The exchange of oxygen (O2) and carbon dioxide (CO2) within an incubator has a significant impact on embryonic development (ED) and hatching processes. This study examines the influence of non-ventilation (NV) conditions during the first ten days of incubation at high altitudes on Leghorn hens hatching eggs. Five hundred four hatching eggs were equally divided into three treatment groups and placed in twelve incubators (R = 4). The first group was subjected to standard ventilated conditions (V) during the setting phase. The ventilation inlet holes of the remaining incubators in the NV treatments were closed with either micropore (M) or polypropylene (P) tape, referred to as NVM and NVP groups, respectively. These two different airtight settings were intended to allow for a gradual rise in CO2 naturally generated by the embryos. Results indicate that carbon dioxide concentration gradually increased during the first half of incubation, reaching 1.42% in the NVM group and 1.20% in the NVP group, while the V condition group remained at 0.15%. From 10 days of incubation onwards, normal V conditions were restored in all incubators. The highest hatchability of fertile eggs (HFE) was shown by the NVP group (55.7%), followed by the V (52.6%) and NVM (38.6%) groups. The NVP group showed a greater yolk-free body mass (YFBM) from 10 days of incubation until the hatch basket transfer. NV conditions during the first 10 days of incubation at high altitude produced higher YFBM with gradually decreasing yolk sac mass. In comparison to the NVM and V conditions, the particular NVP condition showed a beneficial impact on the quality of hatched chicks. Sustaining NVP condition (1.2% of CO2) throughout the first half of incubation at high altitude generated the optimal environment in the incubator ensuring the best hatchability results. This study highlights how important it is for hatchery managers to recognize the influence of low O2 and high levels of CO2 on the development trajectories of Leghorn embryos during early incubation at high altitudes.
References
[1]
De Smit, L., Bruggeman, V., Tona, J.K., Debonne, M., Onagbesan, O., Arckens, L., et al. (2006) Embryonic Developmental Plasticity of the Chick: Increased CO2 during Early Stages of Incubation Changes the Developmental Trajectories during Prenatal and Postnatal Growth. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 145, 166-175. https://doi.org/10.1016/j.cbpa.2006.06.046
[2]
García, H.J., Juárez E.M.A. and López, C.S. (2013) Gradual Increase of CO2 during First Stages of Incubation with Late Change of O2 Partial Pressure, Modifies the Hatch Trajectory of Broiler Chicks. Veterinaria México, 44, 1-16. https://www.scielo.org.mx/scielo.php?pid=S0301-50922013000100001&script=sci_abstract&tlng=en
[3]
Tona, K., Voemesse, K., N’nanlé, O., Oke, O.E., Kouame, Y.A.E., Bilalissi, A., et al. (2022) Chicken Incubation Conditions: Role in Embryo Development, Physiology and Adaptation to the Post-Hatch Environment. Frontiers in Physiology, 13, Article 895854. https://doi.org/10.3389/fphys.2022.895854
[4]
Ho, D.H., Reed, W.L. and Burggren, W.W. (2011) Egg Yolk Environment Differentially Influences Physiological and Morphological Development of Broiler and Layer Chicken Embryos. Journal of Experimental Biology, 214, 619-628. https://doi.org/10.1242/jeb.046714
[5]
Molenaar, R., Reijrink, I., Meijerhof, R. and Van den Brand, H. (2010) Meeting Embryonic Requirements of Broilers throughout Incubation: A Review. Revista Brasileira de Ciência Avícola, 12, 137-148. https://doi.org/10.1590/s1516-635x2010000300001
