Environmental Enrichments in Laying Hen Production Systems with Emphasis on Welfare and Egg Quality

To improve hen welfare, several studies have investigated various environmental enrichments that suit different laying hen production systems. The positive results of these studies can enable such environmental enrichments to be utilized in commercial laying hen production. This paper reviewed the effects of environmental enrichments in different laying hen production systems on hen welfare and egg quality. The successfully proven environmental enrichments in free-range production system include forage, shelterbelt, and artificial shade in outdoor area and novel objects and Hshaped perching structures in indoor. These are associated with increased range use that positively affects hen welfare. In aviary system, perches, and litter materials (e.g., straw, sand) as environmental enrichments are linked to improved behavioral expression, reduced stress, and enhanced immune system. Under the litter system, environmental enrichment with substrates (e.g., pecking stones, alfalfa blocks, silage, straw, barley) has been found to increase the foraging behavior of laying hens. This reduces severe feather pecking thus, improving the plumage condition of hens. Although the effects of environmental enrichments on hen welfare have been assessed and scientifically proven in the reviewed studies, significant progress of their impact on egg quality traits has not been reported. The studies have shown that environmental enrichments have no significant effect on egg quality traits. Also, appropriate pasture or plant species as environmental enrichments in free-range production system in relation to hen welfare and egg quality have not been identified. Therefore, it is important to continue studies on environmental enrichments while emphasizing their influence on egg quality since it is a major performance trait in the egg industry. In addition, there is a need for studies to identify ideal pasture or plant species for free-range production system that positively affects hen welfare and egg quality

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Abdel-Wareth AA, Lohakare JD. 2020. Productive performance, egg quality, nutrients digestibility, and physiological response of bovans brown hens fed various dietary inclusion levels of peppermint oil. Animal Feed Science and Technology, 267: 114554. doi.org/10.1016/j.anifeedsci.2020.114554.

Alberghina D, Biondi V, Passantino A, Giunta F, Panzera M. 2020. Plasma Serotonin in Laying Hens (Gallus gallus domesticus) With and Without Foot pad Dermatitis. International Journal of Tryptophan Research, 13: 1178646920927380. doi.org/10.1177%2F1178646920927380.

Appleby M.C. 2003a. The EU ban on battery cages: History and prospects. In D.J. Salem & A.N. Rowan (Eds.), The state of the animals II. Washington, DC: Humane Society Press. pp. 159-174.

Appleby MC. 2003b. The European Union ban on conventional cages for laying hens: History and prospects. Journal of Applied Animal Welfare Science, 6 (2): 103-21. doi.org/10.1207/S15327604JAWS0602_03.

Bain MM, Nys Y, Dunn IC. 2016. Increasing persistency in lay and stabilising egg quality in longer laying cycles. What are the challenges?. British Poultry Science, 57 (3): 330-8. doi.org/10.1080/00071668.2016.1161727.

Baker SL, Robison CI, Karcher DM, Toscano MJ, Makagon MM. 2020. Keel impacts and associated behaviors in laying hens. Applied Animal Behaviour Science, 222: 104886. doi.org/10.1016/j.applanim.2019.104886.

Bari MS, Cohen-Barnhouse AM, Campbell DL. 2020b. Early rearing enrichments influenced nest use and egg quality in free-range laying hens. Animal 2020; 14 (6): 1249-57. doi.org/10.1017/S1751731119003094

Bari MS, Downing JA, Dyall TR, Lee C, Campbell DL. 2020c. Relationships between rearing enrichments, range use, and an environmental stressor for free-range laying hen welfare. Frontiers in Veterinary Science, 7. doi.org/10.3389%2 Ffvets.2020.00480.

Bari MS, Laurenson YC, Cohen-Barnhouse AM, WalkdenBrown SW, Campbell DL. 2020a. Effects of outdoor ranging on external and internal health parameters for hens from different rearing enrichments. Peer Journal, 8: e8720. doi.org/10.7717/peerj.8720.

