Trends in Measurement Techniques in Laying Hen Farm Welfare: A Review
Abstract
Animal welfare is a crucial issue in animal production, and researchers are seeking optimal methods to evaluate animal welfare in the field. In poultry farming, laying hen health and welfare are critical to consumer perception of product quality. The aim of the review was to examine traditional and advanced measurement trends of animal welfare in laying hens’ farms. Emerging technologies have facilitated a more profound comprehension of animal responses to diverse scenarios encountered in livestock production systems. Currently, conventional methods, such as behavioral observations, are time-consuming and highly dependent on the experienced observer’s expertise; likewise, other valuable indicators, including physiological parameters, hormonal levels, thermographic changes in the body, and hematological parameters, are widely used but are being re-evaluated. Currently, technological advances are developing comparatively non-invasive methods for multiple and long-term monitoring, such as machine vision and deep learning algorithms to track bird behavior. In addition, molecular techniques have emerged as promising tools to understand the cellular responses under internal or external stressful conditions and improve farm animal welfare. However, several challenges exist in terms of standardization and implementation of the new technologies, especially in developing countries. These challenges include limited access to advanced tools, costs, among others, and hinder implementation. In this review, we conclude that welfare research requires a holistic and interdisciplinary approach, utilizing both conventional measurements and new technologies to enable a more comprehensive assessment of animal welfare.
Full text article
References
Abdel-Khalik, J., Björklund, E., & Hansen, M. (2013). Simultaneous determination of endogenous steroid hormones in human and animal plasma and serum by liquid or gas chromatography coupled to tandem mass spectrometry. Journal of Chromatography B, 928, 58–77. https://doi.org/10.1016/j.jchromb.2013.03.013
Adaway, J. E., Keevil, B. G., & Owen, L. J. (2015). Liquid chromatography tandem mass spectrometry in the clinical laboratory. Annals of Clinical Biochemistry, 52(1), 18–38. https://doi.org/10.1177/0004563214557678
Adnane, M., de Almeida, A. M., & Chapwanya, A. (2024). Unveiling the power of proteomics in advancing tropical animal health and production. Tropical Animal Health and Production, 56(5), 182. https://doi.org/10.1007/s11250-024-04037-4
Afrouziyeh, M., & Zuidhof, M. J. (2022). Impact of broiler breeder growth trajectory on plasma corticosterone concentration: a comparison of analytical methods. Poultry Science, 101(5), 101792. https://doi.org/10.1016/j.psj.2022.101792
Ahmmed, P., Reynolds, J., Bozkurt, A., & Regmi, P. (2023). Continuous heart rate variability monitoring of freely moving chicken through a wearable electrocardiography recording system. Poultry Science, 102(2), 102375. https://doi.org/10.1016/j.psj.2022.102375
Alemu, S. W., Calus, M. P. L., Muir, W. M., Peeters, K., Vereijken, A., & Bijma, P. (2016). Genomic prediction of survival time in a population of brown laying hens showing cannibalistic behavior. Genetics Selection Evolution, 48, 1–10. https://doi.org/10.1186/s12711-016-0247-4
Alm, M., Holm, L., Tauson, R., & Wall, H. (2014). Corticosterone metabolites in laying hen droppings—Effects of fiber enrichment, genotype, and daily variations. Poultry Science, 93(10), 2615–2621. https://doi.org/10.3382/ps.2014-04193
Anjum, M. S., Sandhu, M. A., Ur-Rahman, Z., & Safdar, A. (2016). Circulating metabolic and reproductive hormone changes in laying hens kept under various heat-combating systems. Turkish Journal of Veterinary & Animal Sciences, 40(6), 730–736. https://doi.org/10.3906/vet-1602-84
Astill, J., Dara, R. A., Fraser, E. D. G., & Sharif, S. (2018). Detecting and predicting emerging disease in poultry with the implementation of new technologies and big data: A focus on avian influenza virus. Frontiers in Veterinary Science, 5, 263. https://doi.org/10.3389/fvets.2018.00263
Attia, Y. A., Rahman, M. T., Hossain, M. J., Basiouni, S., Khafaga, A. F., Shehata, A. A., & Hafez, H. M. (2022). Poultry production and sustainability in developing countries under the COVID-19 crisis: Lessons learned. Animals, 12(5), 644. https://doi.org/10.3390/ani12050644
Aydin, A., & Berckmans, D. (2016). Using sound technology to automatically detect the short-term feeding behaviours of broiler chickens. Computers and Electronics in Agriculture, 121, 25–31. https://doi.org/10.1016/j.compag.2015.11.010
Aydin, S. (2015). A short history, principles, and types of ELISA, and our laboratory experience with peptide/protein analyses using ELISA. Peptides, 72, 4–15. https://doi.org/10.1016/j.peptides.2015.04.012
Babington, S., Tilbrook, A. J., Maloney, S. K., Fernandes, J. N., Crowley, T. M., Ding, L., Fox, A. H., Zhang, S., Kho, E. A., & Cozzolino, D. (2024). Finding biomarkers of experience in animals. Journal of Animal Science and Biotechnology, 15(1), 28. https://doi.org/10.1186/s40104-023-00989-z
Bahrndorff, S., Alemu, T., Alemneh, T., & Lund Nielsen, J. (2016). The microbiome of animals: implications for conservation biology. International Journal of Genomics, 2016(1), 5304028. https://doi.org/10.1155/2016/5304028
Baker, L., Muir, P., & Sample, S. J. (2019). Genome-wide association studies and genetic testing: understanding the science, success, and future of a rapidly developing field. Journal of the American Veterinary Medical Association, 255(10), 1126–1136. https://doi.org/10.2460/javma.255.10.1126
Banakar, A., Sadeghi, M., & Shushtari, A. (2016). An intelligent device for diagnosing avian diseases: Newcastle, infectious bronchitis, avian influenza. Computers and Electronics in Agriculture, 127, 744–753. https://doi.org/10.1016/j.compag.2016.08.006
Banerjee, D., Daigle, C. L., Dong, B., Wurtz, K., Newberry, R. C., Siegford, J. M., & Biswas, S. (2014). Detection of jumping and landing force in laying hens using wireless wearable sensors. Poultry Science, 93(11), 2724–2733. https://doi.org/10.3382/ps.2014-04006
Barnett, J. L., & Hemsworth, P. H. (2003). Science and its application in assessing the welfare of laying hens in the egg industry. Australian Veterinary Journal, 81(10), 615–624. https://doi.org/10.1111/j.1751-0813.2003.tb12506.x
Barnett, J. L., Hemsworth, P. H., Hennessy, D. P., McCallum, T. H., & Newman, E. A. (1994). The effects of modifying the amount of human contact on behavioural, physiological and production responses of laying hens. Applied Animal Behaviour Science, 41(1–2). https://doi.org/10.1016/0168-1591(94)90054-X
Bateson, M., & Martin, P. (2021). Measuring behaviour: an introductory guide. Cambridge university press. https://doi.org/10.1017/9781108776462
Beaulieu, M. (2024). Capturing wild animal welfare: a physiological perspective. Biological Reviews, 99(1), 1–22. https://doi.org/10.1111/brv.13009