[6]
Fernandes, J., Bortoluzzi, C., Esser, A., Contini, J., Stokler, P. and Faust, D. (2014) Performance of Broilers Submitted to High CO2 Levels during Incubation Combined with Temperature Fluctuations at Late Post-Hatch. Revista Brasileira de Ciência Avícola, 16, 285-290. https://doi.org/10.1590/1516-635x1603285-290
[7]
Yilmaz-Dikmen, B., Sahan, Ü., Ipek, A., Aydin, C. and Kederli, E. (2015) Effect of Oxygen Supplementation in a Hatchery at High Altitude and Growth Performance of Broilers Reared at Low Altitude. South African Journal of Animal Science, 44, 350-359. https://doi.org/10.4314/sajas.v44i4.5
[8]
Okur, N., Eratalar, S.A., Yiğit, A.A., Kutlu, T., Kabakçi, R. and Özsoy, Ş.Y. (2022) Effects of Incubator Oxygen and Carbon Dioxide Concentrations on Hatchability of Fertile Eggs, Some Blood Parameters, and Histopathological Changes of Broilers with Different Parental Stock Ages in High Altitude. Poultry Science, 101, Article ID: 101609. https://doi.org/10.1016/j.psj.2021.101609
[9]
Fares, W.A., Ahmed, M.R.M., Rizk, R.E., Shahein, E.H.A., Boutrous, N.G. and El-Sabrout, K. (2023) Influence of Non-Ventilating Intervals during Early Incubation Stage on Egg Hatching Process. Veterinary World, 16, 1534-1540. https://doi.org/10.14202/vetworld.2023.1534-1540
[10]
Villamor, E., Kessels, C.G.A., Ruijtenbeek, K., van Suylen, R.J., Belik, J., De Mey, J.G.R., et al. (2004) Chronic in OVO Hypoxia Decreases Pulmonary Arterial Contractile Reactivity and Induces Biventricular Cardiac Enlargement in the Chicken Embryo. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 287, R642-R651. https://doi.org/10.1152/ajpregu.00611.2003
[11]
Mortola, J.P. (2009) Gas Exchange in Avian Embryos and Hatchlings. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 153, 359-377. https://doi.org/10.1016/j.cbpa.2009.02.041
[12]
Fernandes, J.I.M., Bortoluzzi, C., Schmidt, J.M., Scapini, L.B., Santos, T.C. and Murakami, A.E. (2017) Single Stage Incubators and Hypercapnia during Incubation Affect the Vascularization of the Chorioallantoic Membrane in Broiler Embryos. Poultry Science, 96, 220-225. https://doi.org/10.3382/ps/pew274
[13]
Okur, N. (2019) Effects of Incubator Carbon Dioxide and Oxygen Levels, and Egg Weight on Broilers’ Hatchability of Fertile Eggs. Brazilian Journal of Poultry Science, 21, 1-7. https://doi.org/10.1590/1806-9061-2019-1038
Walsberg, G.E. (1980) The Gaseous Microclimate of the Avian Nest during Incubation. American Zoologist, 20, 363-372. https://doi.org/10.1093/icb/20.2.363
[16]
Decuypere, E., Tona, K., Bruggeman, V. and Bamelis, F. (2001) The Day-Old Chick: A Crucial Hinge between Breeders and Broilers. World’s Poultry Science Journal, 57, 127-138. https://doi.org/10.1079/wps20010010
[17]
Fasenko, G.M., Robinson, F.E. and Christensen, V.L. (2009) Effects of Long Term Storage on the Egg, Embryo and Chick. Avian Biology Research, 2, 73-79. https://doi.org/10.3184/175815509x431858
[18]
Hogg, A. (1997) Single Stage Incubation Trials. Poultry and Avian Biology Review, 8, 168.
[19]
Ahmed, M., Biswas, A., Roy, B.G. and Srivastava, R.B. (2013) Frequently Encountered Problems during Hatching in Cold Arid High Altitude Regions Such as Ladakh in India: Causes and Remedies. World’s Poultry Science Journal, 69, 897-902. https://doi.org/10.1017/s0043933913000895
[20]
Hassanzadeh, M. (2009) Chronic Hypoxia Due to High Altitude at the Early Stage of Incubation Influenced Pre-and Postnatal Parameters Related to Ascites Syndrome in Broiler Chickens. Proceedings of the 2nd Mediterraean Summit of WPSA, Antalya, 4-7 October 2009, 279-283.