Bejaei M, Cheng KM. 2020. The effect of including full-fat dried black soldier fly larvae in laying hen diet on egg quality and sensory characteristics. Journal of Insects as Food and Feed, 6 (3): 305-314. doi.org/10.1016/j.psj.2020.01.029.

Bennett RM, Jones PJ, Nicol CJ, Tranter RB, Weeks CA. 2016. Consumer attitudes to injurious pecking in free range egg production. Animal Welfare, 25 (1): 91-100. doi.org/10.7120/09627286.25.1.091.

Bessei W. 2018. Impact of animal welfare on worldwide poultry production. World's Poultry Science Journal, 74 (2): 211-224. doi.org/10.1017/S0043933918000028.

Bhattacharya TK, Chatterjee RN, Dange M, Bhanja SK. 2019. Polymorphisms in GnRHI and GnRHII genes and their association with egg production and egg quality traits in chicken. British Poultry Science, 60 (3): 187-194. doi.org/10.1080/00071668.2019.1575505.

Bhattacharya TK, Chatterjee RN, Sharma RP, Rajkumar U, Niranjan M, Reddy BL. 2011. Association of polymorphism in the prolactin promoter and egg quality traits in laying hens. British Poultry Science, 52 (5): 551-557. doi.org/10.1080/ 00071668.2011.617727.

Blokhuis HJ, Van der Haar J. 1992. Effects of pecking incentives during rearing on feather pecking of laying hens. British Poultry Science, 33 (1): 17-24. doi.org/10.1080/ 00071669208417440.

Brantsæter M, Nordgreen J, Rodenburg TB, Tahamtani FM, Popova A, Janczak AM. 2016. Exposure to increased environmental complexity during rearing reduces fearfulness and increases use of three-dimensional space in laying hens (Gallus gallus domesticus). Frontiers in Veterinary Science, 3:14. doi.org/10.3389/fvets.2016.00014.

Brendler C, Kipper S, Schrader L. 2014. Vigilance and roosting behaviour of laying hens on different perch heights. Applied Animal Behavior Science, 157: 93-99. doi.org/10.1016/ j.applanim.2014.06.004.

Campbell DL, Bari MS, Rault JL. 2020a. Free-range egg production: its implications for hen welfare. Animal Production Science. AN19576. doi.org/10.1071/AN19576.

Campbell DL, De Haas EN, Lee C. 2019. A review of environmental enrichment for laying hens during rearing in relation to their behavioral and physiological development. Poultry Science, 98 (1): 9-28. doi.org/10.3382/ps/pey319.

Campbell DL, Dyall TR, Downing JA, Cohen-Barnhouse AM, Lee C. 2020b. Rearing enrichments affected ranging behavior in free-range laying hens. Frontiers in Veterinary Science, 7: 446. doi.org/10.3389%2Ffvets.2020.00446.

Campbell DL, Hinch GN, Downing JA, Lee C. 2017. Outdoor stocking density in free-range laying hens: effects on behaviour and welfare. Animal, 11 (6): 1036-1045. doi:10.1017/S1751731116002342.

Campbell DL, Makagon MM, Swanson JC, Siegford JM. 2016a. Laying hen movement in a commercial aviary: Enclosure to floor and back again. Poultry Science, 95 (1): 176-187. doi.org/10.3382/ps/pev186.

Campbell DL, Makagon MM, Swanson JC, Siegford JM. 2016b. Perch use by laying hens in a commercial aviary. Poultry Science, 95 (8): 1736-1742. doi.org/10.3382/ps/pew111.

Campderrich I, Nazar FN, Wichman A, Marin RH, Estevez I, Keeling LJ. 2019. Environmental complexity: A buffer against stress in the domestic chick. PloS 0ne, 14 (1): e0210270. doi.org/10.1371/journal.pone.0210270.