Bekhbat, M., Glasper, E. R., Rowson, S. A., Kelly, S. D., & Neigh, G. N. (2018). Measuring corticosterone concentrations over a physiological dynamic range in female rats. Physiology & Behavior, 194, 73–76. https://doi.org/10.1016/j.physbeh.2018.04.033
Ben Sassi, N., Averós, X., & Estevez, I. (2016). Technology and poultry welfare. Animals, 6(10), 62. https://doi.org/10.3390/ani6100062
Bhanja, S. K., & Bhadauria, P. (2018). Behaviour and welfare concepts in laying hens and their association with housing systems. https://doi.org/10.5958/0974-8180.2018.00009.0
Bird, A. (2002). DNA methylation patterns and epigenetic memory. Genes & Development, 16(1), 6–21. https://doi.org/10.1101/gad.947102
Bowden, J. A., Colosi, D. M., Mora-Montero, D. C., Garrett, T. J., & Yost, R. A. (2009). Enhancement of chemical derivatization of steroids by gas chromatography/mass spectrometry (GC/MS). Journal of Chromatography B, 877(27), 3237–3242. https://doi.org/10.1016/j.jchromb.2009.08.005
Brito, L. F., Oliveira, H. R., McConn, B. R., Schinckel, A. P., Arrazola, A., Marchant-Forde, J. N., & Johnson, J. S. (2020). Large-scale phenotyping of livestock welfare in commercial production systems: a new frontier in animal breeding. Frontiers in Genetics, 11, 552352. https://doi.org/10.3389/fgene.2020.00793
Broom, D. M. (2010). Welfare of animals: behavior as a basis for decisions. Encyclopedia of Animal Behavior, 580-584. https://doi.org/10.1016/B978-0-08-045337-8.00080-2
Broom, D. M., & Johnson, K. G. (1993). Stress and animal welfare (1st edition). Springer Dordrecht. https://doi.org/10.1007/978-94-024-0980-2
Budhlakoti, N., Kushwaha, A. K., Rai, A., Chaturvedi, K. K., Kumar, A., Pradhan, A. K., Kumar, U., Kumar, R. R., Juliana, P., & Mishra, D. C. (2022). Genomic selection: A tool for accelerating the efficiency of molecular breeding for development of climate-resilient crops. Frontiers in Genetics, 13, 832153. https://doi.org/10.3389/fgene.2022.832153
Cai, Z., Cui, J., Yuan, H., & Cheng, M. (2023). Application and research progress of infrared thermography in temperature measurement of livestock and poultry animals: A review. Computers and Electronics in Agriculture, 205. https://doi.org/10.1016/j.compag.2022.107586
Cammen, K. M., Andrews, K. R., Carroll, E. L., Foote, A. D., Humble, E., Khudyakov, J. I., Louis, M., McGowen, M. R., Olsen, M. T., & Van Cise, A. M. (2016). Genomic methods take the plunge: recent advances in high-throughput sequencing of marine mammals. Journal of Heredity, 107(6), 481–495. https://doi.org/10.1093/jhered/esw044
Campbell, A. M., Johnson, A. M., Persia, M. E., & Jacobs, L. (2022). Effects of housing system on anxiety, chronic stress, fear, and immune function in bovan brown laying hens. Animals, 12(14), 1803. https://doi.org/10.3390/ani12141803
Campo, J. L., Gil, M. G., & Davila, S. G. (2005). Effects of specific noise and music stimuli on stress and fear levels of laying hens of several breeds. Applied Animal Behaviour Science, 91(1–2), 75–84. https://doi.org/10.1016/j.applanim.2004.08.028
Carbajal, A., Tallo-Parra, O., Sabes-Alsina, M., Mular, I., & Lopez-Bejar, M. (2014). Feather corticosterone evaluated by ELISA in broilers: a potential tool to evaluate broiler welfare. Poultry Science, 93(11), 2884–2886. https://doi.org/10.3382/ps.2014-04092
Carpentier, L., Vranken, E., Berckmans, D., Paeshuyse, J., & Norton, T. (2019). Development of sound-based poultry health monitoring tool for automated sneeze detection. Computers and Electronics in Agriculture, 162, 573–581. https://doi.org/10.1016/j.compag.2019.05.013
Carvalho, C. L., Andretta, I., Galli, G. M., Martins, G. B., Camargo, N. de O. T., Stefanello, T. B., Melchior, R., & Da Silva, M. K. (2022). Dietary supplementation with β-mannanase and probiotics as a strategy to improve laying hen’s welfare. Frontiers in Veterinary Science, 9, 985947. https://doi.org/10.3389/fvets.2022.985947
Caulfield, M. P., & Padula, M. P. (2020). HPLC MS-MS analysis shows measurement of corticosterone in egg albumen is not a valid indicator of chicken welfare. Animals, 10(5), 821. https://doi.org/10.3390/ani10050821
Chafi, S., & Ballesteros, E. (2022). A sensitive, robust method for determining natural and synthetic hormones in surface and wastewaters by continuous solid-phase extraction–gas chromatography–mass spectrometry. Environmental Science and Pollution Research, 29(35), 53619–53632. https://doi.org/10.1007/s11356-022-19577-1
Chen, X., Sun, X., Chimbaka, I. M., Qin, N., Xu, X., Liswaniso, S., Xu, R., & Gonzalez, J. M. (2021). Transcriptome analysis of ovarian follicles reveals potential pivotal genes associated with increased and decreased rates of chicken egg production. Frontiers in Genetics, 12(1), 622751. https://doi.org/10.3389/fgene.2021.622751
Chloupek, P., Voslářová, E., Chloupek, J., Bedáňová, I., Pištěková, V., & Večerek, V. (2009). Stress in broiler chickens due to acute noise exposure. Acta Veterinaria Brno, 78(1), 93–98. https://doi.org/10.2754/avb200978010093
Choudhary, R. K., Kumar B. V., S., Sekhar Mukhopadhyay, C., Kashyap, N., Sharma, V., Singh, N., Salajegheh Tazerji, S., Kalantari, R., Hajipour, P., & Singh Malik, Y. (2024). Animal wellness: the power of multiomics and integrative strategies. Veterinary Medicine International, 2024(1), 4125118. https://doi.org/10.1155/2024/4125118
Clark, B., Stewart, G. B., Panzone, L. A., Kyriazakis, I., & Frewer, L. J. (2016). A systematic review of public attitudes, perceptions and behaviours towards production diseases associated with farm animal welfare. Journal of Agricultural and Environmental Ethics, 29(3), 455–478. https://doi.org/10.1007/s10806-016-9615-x
Cohen, S., & Ho, C. (2023). Review of rat (Rattus norvegicus), mouse (Mus musculus), guinea pig (Cavia porcellus), and rabbit (Oryctolagus cuniculus) indicators for welfare assessment. Animals, 13(13), 2167. https://doi.org/10.3390/ani13132167
Conti, A., & Alessio, M. (2015). Chapter Five - Comparative Proteomics for the Evaluation of Protein Expression and Modifications in Neurodegenerative Diseases. In M. J. Hurley (Ed.), International Review of Neurobiology (Vol. 121, pp. 117–152). Academic Press. https://doi.org/10.1016/bs.irn.2015.05.004
Coskun, O. (2016). Separation techniques: chromatography. Northern Clinics of Istanbul, 3(2), 156. https://doi.org/10.14744/nci.2016.32757
Cuan, K., Zhang, T., Huang, J., Fang, C., & Guan, Y. (2020). Detection of avian influenza-infected chickens based on a chicken sound convolutional neural network. Computers and Electronics in Agriculture, 178, 105688. https://doi.org/10.1016/j.compag.2020.105688
Cuan, K., Zhang, T., Li, Z., Huang, J., Ding, Y., & Fang, C. (2022). Automatic Newcastle disease detection using sound technology and deep learning method. Computers and Electronics in Agriculture, 194, 106740. https://doi.org/10.1016/j.compag.2022.106740
Dai, X., & Shen, L. (2022). Advances and trends in omics technology development. Frontiers in Medicine, 9, 911861. https://doi.org/10.3389/fmed.2022.911861
Daigle, C. L. (2013). Integrating technology and animal welfare: Space and resource use of individual non-cage laying hens. Michigan State University.