[21]
Şahan, Ü., İpek, A., Yilmaz-Dıkmen, B., Aydin, C. and Kederlı, E. (2011) Effect of Oxygen Supplementation in the Hatcher at High Altitude on the Incubation Results of Broiler Eggs Laid at Low Altitude. British Poultry Science, 52, 388-394. https://doi.org/10.1080/00071668.2011.578122
[22]
Everaert, N., Kamers, B., Witters, A., De Smit, L., Debonne, M., Decuypere, E., et al. (2007) Effect of Four Percent Carbon Dioxide during the Second Half of Incubation on Embryonic Development, Hatching Parameters, and Posthatch Growth. Poultry Science, 86, 1372-1379. https://doi.org/10.1093/ps/86.7.1372
[23]
Bruggeman, V., Tona, K., Onagbesan, O. and Decuypere, E. (2009) Hatching Egg and Chick Quality. In: Hocking, P., Ed., Biology of Breeding Poultry, CABI, 224-239.
[24]
Celen, M.F., Yİldİrİm, I., Parlat, S.S. and Alkis, E. (2009) The Effects of Broiler Breeder Age and Extra Oxygen Addition Into Incubator at High Altitude (1700 m) on Hatching Results and Subsequent Performance in Broilers. Journal of Animal and Veterinary Advances, 8, 1438-1442. http://medwelljournals.com/fulltext/java/2009/1438-1442.pdf
[25]
Tona, K., Onagbesan, O., Bruggeman, V., De Smit, L., Figueiredo, D. and Decuypere, E. (2007) Non-Ventilation during Early Incubation in Combination with Dexamethasone Administration during Late Incubation: 1. Effects on Physiological Hormone Levels, Incubation Duration and Hatching Events. Domestic Animal Endocrinology, 33, 32-46. https://doi.org/10.1016/j.domaniend.2006.04.002
[26]
De Smit, L., Bruggeman, V., Debonne, M., Tona, J.K., Kamers, B., Everaert, N., et al. (2008) The Effect of Nonventilation during Early Incubation on the Embryonic Development of Chicks of Two Commercial Broiler Strains Differing in Ascites Susceptibility. Poultry Science, 87, 551-560. https://doi.org/10.3382/ps.2007-00322
[27]
Maatjens, C.M., Reijrink, I.A.M., Molenaar, R., van der Pol, C.W., Kemp, B. and van den Brand, H. (2014) Temperature and CO2 during the Hatching Phase. I. Effects on Chick Quality and Organ Development. Poultry Science, 93, 645-654. https://doi.org/10.3382/ps.2013-03490
[28]
Tong, Q., McGonnell, I.M., Roulston, N., Bergoug, H., Romanini, C.E.B., Garain, P., et al. (2015) Higher Levels of CO2 during Late Incubation Alter the Hatch Time of Chicken Embryos. British Poultry Science, 56, 503-509. https://doi.org/10.1080/00071668.2015.1041097
[29]
Özlü, S., Uçar, A., Banwell, R. and Elibol, O. (2019) The Effect of Increased Concentration of Carbon Dioxide during the First 3 Days of Incubation on Albumen Characteristics, Embryonic Mortality and Hatchability of Broiler Hatching Eggs. Poultry Science, 98, 771-776. https://doi.org/10.3382/ps/pey464
[30]
Tona, K., Everaert, N., Willemsen, H., Gbeassor, M., Decuypere, E. and Buyse, J. (2013) Effects of Interaction of Incubator CO2 Levels and Mixing Hatching Eggs of Different Embryo Growth Trajectory on Embryo Physiological and Hatching Parameters. British Poultry Science, 54, 545-551. https://doi.org/10.1080/00071668.2013.807907
[31]
Gildersleeve, R.P. and Boeschen, D.P. (1983) The Effects of Incubator Carbon Dioxide Level on Turkey Hatchability. Poultry Science, 62, 779-784. https://doi.org/10.3382/ps.0620779
[32]
El-Hanoun, A., El-Sabrout, K., Abdella, M. and Eid, M. (2019) Effect of Carbon Dioxide during the Early Stage of Duck Egg Incubation on Hatching Characteristics and Duckling Performance. Physiology & Behavior, 208, Article ID: 112582. https://doi.org/10.1016/j.physbeh.2019.112582
[33]
Beker, A., Vanhooser, S.L. and Teeter, R.G. (1995) Effect of Oxygen Level on Ascites Incidence and Performance in Broiler Chicks. Avian Diseases, 39, 285-291. https://doi.org/10.2307/1591869
[34]
Hassanzadeh, M., Fard, M.H.B., Buyse, J., Bruggeman, V. and Decuypere, E. (2004) Effect of Chronic Hypoxia during Embryonic Development on Physiological Functioning and on Hatching and Post-Hatching Parameters Related to Ascites Syndrome in Broiler Chickens. Avian Pathology, 33, 558-564. https://doi.org/10.1080/03079450400013188