Campe A, Hoes C, Koesters S, Froemke C, Bougeard S, Staack M, Bessei W, Manton A, Scholz B, Schrader L, Thobe P. 2018. Analysis of the influences on plumage condition in laying hens: How suitable is a whole body plumage score as an outcome?. Poultry Science. 97 (2): 358-367. doi.org/10.3382/ps/pex321.

Carvalho RR, Palme R, da Silva Vasconcellos A. 2018. An integrated analysis of social stress in laying hens: The interaction between physiology, behaviour, and hierarchy. Behavioural Processes, 149: 43-51. doi.org/10.1016/ j.beproc.2018.01.016.

Caulfield MP, Padula MP. 2020. HPLC MS-MS analysis shows measurement of corticosterone in egg albumen is not a valid indicator of chicken welfare. Animals, 10 (5): 821. doi.org/10.3390/ani10050821.

Chielo LI, Pike T, Cooper J. 2016. Ranging behaviour of commercial free-range laying hens. Animals, 6 (5): 28. doi.org/10.3390/ani6050028.

Cronin GM, Glatz PC. 2020. Causes of feather pecking and subsequent welfare issues for the laying hen: a review. Animal Production Science. AN19628. doi.org/10.1071/ AN19628.

Cronin GM, Hopcroft RL, Groves PJ, Hall EJ, Phalen DN, Hemsworth PH. 2018. Why did severe feather pecking and cannibalism outbreaks occur? An unintended case study while investigating the effects of forage and stress on pullets during rearing. Poultry Science, 97 (5): 1484-14502. doi.org/10.3382/ps/pey022.

de Koning C, Barekatain R, Singh M, Drake K. 2019b. Saltbush (Atriplex nummularia and A. amnicola) as potential plants for free-range layer farms: consequences for layer performance, egg sensory qualities, and excreta moisture. Poultry Science, 98 (10): 4555-4564. doi.org/10.3382/ps/pez294.

de Koning C, Kitessa SM, Barekatain R, Drake K. 2019a. Determination of range enrichment for improved hen welfare on commercial fixed-range free-range layer farms. Animal Production Science, 59 (7): 1336-1348. doi.org/10.1071/ AN17757.

Decina C, Berke O, van Staaveren N, Baes CF, HarlanderMatauscheck A. 2019. Development of a scoring system to assess feather damage in Canadian laying hen flocks. Animals, 9 (7): 436. doi.org/10.3390/ani9070436.

Du X, Carpentier L, Teng G, Liu M, Wang C, Norton T. 2020. Assessment of laying hens’ thermal comfort using sound technology. Sensors, 20 (2): 473. doi.org/10.3390/ s20020473.

Duman M, Şekeroğlu A, Yıldırım A, Eleroğlu HA, Camcı Ö. 2016. Relation between egg shape index and egg quality characteristics. European Poultry Science, 80: 1-9. doi: 10.1399/eps.2016.117.

Esfahani MB, Moravej H, Ghaffarzadeh M, Paghaleh GA. 2021. Comparison the Zn-threonine, Zn-methionine, and Zn oxide on performance, egg quality, Zn bioavailability, and Zn content in egg and excreta of laying hens. Biological trace element research, 199 (1): 292-304. doi.org/10.1007/s12011- 020-02141-8.

Giersberg MF, Spindler B, Kemper N. 2017. Assessment of plumage and integument condition in dual-purpose breeds and conventional layers. Animals, 7 (12): 97. doi.org/10.3390/ani7120097.

Giersberg MF, Spindler B, Kemper N. 2019. Linear space requirements and perch use of conventional layer hybrids and dual-purpose hens in an aviary system. Frontiers in Veterinary Science, 6: 231. doi.org/10.3389/ fvets.2019.00231

Giersberg MF, Spindler B, Rodenburg B, Kemper N. 2020. The dual-purpose hen as a chance: Avoiding injurious pecking in modern laying hen husbandry. Animals, 10 (1): 16. . doi.org/10.3390/ani10010016.