Daigle, C. L., Banerjee, D., Montgomery, R. A., Biswas, S., & Siegford, J. M. (2014). Moving GIS research indoors: Spatiotemporal analysis of agricultural animals. PLoS One, 9(8), e104002. https://doi.org/10.1371/journal.pone.0104002
Darwish, I. A. (2006). Immunoassay methods and their applications in pharmaceutical analysis: basic methodology and recent advances. International Journal of Biomedical Science: IJBS, 2(3), 217. https://doi.org/10.59566/IJBS.2006.2217
David, B., Mejdell, C., Michel, V., Lund, V., & Oppermann Moe, R. (2015). Air quality in alternative housing systems may have an impact on laying hen welfare. Part II—Ammonia. Animals, 5(3), 886–896. https://doi.org/10.3390/ani5030368
Dawkins, M. S. (2004). Using behaviour to assess animal welfare. Animal Welfare, 13(S1), S3–S7. https://doi.org/10.1017/S0962728600014317
de Alencar Nääs, I., da Silva Lima, N. D., Gonçalves, R. F., de Lima, L. A., Ungaro, H., & Abe, J. M. (2021). Lameness prediction in broiler chicken using a machine learning technique. Information Processing in Agriculture, 8(3), 409–418. https://doi.org/10.1016/j.inpa.2020.10.003
Decina, C., Berke, O., van Staaveren, N., Baes, C. F., Widowski, T. M., & Harlander-Matauschek, A. (2019). An investigation of associations between management and feather damage in Canadian laying hens housed in furnished cages. Animals, 9(4), 135. https://doi.org/10.3390/ani9040135
Demir, E., Bilginer, U., Balcioglu, M. S., & Karsli, T. (2021). Direct and indirect contributions of molecular genetics to farm animal welfare: a review. Animal Health Research Reviews, 22(2), 177–186. https://doi.org/10.1017/S1466252321000104
Derakhshani, S. M., Overduin, M., van Niekerk, T. G. C. M., & Groot Koerkamp, P. W. G. (2022). Implementation of inertia sensor and machine learning technologies for analyzing the behavior of individual laying hens. Animals, 12(5), 536. https://doi.org/10.3390/ani12050536
Ding, X., Du, J., Zhang, K., Bai, S., Zeng, Q., Peng, H., Xuan, Y., Su, Z., & Wang, J. (2020). Tandem mass tag-based quantitative proteomics analysis and gelling properties in egg albumen of laying hens feeding tea polyphenols. Poultry Science, 99(1), 430–440. https://doi.org/10.3382/ps/pez523
Downing, J. A., & Bryden, W. L. (2008). Determination of corticosterone concentrations in egg albumen: A non-invasive indicator of stress in laying hens. Physiology and Behavior, 95(3). https://doi.org/10.1016/j.physbeh.2008.07.001
EFSA AHAW Panel (EFSA Panel on Animal Health and Animal Welfare), Nielsen, S. S., Alvarez, J., Bicout, D. J., Calistri, P., Canali, E., Drewe, J. A., Garin-Bastuji, B., Gonzales Rojas, J. L., Gortázar Schmidt, C., Herskin, M., Miranda Chueca, M. Á., Padalino, B., Pasquali, P., Roberts, H. C., Spoolder, H., Stahl, K., Velarde, A., Viltrop, A., Winckler, C., Estevez, I., Guinebretière, M., Rodenburg, B., Schrader, L., Tiemann, I., Van Niekerk, T., Ardizzone, M., Ashe, S., Hempen, M., Mosbach-Schulz, O., Gimeno Rojo, C., Van der Stede, Y., Vitali, M., & Michel, V. (2023). Welfare of laying hens on farm. EFSA Journal, 21(2), 7789. https://doi.org/10.2903/j.efsa.2023.7789
El-Sabrout, K., Aggag, S., & Mishra, B. (2022). Advanced practical strategies to enhance table egg production. Scientifica, 2022(1), 1393392. https://doi.org/10.1155/2022/1393392
Erensoy, K., Sarıca, M., Boz, M. A., & Uçar, A. (2021). Health Welfare of Laying Hens Reared in Cage and Non-Cage Systems. International Journal of Poultry-Ornamental Birds Science and Technology, 2(1), 30–35.
Fabrile, M. P., Ghidini, S., Conter, M., Varrà, M. O., Ianieri, A., & Zanardi, E. (2023). Filling gaps in animal welfare assessment through metabolomics. Frontiers in Veterinary Science, 10, 1129741. https://doi.org/10.3389/fvets.2023.1129741
Færgestad, E. M., Langsrud, Ø., Høy, M., Hollung, K., Sæbø, S., Liland, K. H., Kohler, A., Gidskehaug, L., Almergren, J., Anderssen, E., & Martens, H. (2009). 4.08 - Analysis of Megavariate Data in Functional Genomics. In S. D. Brown, R. Tauler, & B. Walczak (Eds.), Comprehensive Chemometrics (pp. 221–278). Elsevier. https://doi.org/10.1016/B978-044452701-1.00011-9
Falker-Gieske, C., Mott, A., Preuß, S., Franzenburg, S., Bessei, W., Bennewitz, J., & Tetens, J. (2020). Analysis of the brain transcriptome in lines of laying hens divergently selected for feather pecking. BMC Genomics, 21, 1–14. https://doi.org/10.1186/s12864-020-07002-1
Ferrante, V. (2009). Welfare issues of modern laying hen farming. Italian Journal of Animal Science, 8(sup1), 175–189. https://doi.org/10.4081/ijas.2009.s1.175
Field, H. P. (2013). Tandem mass spectrometry in hormone measurement. Hormone Assays in Biological Fluids, 1(1065), 45–74. https://doi.org/10.1007/978-1-62703-616-0_4
Filazzola, A., & Cahill Jr, J. F. (2021). Replication in field ecology: Identifying challenges and proposing solutions. Methods in Ecology and Evolution, 12(10), 1780–1792. https://doi.org/10.1111/2041-210X.13657
Fraser, D., & Matthews, L. R. (1997). Preference and motivation testing. In M. C. Appleby & B. O. Hughes (Eds.), Animal Welfare (pp. 159-173). CAB International.
Fritsche, S., Schmidt, G., & Steinhart, H. (1999). Gas chromatographic-mass spectrometric determination of natural profiles of androgens, progestogens, and glucocorticoids in muscle tissue of male cattle. European Food Research and Technology, 209, 393–399. https://doi.org/10.1007/s002170050515
Fujinami, K., Takuno, R., Sato, I., & Shimmura, T. (2023). Evaluating Behavior Recognition Pipeline of Laying Hens Using Wearable Inertial Sensors. Sensors, 23(11), 5077. https://doi.org/10.3390/s23115077
Giloh, M., Shinder, D., & Yahav, S. (2012). Skin surface temperature of broiler chickens is correlated to body core temperature and is indicative of their thermoregulatory status. Poultry Science, 91(1), 175–188. https://doi.org/10.3382/ps.2011-01497
Ginovart-Panisello, G. J., Iriondo, I., Panisello Monjo, T., Riva, S., Cancer, J. C., & Alsina-Pages, R. M. (2024). Acoustic detection of vaccine reactions in hens for assessing anti-inflammatory product efficacy. Applied Sciences, 14(5), 2156. https://doi.org/10.3390/app14052156
González-Salcedo, L. O., Marmolejo-Villanueva, F. A., Quiroz-Morán, D. A., Ospina-Trujillo, K. A., & Malagón-Manrique, R. (2020). Monitoring and Characterization of the Thermal Environment of Special-Use Buildings: Case Study in Pigpens Located in Palmira, Colombia. Ciencia e Ingeniería Neogranadina, 30(2), 81–95. https://doi.org/10.18359/rcin.4435
Grebe, S. K. G., & Singh, R. J. (2011). LC-MS/MS in the clinical laboratory–where to from here? The Clinical Biochemist Reviews, 32(1), 5.