[35]
Wolanski, N.J., Renema, R.A., Robinson, F.E., Carney, V.L. and Fancher, B.I. (2006) Relationship between Chick Conformation and Quality Measures with Early Growth Traits in Males of Eight Selected Pure or Commercial Broiler Breeder Strains. Poultry Science, 85, 1490-1497. https://doi.org/10.1093/ps/85.8.1490
[36]
Willemsen, H., Li, Y., Willems, E., Franssens, L., Wang, Y., Decuypere, E., et al. (2011) Intermittent Thermal Manipulations of Broiler Embryos during Late Incubation and Their Immediate Effect on the Embryonic Development and Hatching Process. Poultry Science, 90, 1302-1312. https://doi.org/10.3382/ps.2011-01390
[37]
Tona, K., Bamelis, F., De Ketelaere, B., Bruggeman, V., Moraes, V., Buyse, J., et al. (2003) Effects of Egg Storage Time on Spread of Hatch, Chick Quality, and Chick Juvenile Growth. Poultry Science, 82, 736-741. https://doi.org/10.1093/ps/82.5.736
[38]
Tona, K., Onagbesan, O.M., Jego, Y., Kamers, B., Decuypere, E. and Bruggeman, V. (2004) Comparison of Embryo Physiological Parameters during Incubation, Chick Quality, and Growth Performance of Three Lines of Broiler Breeders Differing in Genetic Composition and Growth Rate. Poultry Science, 83, 507-513. https://doi.org/10.1093/ps/83.3.507
[39]
Willemsen, H., Everaert, N., Witters, A., De Smit, L., Debonne, M., Verschuere, F., et al. (2008) Critical Assessment of Chick Quality Measurements as an Indicator of Posthatch Performance. Poultry Science, 87, 2358-2366. https://doi.org/10.3382/ps.2008-00095
[40]
Tona, K., Bruggeman, V., Onagbesana, O., Bamelis, F., Gbeassor, M., Mertens, K. and Decuypere, E. (2005) Day-Old Chick Quality: Relationship to Hatching Egg Quality, Adequate Incubation Practice and Prediction of Broiler Performance. Avian and Poultry Biology Reviews, 16, 109-119. http://dx.doi.org/10.3184/147020605783438787
[41]
Bruggeman, V., Witters, A., De Smit, L., Debonne, M., Everaert, N., Kamers, B., et al. (2007) Acid-Base Balance in Chicken Embryos (Gallus domesticus) Incubated under High CO2 Concentrations during the First 10 Days of Incubation. Respiratory Physiology & Neurobiology, 159, 147-154. https://doi.org/10.1016/j.resp.2007.04.013
[42]
Everaert, N., Willemsen, H., Hulikova, A., Brown, H., Decuypere, E., Swietach, P., et al. (2010) The Importance of Carbonic Anhydrase II in Red Blood Cells during Exposure of Chicken Embryos to CO2. Respiratory Physiology & Neurobiology, 172, 154-161. https://doi.org/10.1016/j.resp.2010.05.007
[43]
Bilalissi, A., Meteyake, H.T., Kouame, Y.A.E., Oke, O.E., Lin, H., Onagbesan, O., et al. (2022) Effects of Pre-Incubation Storage Duration and Nonventilation Incubation Procedure on Embryonic Physiology and Post-Hatch Chick Performance. Poultry Science, 101, Article ID: 101810. https://doi.org/10.1016/j.psj.2022.101810
[44]
Chan, T. and Burggren, W. (2005) Hypoxic Incubation Creates Differential Morphological Effects during Specific Developmental Critical Windows in the Embryo of the Chicken (Gallus gallus). Respiratory Physiology & Neurobiology, 145, 251-263. https://doi.org/10.1016/j.resp.2004.09.005
[45]
Uni, Z. and Ferket, R.P. (2004) Methods for Early Nutrition and Their Potential. World’s Poultry Science Journal, 60, 101-111. https://doi.org/10.1079/wps20038
[46]
Everaert, N., Willemsen, H., Willems, E., Franssens, L. and Decuypere, E. (2011) Acid-Base Regulation during Embryonic Development in Amniotes, with Particular Reference to Birds. Respiratory Physiology & Neurobiology, 178, 118-128. https://doi.org/10.1016/j.resp.2011.04.023
[47]
Rahn, H., Carey, C., Balmas, K., Bhatia, B. and Paganelli, C. (1977) Reduction of Pore Area of the Avian Eggshell as an Adaptation to Altitude. Proceedings of the National Academy of Sciences of the United States of America, 74, 3095-3098. https://doi.org/10.1073/pnas.74.7.3095
[48]
Scanes, C.G. and Dridi, S. (2021) Sturkie’s Avian Physiology. Academic Press.