Hartcher KM, Jones B. 2017. The welfare of layer hens in cage and cage-free housing systems. World's Poultry Science Journal, 73 (4): 767-782. doi.org/10.1017/ S0043933917000812.

Hartcher KM, Tran KT, Wilkinson SJ, Hemsworth PH, Thomson PC, Cronin GM. 2015. The effects of environmental enrichment and beak-trimming during the rearing period on subsequent feather damage due to feather-pecking in laying hens. Poultry Science, 94 (5): 852-859. doi.org/10.3382/ ps/pev061.

Heerkens JL, Delezie E, Ampe B, Rodenburg TB, Tuyttens FA. 2016b. Ramps and hybrid effects on keel bone and foot pad disorders in modified aviaries for laying hens. Poultry Science, 95 (11): 2479-2488. doi.org/10.3382/ps/pew157.

Heerkens JL, Delezie E, Rodenburg TB, Kempen I, Zoons J, Ampe B, Tuyttens FA. 2016a. Risk factors associated with keel bone and foot pad disorders in laying hens housed in aviary systems. Poultry Science, 95 (3): 482-488. doi.org/10.3382/ps/pev339.

Hofmann T, Schmucker SS, Bessei W, Grashorn M, Stefanski V. 2020. Impact of housing environment on the immune system in chickens: A review. Animals, 10 (7): 1138. doi.org/10.3390/ani10071138.

Hu JY, Hester PY, Xiong Y, Gates RS, Makagon MM, Cheng HW. 2019. Effect of cooled perches on the efficacy of an induced molt in White Leghorn laying hens previously exposed to heat stress. Poultry Science, 98 (10): 4290-4300. doi.org/10.3382/ps/pez317.

Iqbal Z, Drake K, Swick RA, Taylor PS, Perez-Maldonado RA, Ruhnke I. 2020. Effect of pecking stones and age on feather cover, hen mortality, and performance in free-range laying hens. Poultry Science, 99 (5): 2307-2314. doi.org/10.1016/ j.psj.2019.11.068.

Janczak AM, Riber AB. 2015. Review of rearing-related factors affecting the welfare of laying hens. Poultry Science, 94 (7): 1454-1469. doi.org/10.3382/ps/pev123.

Kittelsen KE, Jensen P, Christensen JP, Toftaker I, Moe RO, Vasdal G. 2020. Prevalence of Keel Bone Damage in Red Jungle Fowls (Gallus gallus)—A Pilot Study. Animals, 10 (9): 1655. doi.org/10.3390/ani10091655.

Larsen H, Cronin GM, Gebhardt-Henrich SG, Smith CL, Hemsworth PH, Rault JL. 2017. Individual ranging behaviour patterns in commercial free-range layers as observed through RFID tracking. Animals, (3): 21. doi.org/10.3390/ ani7030021.

Larsen H, Rault JL. 2021. Preference for artificial range enrichment design features in free-range commercial laying hens. 1-9. British Poultry Science. doi.org/10.1080/ 00071668.2021.1879993.

Li C, Zhang R, Wei H, Wang Y, Chen Y, Zhang H, Li X, Liu H, Li J, Bao J. 2021. Enriched environment housing improved the laying hen’s resistance to transport stress via modulating the heat shock protective response and inflammation. Poultry Science, 100 (3): 100939 doi.org/10.1016/j.psj.2020.12.036.

Liebers CJ, Schwarzer A, Erhard M, Schmidt P, Louton H. 2019. The influence of environmental enrichment and stocking density on the plumage and health conditions of laying hen pullets. Poultry Science, 98 (6): 2474-2488. doi.org/10.3382/ ps/pez024.

Liu Z, Sun C, Yan Y, Li G, Shi F, Wu G, Liu A, Yang N. 2018. Genetic variations for egg quality of chickens at late laying period revealed by genome-wide association study. Scientific Reports, 8 (1): 10832. doi:10.1038/s41598-018-29162-7.