Gržinić, G., Piotrowicz-Cieślak, A., Klimkowicz-Pawlas, A., Górny, R. L., Ławniczek-Wałczyk, A., Piechowicz, L., Olkowska, E., Potrykus, M., Tankiewicz, M., & Krupka, M. (2023). Intensive poultry farming: A review of the impact on the environment and human health. Science of the Total Environment, 858(3), 160014. https://doi.org/10.1016/j.scitotenv.2022.160014
Guerrero-Bosagna, C., Pértille, F., Gomez, Y., Rezaei, S., Gebhardt-Henrich, S. G., Vögeli, S., Stratmann, A., Voelkl, B., & Toscano, M. J. (2020). DNA methylation variation in the brain of laying hens in relation to differential behavioral patterns. Comparative Biochemistry and Physiology Part D: Genomics and Proteomics, 35, 100700. https://doi.org/10.1016/j.cbd.2020.100700
Guevara, R. D., Pastor, J. J., Manteca, X., Tedo, G., & Llonch, P. (2022). Systematic review of animal-based indicators to measure thermal, social, and immune-related stress in pigs. PloS One, 17(5), e0266524. https://doi.org/10.1371/journal.pone.0266524
Hackney, A. C. (2018). Chapter 10 - Athlete Testing, Analytical Procedures, and Adverse Analytical Findings. In A. C. Hackney (Ed.), Doping, Performance Enhancing Drugs, and Hormones in Sport (pp. 113–127). Elsevier. https://doi.org/10.1016/B978-0-12-813442-9.00010-9
Häffelin, K. E., Lindenwald, R., Kaufmann, F., Döhring, S., Spindler, B., Preisinger, R., Rautenschlein, S., Kemper, N., & Andersson, R. (2020). Corticosterone in feathers of laying hens: an assay validation for evidence-based assessment of animal welfare. Poultry Science, 99(10), 4685–4694. https://doi.org/10.1016/j.psj.2020.06.065
Häffelin, K. E., Kaufmann, F., Lindenwald, R., Döhring, S., Spindler, B., Preisinger, R., Rautenschlein, S., Kemper, N., & Andersson, R. (2021). Corticosterone in feathers: Inter-and intraindividual variation in pullets and the importance of the feather type. Veterinary and Animal Science, 11, 100155. https://doi.org/10.1016/j.vas.2020.100155
Harikrishnan, V. S. (2021). Laboratory Animal Behaviour and Its Applications in Biomedical Research. Essentials of Laboratory Animal Science: Principles and Practices, 479–495. https://doi.org/10.1007/978-981-16-0987-9_19
Hartmann, S., Lacorn, M., & Steinhart, H. (1998). Natural occurrence of steroid hormones in food. Food Chemistry, 62(1), 7–20. https://doi.org/10.1016/S0308-8146(97)00150-7
Hell, J., Kneifel, W., Rosenau, T., & Böhmdorfer, S. (2014). Analytical techniques for the elucidation of wheat bran constituents and their structural features with emphasis on dietary fiber–A review. Trends in Food Science & Technology, 35(2), 102–113. https://doi.org/10.1016/j.tifs.2013.10.012
Hemathilake, D., & Gunathilake, D. (2022). Chapter 31 - Agricultural productivity and food supply to meet increased demands. In R. Bhat (Ed.), Future foods (pp. 539–553). Elsevier. https://doi.org/10.1016/B978-0-323-91001-9.00016-5
Hemsworth, P. H., & Edwards, L. E. (2020). Natural behaviours, their drivers and their implications for laying hen welfare. Animal Production Science, 61(10), 915–930. https://doi.org/10.1071/AN19630
Herrera-Sánchez, M. P., Lozano-Villegas, K. J., Rondón-Barragán, I. S., & Rodríguez-Hernández, R. (2023). Identification of reference genes for expression studies in the liver and spleen of laying hens housed in cage and cage-free systems. Open Veterinary Journal, 13(3), 270–277. https://doi.org/10.5455/OVJ.2023.v13.i3.3
Herrera-Sánchez, M. P., Rodríguez-Hernández, R., & Rondón-Barragán, I. S. (2024). Stress‐Related Gene Expression in Liver Tissues from Laying Hens Housed in Conventional Cage and Cage‐Free Systems in the Tropics. Veterinary Medicine International, 2024(1), 4107326. https://doi.org/10.1155/2024/4107326
Herrera-Sánchez, M. P., Rodríguez-Hernández, R., & Rondón-Barragán, I. S. (2025). Comparative Transcriptome Analysis of Hens’ Livers in Conventional Cage vs. Cage-Free Egg Production Systems. Veterinary Medicine International, 2025(1), 3041254. https://doi.org/10.1155/vmi/3041254
Hiller-Sturmhöfel, S., & Bartke, A. (1998). The endocrine system: an overview. Alcohol Health and Research World, 22(3), 153.
Huang, X., Zhang, H., Cao, H., Zhou, W., Xiang, X., & Yin, Z. (2022). Transcriptomics and metabolomics analysis of the ovaries of high and low egg production chickens. Animals, 12(16), 2010. https://doi.org/10.3390/ani12162010
Ibeagha-Awemu, E. M., & Yu, Y. (2021). Consequence of epigenetic processes on animal health and productivity: is additional level of regulation of relevance? Animal Frontiers, 11(6), 7–18. https://doi.org/10.1093/af/vfab057
James, K. A., Stromin, J. I., Steenkamp, N., & Combrinck, M. I. (2023). Understanding the relationships between physiological and psychosocial stress, cortisol and cognition. Frontiers in Endocrinology, 14, 1085950. https://doi.org/10.3389/fendo.2023.1085950
Ji, B., Zheng, W., Gates, R. S., & Green, A. R. (2016). Design and performance evaluation of the upgraded portable monitoring unit for air quality in animal housing. Computers and Electronics in Agriculture, 124, 132–140. https://doi.org/10.1016/j.compag.2016.03.030
Ji, Y., Mingxia, S., Longshen, L. I. U., Mingzhou, L. U., Canlong, H. E., & Jiawei, L. I. (2018). Research of detection method for broiler chicken feed intake based on audio technology. Journal of South China Agricultural University, 39(5), 118–124.
Jones, R. B. (1996). Fear and adaptability in poultry: insights, implications and imperatives. World’s Poultry Science Journal, 52(2), 131–174. https://doi.org/10.1079/WPS19960013
Kang, D. R., & Shim, K. S. (2020). Proteomic Analysis of the Protective Effect of Early Heat Exposure against Chronic Heat Stress in Broilers. Animals 2020, Vol. 10, Page 2365, 10(12), 2365. https://doi.org/10.3390/ani10122365
Kasper, C., Ribeiro, D., Almeida, A. M. de, Larzul, C., Liaubet, L., & Murani, E. (2020). Omics application in animal science—a special emphasis on stress response and damaging behaviour in pigs. Genes, 11(8), 920. https://doi.org/10.3390/genes11080920
Khullar, D., & Jena, A. B. (2021). “Natural Experiments” in health care research. JAMA Health Forum, 2(6), e210290–e210290. https://doi.org/10.1001/jamahealthforum.2021.0290
Kim, D. H., Lee, Y. K., Lee, S. D., Kim, S. H., & Lee, K. W. (2021a). Physiological and behavioral responses of laying hens exposed to long-term high temperature. Journal of Thermal Biology, 99, 103017. https://doi.org/10.1016/j.jtherbio.2021.103017
Kim, N. Y., Kim, S. J., Oh, M., Jang, S. Y., & Moon, S. H. (2021b). Changes in facial surface temperature of laying hens under different thermal conditions. Animal Bioscience, 34(7), 1235. https://doi.org/10.5713/ab.20.0647
Kinn Rød, A. M., Harkestad, N., Jellestad, F. K., & Murison, R. (2017). Comparison of commercial ELISA assays for quantification of corticosterone in serum. Scientific Reports, 7(1), 6748. https://doi.org/10.1038/s41598-017-06006-4
Klee, G. G. (2003). Laboratory techniques for recognition of endocrine disorders. Williams Textbook of Endocrinology, 67–81.
Koknaroglu, H., & Akunal, T. (2013). Animal welfare: An animal science approach. Meat Science, 95(4), 821–827. https://doi.org/10.1016/j.meatsci.2013.04.030
Kokocińska, A., & Kaleta, T. (2016). The role of ethology in animal welfare. System, 27, 39. https://doi.org/10.5604/01.3001.0013.6981
Lamping, C., Derks, M., Koerkamp, P. G., & Kootstra, G. (2022). ChickenNet-an end-to-end approach for plumage condition assessment of laying hens in commercial farms using computer vision. Computers and Electronics in Agriculture, 194, 106695. https://doi.org/10.1016/j.compag.2022.106695
Lay Jr, D. C., Fulton, R. M., Hester, P. Y., Karcher, D. M., Kjaer, J. B., Mench, J. A., Mullens, B. A., Newberry, R. C., Nicol, C. J., & O’Sullivan, N. P. (2011). Hen welfare in different housing systems. Poultry Science, 90(1), 278–294. https://doi.org/10.3382/ps.2010-00962
Lee, H. M., Kim, K. S., & Lee, J. G. (2003). Investigation of abnormal eggs and cortisol stress hormone in laying hens due to the artificial noise. Journal of Korean Society of Environmental Engineers, 25(7), 13–860.
