiler breeders. J Appl Poult Res 2017;26:183-91. https://doi.org/10.3382/japr/pfw061
  27. Khanal T, Bédécarrats GY, Widowski TM, Kiarie EG. Rearing cage type and dietary limestone particle size: II, effects on egg production, eggshell, and bone quality in Lohmann selected Leghorn-Lite hens. Poult Sci 2020;99:5763-70. https://doi.org/10.1016/j.psj.2020.06.079
  28. Fathi MM, Galal A, El-Safty S, Mahrous M. Naked neck and frizzle genes for improving chickens raised under high ambient temperature: I. growth performance and egg production. World's Poult Sci J 2013;69:813-32. https://doi.org/10.1017/S0043933913000834
  29. Holt PS, Davies RH, Dewulf J, et al. The impact of different housing systems on egg safety and quality. Poult Sci 2011;90: 251-62. https://doi.org/10.3382/ps.2010-00794
  30. Voslářová E, Hanzálek Z, Večerek V, Straková E, Suchý P. Comparison between laying hen performance in the cage system and the deep litter system on a diet free from animal protein. Acta Vet Brno 2006;75:219-25. https://doi.org/10.2754/avb200675020219
  31. Fathi M, Ebeid T, Rayan G, El-Safty S, Abou-Emera O. Genetic differences in eggshell ultrastructural properties of Saudi native chicken breeds kept at high ambient temperatures. Czech J Anim Sci 2018;63:363-70. https://doi.org/10.17221/29/2018-CJAS
  32. Rizzi C, Verdiglione R. Testicular growth and comb and wattles development in three Italian chicken genotypes reared under free-range conditions. Ital J Anim Sci 2015;14:3653. https://doi.org/10.4081/ijas.2015.3653
  33. Rizzi L, Simioli M, Martelli G, Paganelli R, Sardi L. Effects of organic farming on egg quality and welfare of laying hens. Worlds Poult Sci J 2006;62:165-9.
  34. Solomon SE. The eggshell: strength, structure and function. Br Poult Sci 2010;51:52-9. https://doi.org/10.1080/00071668.2010.497296
  35. Lichovníková M, Zeman L. Effect of housing system on the calcium requirement of laying hens and on eggshell quality. Czech J Anim Sci 2008;53:162-8. https://doi.org/10.17221/375-CJAS
  36. Salahuddin M, Howlider MAR. Effect of breed and season on egg-quality traits of fowl. Indian J Anim Sci 1991;61:859-63. https://doi.org/10.18805/ijar.v0iOF.8458
  37. Singh M, Ruhnke I, de Koning C, et al. Demographics and practices of semi-intensive free-range farming systems in Australia with an outdoor stocking density of ≤1500 hens/hectare. PLOS ONE 2017;12:e0187057. https://doi.org/10.1371/journal.pone.0187057
  38. Fathi M, Al-Homidan I, Rayan G, El-Safty S, Ebeid T, AbouEmera O. Laying performance, immune response and antioxidant properties of hens segregating for naked neck and frizzle genes under low ambient temperature. Czech J Anim Sci 2019;64:216-25. https://doi.org/10.17221/221/2018-CJAS
  39. Adenaike AS, Akpan U, Awopejo OO, et al. Characterization of the cecal microbiome composition of Nigerian indigenous chickens. Trop Anim Health Prod 2022;54:211. https://doi.org/10.1007/s11250-022-03191-x
  40. Patra BN, Bais RKS, Sharma D, Singh BP, Prasad RB, Bhushan B. Immunocompetence status of white plumage naked neck versus normally feathered broilers in tropical climates. AsianAustralas J Anim Sci 2004;17:560-3. https://doi.org/10.5713/ajas.2004.560
  41. Haunshi S, Sharma D, Nayal LMS, Singh DP, Singh RV. Effect of naked neck gene (NA) and frizzle gene (F) on immunocompetence in chickens. Br Poult Sci 2002;43:28-32. https://doi.org/10.1080/00071660120109863
  42. Zita L, Jeníková M, Härtlová H. Effect of housing system on egg quality and the concentration of cholesterol in egg yolk and blood of hens of native resources of the Czech Republic and Slovakia. J Appl Poult Res 2018;27:380-8. https://doi.org/10.3382/japr/pfy009
  43. Pavlík A, Pokludová M, Zapletal D, Jelínek P. Effects of housing systems on biochemical indicators of blood plasma in laying hens. Acta Vet Brno 2007;76:339-47. https://doi.org/10.2754/avb200776030339
  44. DİktaŞ M, Şekeroğlu A, Duman M, Yildirim A. Effect of different housing systems on production and blood profile of slow-growing broilers. Kafkas Üniv Vet Fak Derg 2015;21: 521-6. https://doi.org/10.9775/kvfd.2014.12867
  45. Dutta RK, Islam MS, Kabir MA. Haematological and biochemical profiles of indigenous, exotic and hybrid chicken breeds (Gallus domesticus L.) from Rajshahi, Bangladesh. Bangladesh J Zool 2013;41:135-44. https://doi.org/10.3329/bjz.v41i2.23314
  46. Rajkumar U, Reddy BLN, Rajaravindra KS, et al. Effect of naked neck gene on immune competence, serum biochemical and carcass traits in chickens under a tropical climate. AsianAustralas J Anim Sci 2010;23:867-72. https://doi.org/10.5713/ajas.2010.90548