Lordelo M, Cid J, Cordovil CM, Alves SP, Bessa RJ, Carolino I. 2020. A comparison between the quality of eggs from indigenous chicken breeds and that from commercial layers. Poultry Science, 99 (3): 1768-1776. doi.org/10.1016/ j.psj.2019.11.023.

MacLachlan SS, Ali AB, Toscano MJ, Siegford JM. 2020. Influence of later exposure to perches and nests on flock level distribution of hens in an aviary system during lay. Poultry Science, 99 (1): 30-38. doi.org/10.3382/ps/pez524.

Malchow J, Berk J, Puppe B, Schrader L. 2019. Perches or grids? What do rearing chickens differing in growth performance prefer for roosting?. Poultry Science, 98 (1): 29-38. doi.org/10.3382/ps/pey320.

Marume U, Mokagane JM, Shole CO, Hugo A. 2020. Citrullus lanatus essential oils inclusion in diets elicit nutraceutical effects on egg production, egg quality, and physiological characteristics in layer hens. Poultry Science, 99 (6): 3038- 3046. doi.org/10.3920/JIFF2019.0045.

Matur E, Akyazi İ, Eraslan E, Ergul Ekiz E, Eseceli H, Keten M, Metiner K, Aktaran Bala D. 2016. The effects of environmental enrichment and transport stress on the weights of lymphoid organs, cell‐mediated immune response, heterophil functions and antibody production in laying hens. Animal Science Journal, 87 (2): 284-292. doi.org/ 10.1111/asj.12411.

McAdie TM, Keeling LJ, Blokhuis HJ, Jones RB. 2005. Reduction in feather pecking and improvement of feather condition with the presentation of a string device to chickens. Applied Animal Behavior Science, 93 (1-2): 67-80. doi.org/10.1016/j.applanim.2004.09.004.

Mench JA, Rodenburg TB. 2018. Sustainability of laying hen housing systems. In Advances in Poultry Welfare. Woodhead Publishing. pp. 199-225. doi.org/10.1016/B978-0-08-100915 -4.00010-5.

Milisits G, Szász S, Donkó T, Budai Z, Almási A, Pőcze O, Ujvári J, Farkas TP, Garamvölgyi E, Horn P, Sütő Z. 2021. Comparison of Changes in the Plumage and Body Condition, Egg Production, and Mortality of Different Non-BeakTrimmed Pure Line Laying Hens during the Egg-Laying Period. Animals, 11 (2): 500. doi.org/10.3390/ani11020500.

Morrissey KL, Brocklehurst S, Baker L, Widowski TM, Sandilands V. 2016. Can non-beak treated hens be kept in commercial furnished cages? Exploring the effects of strain and extra environmental enrichment on behaviour, feather cover, and mortality. Animals, 6 (3): 17. doi.org/ 10.3390/ani6030017.

Nagle TA, Glatz PC. 2012. Free range hens use the range more when the outdoor environment is enriched. AsianAustralasian Journal of Animal Sciences, 25 (4): 584-591 doi.org/10.5713%2Fajas.2011.11051.

Newberry RC. 1995. Environmental enrichment: increasing the biological relevance of captive environments. Applied Animal Behavior Science, 44 (2-4): 229-243.

Nørgaard-Nielsen G, Vestergaard K, Simonsen HB. 1993. Effects of rearing experience and stimulus enrichment on feather damage in laying hens. Applied Animal Behavior Science, 38 (3-4): 345-352. doi.org/10.1016/0168-1591(93)90032-K.

Onbaşılar EE, Kahraman M, Güngör ÖF, Kocakaya A, Karakan T, Pirpanahi M, Doğan B, Metin D, Akan M, Şehu A, Elibol FE. 2020. Effects of cage type on performance, welfare, and microbiological properties of laying hens during the molting period and the second production cycle. Tropical Animal Health and Production, 52 (6): 3713-3724. doi.org/10.1007/ s11250-020-02409-0.