Lee, H., Roberts, S. J., Drake, K. A., & Dawkins, M. S. (2011). Prediction of feather damage in laying hens using optical flows and Markov models. Journal of the Royal Society Interface, 8(57), 489–499. https://doi.org/10.1098/rsif.2010.0268
Lee, D., Lee, H. J., Jung, D. Y., Kim, H. J., Jang, A., & Jo, C. (2022). Effect of an animal-friendly raising environment on the quality, storage stability, and metabolomic profiles of chicken thigh meat. Food Research International, 155. https://doi.org/10.1016/j.foodres.2022.111046
Lee, N., Sharma, M. K., Paneru, D., Ward, E. D., Kim, W. K., & Suh, J. H. (2024). Metabolomic analysis reveals altered amino acid metabolism and mechanisms underlying Eimeria infection in laying hens. Poultry Science, 103(11), 104244. https://doi.org/10.1016/j.psj.2024.104244
Leroy, T., Vranken, E., Van Brecht, A., Struelens, E., Sonck, B., & Berckmans, D. (2006). A computer vision method for on-line behavioral quantification of individually caged poultry. Transactions of the ASABE, 49(3), 795–802. https://doi.org/10.13031/2013.20462
Lewis, A., Douka, D., Koukoura, A., Valla, V., Smirthwaite, A., Faarbaek, S. H., & Vassiliadis, E. (2022). Preference testing in medical devices: current framework and regulatory gaps. Medical Devices: Evidence and Research, 199–213. https://doi.org/10.2147/MDER.S368420
Li, C., Wang, X., Wang, G., Li, N., & Wu, C. (2011). Expression analysis of global gene response to chronic heat exposure in broiler chickens (Gallus gallus) reveals new reactive genes. Poultry Science, 90(5), 1028–1036. https://doi.org/10.3382/ps.2010-01144
Li, H., Wang, T., Xu, C., Wang, D., Ren, J., Li, Y., Tian, Y., Wang, Y., Jiao, Y., & Kang, X. (2015). Transcriptome profile of liver at different physiological stages reveals potential mode for lipid metabolism in laying hens. BMC Genomics, 16, 1–13. https://doi.org/10.1186/s12864-015-1943-0
Li, I., Yang, W., Chou, C., Chen, Y., Kuo, S., & Wang, S. (2019). Analysis of steroid hormones in shell eggs from layer breeds common to Taiwan by liquid chromatography–tandem mass spectrometry. Food Science & Nutrition, 7(7), 2319–2326. https://doi.org/10.1002/fsn3.1074
Li, D., Tong, Q., Shi, Z., Li, H., Wang, Y., Li, B., Yan, G., Chen, H., & Zheng, W. (2020a). Effects of chronic heat stress and ammonia concentration on blood parameters of laying hens. Poultry Science, 99(8), 3784–3792. https://doi.org/10.1016/j.psj.2020.03.060
Li, N., Ren, Z., Li, D., & Zeng, L. (2020b). Review: Automated techniques for monitoring the behaviour and welfare of broilers and laying hens: towards the goal of precision livestock farming. Animal, 14(3), 617-625. https://doi.org/10.1017/S1751731119002155
Li, B., Wang, Y., Rong, L., & Zheng, W. (2023a). Research progress on animal environment and welfare. Animal Research and One Health, 1(1), 78–91. https://doi.org/10.1002/aro2.16
Li, D., Wu, Y., Shi, K., Shao, M., Duan, Y., Yu, M., & Feng, C. (2023b). Untargeted metabolomics reveals the effect of rearing systems on bone quality parameters in chickens. Frontiers in Genetics, 13, 1071562. https://doi.org/10.3389/fgene.2022.1071562
Liang, R. C. M. Y., Neo, J. C. H., Ling Lo, S., San Tan, G., Keong Seow, T., & Chung, M. C. M. (2002). Proteome database of hepatocellular carcinoma. Journal of Chromatography B, 771(1), 303–328. https://doi.org/10.1016/S1570-0232(02)00041-7
Liang, Q., Huan, S., Lin, Y., Su, Z., Yao, X., Li, C., Ji, Z., & Zhang, X. (2024). Screening of heat stress-related biomarkers in chicken serum through label-free quantitative proteomics. Poultry Science, 103(2), 103340. https://doi.org/10.1016/j.psj.2023.103340
Long, J. A. (2020). The ‘omics’ revolution: Use of genomic, transcriptomic, proteomic and metabolomic tools to predict male reproductive traits that impact fertility in livestock and poultry. Animal Reproduction Science, 220, 106354. https://doi.org/10.1016/j.anireprosci.2020.106354
Lutz, V., Stratz, P., Preuß, S., Tetens, J., Grashorn, M. A., Bessei, W., & Bennewitz, J. (2017). A genome-wide association study in a large F2-cross of laying hens reveals novel genomic regions associated with feather pecking and aggressive pecking behavior. Genetics Selection Evolution, 49, 1–11. https://doi.org/10.1186/s12711-017-0287-4
Madzingira, O. (2018). Animal welfare considerations in food-producing animals. In M. Abubakar & S. Manzoor (Eds.), Animal welfare. IntechOpen. https://doi.org/10.5772/intechopen.78223
Mahdavian, A., Minaei, S., Marchetto, P. M., Almasganj, F., Rahimi, S., & Yang, C. (2021). Acoustic features of vocalization signal in poultry health monitoring. Applied Acoustics, 175, 107756. https://doi.org/10.1016/j.apacoust.2020.107756
Main, D. C. J., Mullan, S., Atkinson, C., Bond, A., Cooper, M., Fraser, A., & Browne, W. J. (2012). Welfare outcomes assessment in laying hen farm assurance schemes. Animal Welfare, 21(3), 389–396. https://doi.org/10.7120/09627286.21.3.389
Malott, R. W., & Kohler, K. T. (2021). Principles of behavior. Routledge. https://doi.org/10.4324/9781003157014
Mann, M., & Jensen, O. N. (2003). Proteomic analysis of post-translational modifications. Nature Biotechnology, 21(3), 255–261. https://doi.org/10.1038/nbt0303-255
Mashaly, M. M., Hendricks 3rd, G. L., Kalama, M. A., Gehad, A. E., Abbas, A. O., & Patterson, P. H. (2004). Effect of heat stress on production parameters and immune responses of commercial laying hens. Poultry Science, 83(6), 889–894. https://doi.org/10.1093/ps/83.6.889
McDonald, J. G., Matthew, S., & Auchus, R. J. (2011a). Steroid profiling by gas chromatography–mass spectrometry and high performance liquid chromatography–mass spectrometry for adrenal diseases. Hormones and Cancer, 2, 324–332. https://doi.org/10.1007/s12672-011-0099-x
Morgado, J. N., Santeramo, F., Lamonaca, E., Ciliberti, M. G., & Caroprese, M. (2022). Meta‐analysis and systematic literature review of climate change effects on livestock welfare. EFSA Journal, 20, e200413. https://doi.org/10.2903/j.efsa.2022.e200413
Mottet, A., & Tempio, G. (2017). Global poultry production: current state and future outlook and challenges. World’s Poultry Science Journal, 73(2), 245–256. https://doi.org/10.1017/S0043933917000071
Muir, W. M., Cheng, H.-W., & Croney, C. (2014). Methods to address poultry robustness and welfare issues through breeding and associated ethical considerations. Frontiers in Genetics, 5, 111722. https://doi.org/10.3389/fgene.2014.00407
Nakarmi, A. D., Tang, L., & Xin, H. (2014). Automated tracking and behavior quantification of laying hens using 3D computer vision and radio frequency identification technologies. Transactions of the ASABE, 57(5), 1455–1472. https://doi.org/10.13031/trans.57.10505
Nardone, A., Ronchi, B., Lacetera, N., Ranieri, M. S., & Bernabucci, U. (2010). Effects of climate changes on animal production and sustainability of livestock systems. Livestock Science, 130(1–3), 57–69. https://doi.org/10.1016/j.livsci.2010.02.011
National Research Council (US) Committee on Recognition and Alleviation of Distress in Laboratory Animals. (2008). Recognition and alleviation of distress in laboratory animals. National Academies Press. https://www.ncbi.nlm.nih.gov/books/NBK4032
Neethirajan, S. (2025). Rethinking poultry welfare—integrating behavioral science and digital innovations for enhanced animal well-being. Poultry, 4(2), 20. https://doi.org/10.3390/poultry4020020
Nery da Silva, A., Silva Araujo, M., Pértille, F., & Zanella, A. J. (2021). How epigenetics can enhance pig welfare? Animals, 12(1), 32. https://doi.org/10.3390/ani12010032
Nguyen, N. H. (2024). Genetics and Genomics of Infectious Diseases in Key Aquaculture Species. Biology, 13(1), 29. https://doi.org/10.3390/biology13010029
Nicol, C. (2023). The Gordon Memorial Lecture: Laying hen welfare. British Poultry Science, 64(4), 441–447. https://doi.org/10.1080/00071668.2023.2211891
Niessen, W. M. A. (2001). Current practice of gas chromatography-mass spectrometry. CRC Press. https://doi.org/10.1201/9780367801274
Nielsen, S. S., Alvarez, J., Bicout, D. J., Calistri, P., Canali, E., Drewe, J. A., Garin-Bastuji, B., Gonzales Rojas, J. L., Gortázar Schmidt, C., Herskin, M., Miranda Chueca, M. Á., Padalino, B., Pasquali, P., Roberts, H. C., Spoolder, H., Stahl, K., Velarde, A., Viltrop, A., … Michel, V. (2023). Welfare of laying hens on farm. EFSA Journal, 21(2), e07789. https://doi.org/10.2903/j.efsa.2023.7789
Nouri, M.-Z., Kroll, K. J., Webb, M., & Denslow, N. D. (2020). Quantification of steroid hormones in low volume plasma and tissue homogenates of fish using LC-MS/MS. General and Comparative Endocrinology, 296, 113543. https://doi.org/10.1016/j.ygcen.2020.113543
Nwaigwe, C. U., Ihedioha, J. I., Shoyinka, S. V., & Nwaigwe, C. O. (2020). Evaluation of the hematological and clinical biochemical markers of stress in broiler chickens. Veterinary World, 13(10). https://doi.org/10.14202/vetworld.2020.2294-2300
Oke, O. E., Akosile, O. A., Oni, A. I., Opowoye, I. O., Ishola, C. A., Adebiyi, J. O., Odeyemi, A. J., Adjei-Mensah, B., Uyanga, V. A., & Abioja, M. O. (2024). Oxidative stress in poultry production. Poultry Science, 103(9). https://doi.org/10.1016/j.psj.2024.104003
Okinda, C., Nyalala, I., Korohou, T., Okinda, C., Wang, J., Achieng, T., Wamalwa, P., Mang, T., & Shen, M. (2020). A review on computer vision systems in monitoring of poultry: A welfare perspective. Artificial Intelligence in Agriculture, (4), 184-208. https://doi.org/10.1016/j.aiia.2020.09.002
Oluwagbenga, E. M., Tetel, V., Schober, J., & Fraley, G. S. (2022). Chronic heat stress part 1: Decrease in egg quality, increase in cortisol levels in egg albumen, and reduction in fertility of breeder pekin ducks. Frontiers in Physiology, 13, 1019741. https://doi.org/10.3389/fphys.2022.1019741
Orihuela, A. (2021). Management of livestock behavior to improve welfare and production. Animal, 15, 100290. https://doi.org/10.1016/j.animal.2021.100290
Ouyang, J. Q., Macaballug, P., Chen, H., Hodach, K., Tang, S., & Francis, J. S. (2021). Infrared thermography is an effective, noninvasive measure of HPA activation. Stress, 24(5). https://doi.org/10.1080/10253890.2020.1868431
Paneru, B., Bist, R., Yang, X., & Chai, L. (2024). Tracking dustbathing behavior of cage-free laying hens with machine vision technologies. Poultry Science, 103(12), 104289. https://doi.org/10.1016/j.psj.2024.104289
Patti, G. J., Yanes, O., & Siuzdak, G. (2012). Metabolomics: the apogee of the omics trilogy. Nature Reviews Molecular Cell Biology, 13(4), 263–269. https://doi.org/10.1038/nrm3314
Pereira, E. M., Nääs, I. de A., & Garcia, R. G. (2014). Identification of acoustic parameters for broiler welfare estimate. Engenharia Agrícola, 34, 413–421. https://doi.org/10.1590/S0100-69162014000300004
Pértille, F., Ibelli, A. M. G., Sharif, M. El, Poleti, M. D., Fröhlich, A. S., Rezaei, S., Ledur, M. C., Jensen, P., Guerrero-Bosagna, C., & Coutinho, L. L. (2020). Putative Epigenetic Biomarkers of Stress in Red Blood Cells of Chickens Reared Across Different Biomes. Frontiers in Genetics, 11. https://doi.org/10.3389/fgene.2020.508809
Pia Franciosini, M., Canali, C., Casagrande Proietti, P., Tarhuni, O., Fringuelli, E., & Asdrubali, G. (2005). Plasma corticosterone levels in laying hens from three different housing systems: preliminary results. Italian Journal of Animal Science, 4(3), 276–278. https://doi.org/10.4081/ijas.2005.276
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. https://doi.org/10.1017/S1751731116001981
Pisula, W. (1999). Dobrostan zwierzat uzytkowych-wybrane zagadnienia psychologii zwierzat. Przegląd Hodowlany, 67(01), 1–3.
Prastiya, R. A., Madyawati, S. P., Sari, S. Y., & Nugroho, A. P. (2022). Effect of follicle-stimulating hormone and luteinizing hormone levels on egg-laying frequency in hens. Veterinary World, 15(12), 2890. https://doi.org/10.14202/vetworld.2022.2890-2895
Prokai-Tatrai, K., Bonds, D., & Prokai, L. (2010). Simultaneous measurement of 17β-estradiol, 17α-estradiol and estrone by GC–isotope dilution MS–MS. Chromatographia, 71, 311–315. https://doi.org/10.1365/s10337-009-1441-0
Rana, M. S., Lee, C., Lea, J. M., & Campbell, D. L. M. (2022). Commercial free-range laying hens’ preferences for shelters with different sunlight filtering percentages. Animals, 12(3), 344. https://doi.org/10.3390/ani12030344
Rettenbacher, S., Möstl, E., Hackl, R., Ghareeb, K., & Palme, R. (2004). Measurement of corticosterone metabolites in chicken droppings. British Poultry Science, 45(5), 704-711. https://doi.org/10.1080/00071660400006156
Rodríguez-Hernández, R., Oviedo-Rondón, E. O., & Rondón-Barragán, I. S. (2021). Identification of reliable reference genes for expression studies in the magnum of laying hens housed in cage and cage-free systems. Veterinary Medicine and Science, 7(5). https://doi.org/10.1002/vms3.507
Rodríguez-Hernández, R., Rondón-Barragán, I. S., & Oviedo-Rondón, E. O. (2024). Egg Quality, Yolk Fatty Acid Profiles from Laying Hens Housed in Conventional Cage and Cage-Free Production Systems in the Andean Tropics. Animals, 14(1). https://doi.org/10.3390/ani14010168
Royo, F., Mayo, S., Carlsson, H.-E., & Hau, J. (2008). Egg corticosterone: a noninvasive measure of stress in egg-laying birds. Journal of Avian Medicine and Surgery, 22(4) 310–314 https://doi.org/10.1647/2008-001.1
Sadeghi, E., Kappers, C., Chiumento, A., Derks, M., & Havinga, P. (2023). Improving piglets health and well-being: A review of piglets health indicators and related sensing technologies. Smart Agricultural Technology, 5(1) 100246. https://doi.org/10.1016/j.atech.2023.100246
Sas, B., Domány, G., Gyimóthy, I., Gaál Kovácsné, K., & Süth, M. (2006). Influence of the type of management system on corticosterone transfer into eggs in laying hens. Acta Veterinaria Hungarica, 54(3), 343–352. https://doi.org/10.1556/avet.54.2006.3.5
Satam, H., Joshi, K., Mangrolia, U., Waghoo, S., Zaidi, G., Rawool, S., Thakare, R. P., Banday, S., Mishra, A. K., & Das, G. (2023). Next-generation sequencing technology: current trends and advancements. Biology, 12(7), 997. https://doi.org/10.3390/biology12070997
Scanes, C. G. (2016). Biology of stress in poultry with emphasis on glucocorticoids and the heterophil to lymphocyte ratio. Poultry Science, 95(9), 2208-2215. https://doi.org/10.3382/ps/pew137
Schmid, B., Chastel, O., & Jenni, L. (2011). The prolactin response to an acute stressor in relation to parental care and corticosterone in a short-lived bird, the Eurasian hoopoe. General and Comparative Endocrinology, 174(1), 22–29. https://doi.org/10.1016/j.ygcen.2011.07.012