Petek M, Çavuşoğlu E. 2020. Welfare Assessment of Two Freerange Laying Hen Flocks in Turkey. Journal of Applied Animal Welfare Science, 1-8. doi.org/10.1080/ 10888705.2020.1790368.

Pettersson IC, Weeks CA, Nicol CJ. 2017. Provision of a resource package reduces feather pecking and improves ranging distribution on free-range layer farms. Applied Animal Behavior Science, 195: 60-66. doi.org/10.1016/ j.applanim.2017.06.007.

Pichová K, Bilčík B. 2017. Assessment of the effect of housing on feather damage in laying hens using IR thermography. Animal, 11 (4): 661-669. doi.org/10.1017/ S1751731116001981.

Rath PK, Mishra PK, Mallick BK, Behura NC. 2015. Evaluation of different egg quality traits and interpretation of their mode of inheritance in White Leghorns. Veterinary World, 8 (4): 449-452. doi.org/10.14202%2Fvetworld.2015.449-452.

Regmi P, Robison CI, Jones DR, Gast RK, Tempelman RJ, Karcher DM. 2018. Effects of different litter substrates and induced molt on production performance and welfare quality parameters of white Leghorn hens housed in multi-tiered aviary system. Poultry Science, 97 (10): 3397-3404. doi.org/10.3382/ps/pey211.

Rentsch AK, Rufener CB, Spadavecchia C, Stratmann A, Toscano MJ. 2019. Laying hen’s mobility is impaired by keel bone fractures and does not improve with paracetamol treatment. Applied Animal Behavior Science, 216: 19-25. doi.org/10.1016/j.applanim.2019.04.015.

Riber AB, Van de Weerd HA, De Jong IC, Steenfeldt S. 2018. Review of environmental enrichment for broiler chickens. Poultry Science, 97 (2): 378-396. doi.org/10.3382/ps/pex344.

Rizzi C. 2020. Yield performance, laying behaviour traits and egg quality of purebred and hybrid hens reared under outdoor conditions. Animals, 10 (4): 584. doi.org/10.3390/ ani10040584.

Ross M, Rausch Q, Vandenberg B, Mason G. 2020. Hens with benefits: Can environmental enrichment make chickens more resilient to stress?. Physiology & Behavior, 226: 113077. doi.org/10.1016/j.physbeh.2020.113077.

Rufener C, Abreu Y, Asher L, Berezowski JA, Sousa FM, Stratmann A, Toscano MJ. 2019. Keel bone fractures are associated with individual mobility of laying hens in an aviary system. Applied Animal Behavior Science, 217: 48-56. doi.org/10.1016/j.applanim.2019.05.007.

Rufener C, Makagon MM. 2020a. Keel bone fractures in laying hens: A systematic review of prevalence across age, housing systems, and strains. Journal of Animal Science, 98 (Supplement_1): S36-51. doi.org/10.1093/jas/skaa145.

Rufener C, Rentsch AK, Stratmann A, Toscano MJ. 2020b. Perch Positioning Affects both Laying Hen Locomotion and Forces Experienced at the Keel. Animals, 10 (7): 1223. doi.org/10.3390/ani10071223.

Saraiva S, Saraiva C, Oliveira I, Stilwell G, Esteves A. 2021. Effects of age, weight, and housing system on prevalence of dead on arrival and carcass condemnation causes in laying hens. Poultry Science, 100 (3): 100910. doi.org/10.1016/ j.psj.2020.12.012.

Scanes CG. 2016. Biology of stress in poultry with emphasis on glucocorticoids and the heterophil to lymphocyte ratio. Poultry Science, 95 (9): 2208-2215. doi.org/10.3382/ ps/pew137.

Schreiter R, Damme K, Freick M. 2020c. Edible Environmental Enrichments in Littered Housing Systems: Do Their Effects on Integument Condition Differ Between Commercial Laying Hen Strains?. Animals, 10 (12): 2434. doi.org/10.3390/ ani10122434.

Schreiter R, Damme K, Klunker M, Raoult C, von Borell E, Freick M. 2020a. Effects of edible environmental enrichments during the rearing and laying periods in a littered aviary—Part 1: integument condition in pullets and laying hens. Poultry Science, 99 (11): 5184-5196. doi.org/10.1016/ j.psj.2020.07.013.

Schreiter R, Damme K, Klunker M, Raoult C, von Borell E, Freick M. 2020b. Effects of edible environmental enrichments during the rearing and laying periods in a littered aviary—Part 2: physical development of pullets and performance, egg quality, and carcass composition in laying hens. Poultry Science, 99 (12): 6685-6696. doi.org/10.1016/j.psj.2020.08.040.

Schreiter R, Damme K, von Borell E, Vogt I, Klunker M, Freick M. 2019. Effects of litter and additional enrichment elements on the occurrence of feather pecking in pullets and laying hens–a focused review. Veterinary Medicine and Science, 5 (4): 500-507. doi.org/10.1002/vms3.184.

Sharma MK, White D, Chen C, Kim WK, Adhikari P. 2021. Effects of the housing environment and laying hen strain on tibia and femur bone properties of different laying phases of Hy-Line hens. Poultry Science, 100 (3): 100933. doi.org/10.1016/j.psj.2020.12.030.

Singh M, Ruhnke I, de Koning C, Drake K, Skerman AG, Hinch GN, Glatz PC. 2017. Demographics and practices of semiintensive free-range farming systems in Australia with an outdoor stocking density of≤ 1500 hens/hectare. PLoS One, 12 (10): e0187057. doi.org/10.1371/journal.pone.0187057.

Sirovnik J, Stratmann A, Gebhardt-Henrich SG, Würbel H, Toscano MJ. 2018. Feeding from perches in an aviary system reduces aggression and mortality in laying hens. Applied Animal Behavior Science, 202: 53-62. doi.org/10.1016/ j.applanim.2018.01.005.

Sokołowicz Z, Dykiel M, Topczewska J, Krawczyk J, Augustyńska-Prejsnar A. 2020. The Effect of the Type of Non-Caged Housing System, Genotype and Age on the Behaviour of Laying Hens. Animals, 10 (12): 2450. doi.org/10.3390/ani10122450.

Stadig LM, Ampe BA, Van Gansbeke S, Van den Bogaert T, D’Haenens E, Heerkens JL, Tuyttens FM. 2016. Survey of egg farmers regarding the ban on conventional cages in the EU and their opinion of alternative layer housing systems in Flanders, Belgium. Poultry Science, 95 (3): 715-725. doi.org/10.3382/ps/pev334.

Steenfeldt S, Kjaer JB, Engberg RM. 2007. Effect of feeding silages or carrots as supplements to laying hens on production performance, nutrient digestibility, gut structure, gut microflora and feather pecking behaviour. British Poultry Science, 48 (4): 454-468. doi.org/10.1080/ 00071660701473857.

Stratmann A, Fröhlich EK, Gebhardt-Henrich SG, HarlanderMatauschek A, Würbel H, Toscano MJ. 2015. Modification of aviary design reduces incidence of falls, collisions and keel bone damage in laying hens. Applied Animal Behaviour Science, 165: 112-123. doi.org/10.1016/ j.applanim.2015.01.012.

Tahamtani FM, Nordgreen J, Brantsæter M, Østby GC, Nordquist RE, Janczak AM. 2016. Does early environmental complexity influence Tyrosine hydroxylase in the chicken hippocampus and “Prefrontal” caudolateral nidopallium?. Frontiers in Veterinary Science, 3: 8. doi.org/10.3389/ fvets.2016.00008.