Schreiter, R., & Freick, M. (2022). Research Note: Is infrared thermography an appropriate method for early detection and objective quantification of plumage damage in white and brown feathered laying hens? Poultry Science, 101(9), 102022. https://doi.org/10.1016/j.psj.2022.102022
Serra, M., Wolkers, C. P. B., & Urbinati, E. C. (2018). Physiological indicators of animal welfare. Revista Brasileira de Zoociências, 19(2). https://doi.org/10.34019/2596-3325.2018.v19.24726
Shahbazi, M., Mohammadi, K., Derakhshani, S. M., & Groot Koerkamp, P. W. G. (2023). Deep learning for laying hen activity recognition using wearable sensors. Agriculture, 13(3), 738. https://doi.org/10.3390/agriculture13030738
Shen, X., Bai, X., Luo, C., Jiang, D., Li, X., Zhang, X., Yunbo, T., & Huang, Y. (2021). Quantitative proteomic analysis of chicken serum reveals key proteins affecting follicle development during reproductive phase transitions. Poultry Science, 100(1), 325–333. https://doi.org/10.1016/j.psj.2020.09.058
Siegford, J. M., Berezowski, J., Biswas, S. K., Daigle, C. L., Gebhardt-Henrich, S. G., Hernandez, C. E., Thurner, S., & Toscano, M. J. (2016). Assessing activity and location of individual laying hens in large groups using modern technology. Animals, 6(2), 10. https://doi.org/10.3390/ani6020010
Sitzenstock, F., Ytournel, F., Sharifi, A. R., Cavero, D., Täubert, H., Preisinger, R., & Simianer, H. (2013). Efficiency of genomic selection in an established commercial layer breeding program. Genetics Selection Evolution, 45, 1–11. https://doi.org/10.1186/1297-9686-45-29
Skånberg, L., Nielsen, C. B. K., & Keeling, L. J. (2021). Litter and perch type matter already from the start: exploring preferences and perch balance in laying hen chicks. Poultry Science, 100(2), 431–440. https://doi.org/10.1016/j.psj.2020.11.041
Skerrett-Byrne Anthony, D., Jiang Chen, C., Nixon, B., & Hondermarck, H. (2023). Transcriptomics. In R. A. Bradshaw, G. W. Hart, & P. D. Stahl (Eds.), Encyclopedia of Cell Biology (2nd Edition) (pp. 363–371). Academic Press. https://doi.org/10.1016/B978-0-12-821618-7.00157-7
Sozzi, M., Pillan, G., Ciarelli, C., Marinello, F., Pirrone, F., Bordignon, F., Bordignon, A., Xiccato, G., & Trocino, A. (2023). Measuring Comfort Behaviours in Laying Hens Using Deep-Learning Tools. Animals, 13(1). https://doi.org/10.3390/ani13010033
Stan, H.-J. (2005). GC-MS. I: Basic principles and technical aspects of GC-MS for pesticide residue analysis. In Comprehensive Analytical Chemistry (Vol. 43, pp. 269–337). Elsevier. https://doi.org/10.1016/S0166-526X(05)80026-1
Stanczyk, F. Z., & Clarke, N. J. (2010). Advantages and challenges of mass spectrometry assays for steroid hormones. The Journal of Steroid Biochemistry and Molecular Biology, 121(3–5), 491–495. https://doi.org/10.1016/j.jsbmb.2010.05.001
Steckl, A. J., & Ray, P. (2018). Stress biomarkers in biological fluids and their point-of-use detection. ACS Sensors, 3(10), 2025–2044. https://doi.org/10.1021/acssensors.8b00726
Steiger, H., & Thaler, L. (2016). Eating disorders, gene-environment interactions and the epigenome: Roles of stress exposures and nutritional status. Physiology & Behavior, 162, 181–185. https://doi.org/10.1016/j.physbeh.2016.01.041
Subedi, S., Bist, R., Yang, X., & Chai, L. (2023). Tracking pecking behaviors and damages of cage-free laying hens with machine vision technologies. Computers and Electronics in Agriculture, 204. https://doi.org/10.1016/j.compag.2022.107545
Sun, J., & Xia, Y. (2023). Pretreating and normalizing metabolomics data for statistical analysis. Genes & Diseases. https://doi.org/10.1016/j.gendis.2023.04.018
Suravajhala, P., Kogelman, L. J. A., & Kadarmideen, H. N. (2016). Multi-omic data integration and analysis using systems genomics approaches: methods and applications in animal production, health and welfare. Genetics Selection Evolution, 48, 1–14. https://doi.org/10.1186/s12711-016-0217-x
Taborda-Charris, J. C., Rodríguez-Hernández, R., Herrera-Sánchez, M. P., Uribe-García, H. F., Otero-Arroyo, R. J., Naranjo-Gomez, J. S., Lozano-Villegas, K. J., & Rondón-Barragán, I. S. (2023). Expression profiling of heat shock protein genes in whole blood of Romosinuano cattle breed. Veterinary World, 16(3). https://doi.org/10.14202/vetworld.2023.601-606
Tahamtani, F. M., Hansen, T. B., Orritt, R., Nicol, C., Moe, R. O., & Janczak, A. M. (2014). Does rearing laying hens in aviaries adversely affect long-term welfare following transfer to furnished cages? PLoS One, 9(9), e107357. https://doi.org/10.1371/journal.pone.0107357
Tainika, B., & Şekeroğlu, A. (2021). Environmental enrichments in laying hen production systems with emphasis on welfare and egg quality. Turkish Journal of Agriculture-Food Science and Technology, 9(8), 1398–1406. https://doi.org/10.24925/turjaf.v9i8.1398-1406.4240
Talbot, R. T., & Sharp, P. J. (1994). A radioimmunoassay for recombinant-derived chicken prolactin suitable for the measurement of prolactin in other avian species. General and Comparative Endocrinology, 96(3), 361–369. https://doi.org/10.1006/gcen.1994.1191
Tattersall, G. J. (2016). Infrared thermography: A non-invasive window into thermal physiology. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 202, 78–98. https://doi.org/10.1016/j.cbpa.2016.02.022
Temple, D., Manteca, X., Escribano, D., Salas, M., Mainau, E., Zschiesche, E., Petersen, I., Dolz, R., & Thomas, E. (2020). Assessment of laying-bird welfare following acaricidal treatment of a commercial flock naturally infested with the poultry red mite (Dermanyssus gallinae). Plos One, 15(11), e0241608. https://doi.org/10.1371/journal.pone.0241608
Thomann, B., Würbel, H., Kuntzer, T., Umstätter, C., Wechsler, B., Meylan, M., & Schüpbach-Regula, G. (2023). Development of a data-driven method for assessing health and welfare in the most common livestock species in Switzerland: The Smart Animal Health project. Frontiers in Veterinary Science, 10, 1125806. https://doi.org/10.3389/fvets.2023.1125806
Tian, W., Wang, L., Lei, H., Sun, Y., & Xiao, Z. (2018). Antibody production and application for immunoassay development of environmental hormones: A review. Chemical and Biological Technologies in Agriculture, 5, 1–12. https://doi.org/10.1186/s40538-018-0117-0
Tilbrook, A. J., & Fisher, A. D. (2020). Stress, health and the welfare of laying hens. Animal Production Science, 61(10), 931–943. https://doi.org/10.1071/AN19666
Tolani, P., Gupta, S., Yadav, K., Aggarwal, S., & Yadav, A. K. (2021). Chapter Four - Big data, integrative omics and network biology. In R. Donev & T. Karabencheva-Christova (Eds.), Advances in protein chemistry and structural biology (Vol. 127, pp. 127–160). Academic Press. https://doi.org/10.1016/bs.apcsb.2021.03.006
Travain, T., & Valsecchi, P. (2021). Infrared thermography in the study of animals’ emotional responses: A critical review. Animals, 11(9), 2510. https://doi.org/10.3390/ani11092510
Turner, J. T., Whittaker, A., McLelland, D., & Fernandez, E. (2023). Preference Tests in Applied Animal Settings: A Systematic Scoping Review Protocol. https://doi.org/10.31219/osf.io/kg6au
Uffelmann, E., Huang, Q. Q., Munung, N. S., de Vries, J., Okada, Y., Martin, A. R., Martin, H. C., Lappalainen, T., & Posthuma, D. (2021). Genome-wide association studies. Nature Reviews Methods Primers, 1(1), 59. https://doi.org/10.1038/s43586-021-00056-9