Tahamtani FM, Nordgreen J, Nordquist RE, Janczak AM. 2015. Early life in a barren environment adversely affects spatial cognition in laying hens (Gallus gallus domesticus). Frontiers in Veterinary Science, 2: 3. doi.org/10.3389/ fvets.2015.00003.

Tainika B, Şekeroğlu A. 2020. Effect of production systems for laying hens on hen welfare. Turkish Journal of AgricultureFood Science and Technology, 8 (1): 239-245. doi.org/10.24925/turjaf.v8i1.239-245.3251.

Tauson R, Kjaer J, Maria GA, Cepero R, Holm KE. 2005. Applied scoring of integument and health in laying hens. Animal Science Paper, 23 (Suppl 1): 153-9.

Taylor PS, Hemsworth PH, Groves PJ, Gebhardt-Henrich SG, Rault JL. 2020. Frequent range visits further from the shed relate positively to free-range broiler chicken welfare. Animal, 14 (1) :138-149. doi.org/10.1017/ S1751731119001514.

Thøfner I, Hougen HP, Villa C, Lynnerup N, Christensen JP. 2020. Pathological characterization of keel bone fractures in laying hens does not support external trauma as the underlying cause. Plos One, 15 (3): e0229735. doi.org/10.1371/journal.pone.0229735.

Tilbrook AJ, Fisher AD. 2020. Stress, health and the welfare of laying hens. Animal Production Science. AN19666. doi.org/10.1071/AN19666.

Toscano MJ, Dunn IC, Christensen JP, Petow S, Kittelsen K, Ulrich R. 2020. Explanations for keel bone fractures in laying hens: are there explanations in addition to elevated egg production?. Poultry Science, 99 (9): 4183-4194. doi.org/10.1016/j.psj.2020.05.035.

Van den Oever AC, Bolhuis JE, van de Ven LJ, Kemp B, Rodenburg TB. 2020. High levels of contact dermatitis and decreased mobility in broiler breeders, but neither have a relationship with floor eggs. Poultry Science, 99 (7): 3355- 3362. doi.org/10.1016/j.psj.2020.04.010.

van Staaveren N, Ellis J, Baes CF, Harlander-Matauschek A. 2021. A meta-analysis on the effect of environmental enrichment on feather pecking and feather damage in laying hens. Poultry Science, 100 (2): 397-411. https://doi.org/ 10.1016/j.psj.2020.11.006.

Veissier I, Boissy A. 2007. Stress and welfare: Two complementary concepts that are intrinsically related to the animal's point of view. Physiology and Behavior, 92 (3): 429- 433. doi.org/10.1016/j.physbeh.2006.11.008.

Wang G, Ekstrand C, Svedberg J. 1998. Wet litter and perches as risk factors for the development of foot pad dermatitis in floor-housed hens. British Poultry Science, 39 (2): 191-197. doi.org/10.1080/00071669889114.

Weeks CA, Nicol CJ. 2006. Behavioural needs, priorities and preferences of laying hens. World's Poultry Science Journal, 62 (2): 296-307. doi.org/10.1079/WPS200598.

Welfare Quality. 2009. Welfare Quality R assessment protocol for poultry (broilers, laying hens). Lelystad, Netherlands: Welfare Quality R Consortium.

Widowski T, Torrey S. 2018. Rearing young birds for adaptability. In: Mench JA. editor. Advances in Poultry Welfare. Duxford: Woodhead Publishing Group. pp. 49–77.

Yılmaz Dikmen B, Ipek A, Şahan Ü, Sözcü A, Baycan SC. 2017. Impact of different housing systems and age of layers on egg quality characteristics. Turkish Journal of Veterinary and Animal Sciences, 41 (1): 77-84.

Zepp M, Louton H, Erhard M, Schmidt P, Helmer F, Schwarzer A. 2018. The influence of stocking density and enrichment on the occurrence of feather pecking and aggressive pecking behavior in laying hen chicks. Journal of Veterinary Behavior, 24: 9-18. doi.org/10.1016/j.jveb.2017.12.005.