van den Heuvel, H., Youssef, A., Grat, L. M., & Neethirajan, S. (2022). Quantifying the effect of an acute stressor in laying hens using thermographic imaging and vocalisations. BioRxiv, 2022–2027. https://doi.org/10.1101/2022.07.31.502171
van Veen, L. A., van den Oever, A. C. M., Kemp, B., & van den Brand, H. (2023). Perception of laying hen farmers, poultry veterinarians, and poultry experts regarding sensor-based continuous monitoring of laying hen health and welfare. Poultry Science, 102(5), 102581. https://doi.org/10.1016/j.psj.2023.102581
Von Borell, E., Langbein, J., Després, G., Hansen, S., Leterrier, C., Marchant, J., Marchant-Forde, R., Minero, M., Mohr, E., & Prunier, A. (2007). Heart rate variability as a measure of autonomic regulation of cardiac activity for assessing stress and welfare in farm animals—A review. Physiology & Behavior, 92(3), 293–316. https://doi.org/10.1016/j.physbeh.2007.01.007
Wang, Z., Gerstein, M., & Snyder, M. (2009). RNA-Seq: a revolutionary tool for transcriptomics. Nature Reviews Genetics, 10(1), 57–63. https://doi.org/10.1038/nrg2484
Wang, X. J., Liu, L., Zhao, J. P., Jiao, H. C., & Lin, H. (2017). Stress impairs the reproduction of laying hens: an involvement of energy. World’s Poultry Science Journal, 73(4), 845–856. https://doi.org/10.1017/S0043933917000794
Wang, C., & Ma, W. (2019). Hypothalamic and pituitary transcriptome profiling using RNA-sequencing in high-yielding and low-yielding laying hens. Scientific Reports, 9(1), 10285. https://doi.org/10.1038/s41598-019-46807-3
Wang, Y., Jia, X., Hsieh, J. C. F., Monson, M. S., Zhang, J., Shu, D., Nie, Q., Persia, M. E., Rothschild, M. F., & Lamont, S. J. (2021). Transcriptome response of liver and muscle in heat-stressed laying hens. Genes, 12(2), 255. https://doi.org/10.3390/genes12020255
Wang, J., Liu, L., Lu, M., Okinda, C., Lovarelli, D., Guarino, M., & Shen, M. (2022). The estimation of broiler respiration rate based on the semantic segmentation and video amplification. Frontiers in Physics, 10, 1047077. https://doi.org/10.3389/fphy.2022.1047077
Wascher, C. A. F. (2021). Heart rate as a measure of emotional arousal in evolutionary biology. Philosophical Transactions of the Royal Society B, 376, 20200479.. https://doi.org/10.1098/rstb.2020.0479
Watters, J. V, Krebs, B. L., & Eschmann, C. L. (2021). Assessing animal welfare with behavior: Onward with caution. Journal of Zoological and Botanical Gardens, 2(1), 75–87. https://doi.org/10.3390/jzbg2010006
Weeks, C. A., & Nicol, C. J. (2006). Behavioural needs, priorities and preferences of laying hens. World’s Poultry Science Journal, 62(2), 296–307. https://doi.org/10.1079/WPS200598
Welch, M., Sibanda, T. Z., De Souza Vilela, J., Kolakshyapati, M., Schneider, D., & Ruhnke, I. (2023). An initial study on the use of machine learning and radio frequency identification data for predicting health outcomes in free-range laying hens. Animals, 13(7), 1202. https://doi.org/10.3390/ani13071202
Whelan, R., Tönges, S., Böhl, F., & Lyko, F. (2023). Epigenetic biomarkers for animal welfare monitoring. Frontiers in Veterinary Science, 9, 1107843. https://doi.org/10.3389/fvets.2022.1107843
Wu, C.-T., & Morris, J. R. (2001). Genes, genetics, and epigenetics: a correspondence. Science, 293(5532), 1103–1105. https://doi.org/10.1126/science.293.5532.1103
Yan, L., Hu, M., Gu, L., Lei, M., Chen, Z., Zhu, H., & Chen, R. (2022). Effect of heat stress on egg production, steroid hormone synthesis, and related gene expression in chicken preovulatory follicular granulosa cells. Animals, 12(11), 1467. https://doi.org/10.3390/ani12111467
Yang, X., Chai, L., Bist, B. R., Subedi, S., & Wu, Z. (2022a). A deep learning model for detecting cage-free hens on the litter floor. Animals, 12(15), 1983. https://doi.org/10.3390/ani12151983
Yang, Y., Han, W., Zhang, A., Zhao, M., Cong, W., Jia, Y., Wang, D., & Zhao, R. (2022b). Chronic corticosterone disrupts the circadian rhythm of CRH expression and m6A RNA methylation in the chicken hypothalamus. Journal of Animal Science and Biotechnology, 13(1), 29. https://doi.org/10.1186/s40104-022-00677-4
Yang, X., Bist, R., Subedi, S., & Chai, L. (2023a). A deep learning method for monitoring spatial distribution of cage-free hens. Artificial Intelligence in Agriculture, 8, 20–29. https://doi.org/10.1016/j.aiia.2023.03.003
Yang, X., Bist, R., Subedi, S., Wu, Z., Liu, T., & Chai, L. (2023b). An automatic classifier for monitoring applied behaviors of cage-free laying hens with deep learning. Engineering Applications of Artificial Intelligence, 123. https://doi.org/10.1016/j.engappai.2023.106377
Yang, X., Bist, R., Paneru, B., & Chai, L. (2024). Monitoring activity index and behaviors of cage-free hens with advanced deep learning technologies. Poultry Science, 103(11), 104193. https://doi.org/10.1016/j.psj.2024.104193
Zaninelli, M., Redaelli, V., Luzi, F., Mitchell, M., Bontempo, V., Cattaneo, D., Dell’Orto, V., & Savoini, G. (2018). Development of a machine vision method for the monitoring of laying hens and detection of multiple nest occupations. Sensors, 18(1), 132. https://doi.org/10.3390/s18010132
Zaytsoff, S. J. M., Brown, C. L. J., Montina, T., Metz, G. A. S., Abbott, D. W., Uwiera, R. R. E., & Inglis, G. D. (2019). Corticosterone-mediated physiological stress modulates hepatic lipid metabolism, metabolite profiles, and systemic responses in chickens. Scientific Reports, 9(1). https://doi.org/10.1038/s41598-019-52267-6
Zhang, M., Yan, F.-B., Li, F., Jiang, K.-R., Li, D.-H., Han, R.-L., Li, Z.-J., Jiang, R.-R., Liu, X.-J., & Kang, X.-T. (2017). Genome-wide DNA methylation profiles reveal novel candidate genes associated with meat quality at different age stages in hens. Scientific Reports, 7(1), 45564. https://doi.org/10.1038/srep45564
Zhang, Y., Fütterer, R., & Notni, G. (2023). Interactive robot teaching based on finger trajectory using multimodal RGB-DT-data. Frontiers in Robotics and AI, 10, 1120357. https://doi.org/10.3389/frobt.2023.1120357
Zheng, A., Zhang, A., Chen, Z., Pirzado, S. A., Chang, W., Cai, H., Bryden, W. L., & Liu, G. (2021). Molecular mechanisms of growth depression in broiler chickens (Gallus Gallus domesticus) mediated by immune stress: a hepatic proteome study. Journal of Animal Science and Biotechnology, 12(1), 1–19. https://doi.org/10.1186/s40104-021-00591-1
Authors
Copyright (c) 2025 Tropical Animal Science Journal

This work is licensed under a Creative Commons Attribution-ShareAlike 4.0 International License.
Authors submitting manuscripts should understand and agree that copyright of manuscripts of the article shall be assigned/transferred to Tropical Animal Science Journal. The statement to release the copyright to Tropical Animal Science Journal is stated in Form A. This work is licensed under a Creative Commons Attribution-ShareAlike 4.0 International License (CC BY-SA) where Authors and Readers can copy and redistribute the material in any medium or format, as well as remix, transform, and build upon the material for any purpose, but they must give appropriate credit (cite to the article or content), provide a link to the license, and indicate if changes were made. If you remix, transform, or build upon the material, you must distribute your contributions under the same license as the original.