[49]
Wolanski, N.J., Renema, R.A., Robinson, F.E., Carney, V.L. and Fancher, B.I. (2007) Relationships among Egg Characteristics, Chick Measurements, and Early Growth Traits in Ten Broiler Breeder Strains. Poultry Science, 86, 1784-1792. https://doi.org/10.1093/ps/86.8.1784
[50]
Deeming, D.C. (2005) Yolk Sac, Body Dimensions and Hatchling Quality of Ducklings, Chicks and Poults. British Poultry Science, 46, 560-564. https://doi.org/10.1080/00071660500255042
[51]
Christensen, V.L., Wineland, M.J., Ort, D.T. and Mann, K.M. (2005) Eggshell Conductance and Incubator Ventilation as Factors in Embryo Survival and Poult Quality. International Journal of Poultry Science, 4, 818-826. https://doi.org/10.3923/ijps.2005.818.826
[52]
Lourens, A., van den Brand, H., Meijerhof, R. and Kemp, B. (2005) Effect of Eggshell Temperature during Incubation on Embryo Development, Hatchability, and Posthatch Development. Poultry Science, 84, 914-920. https://doi.org/10.1093/ps/84.6.914
[53]
Sato, M., Tachibana, T. and Furuse, M. (2006) Heat Production and Lipid Metabolism in Broiler and Layer Chickens during Embryonic Development. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 143, 382-388. https://doi.org/10.1016/j.cbpa.2005.12.019
[54]
van der Wagt, I., de Jong, I.C., Mitchell, M.A., Molenaar, R. and van den Brand, H. (2020) A Review on Yolk Sac Utilization in Poultry. Poultry Science, 99, 2162-2175. https://doi.org/10.1016/j.psj.2019.11.041
[55]
Uni, Z., Ferket, P.R., Tako, E. and Kedar, O. (2005) In OVO Feeding Improves Energy Status of Late-Term Chicken Embryos. Poultry Science, 84, 764-770. https://doi.org/10.1093/ps/84.5.764
[56]
Moran, E.T. (2007) Nutrition of the Developing Embryo and Hatchling. Poultry Science, 86, 1043-1049. https://doi.org/10.1093/ps/86.5.1043
[57]
Druyan, S. (2010) The Effects of Genetic Line (Broilers Vs. Layers) on Embryo Development. Poultry Science, 89, 1457-1467. https://doi.org/10.3382/ps.2009-00304
[58]
Christensen, V.L., Wineland, M.J., Fasenko, G.M. and Donaldson, W.E. (2001) Egg Storage Effects on Plasma Glucose and Supply and Demand Tissue Glycogen Concentrations of Broiler Embryos. Poultry Science, 80, 1729-1735. https://doi.org/10.1093/ps/80.12.1729
[59]
Ipek, A., Sahan, U., Baycan, S.C. and Sozcu, A. (2014) The Effects of Different Eggshell Temperatures on Embryonic Development, Hatchability, Chick Quality, and First-Week Broiler Performance. Poultry Science, 93, 464-472. https://doi.org/10.3382/ps.2013-03336
[60]
Reijrink, I.A.M., Meijerhof, R., Kemp, B. and Van Den Brand, H. (2008) The Chicken Embryo and Its Micro Environment during Egg Storage and Early Incubation. World’s Poultry Science Journal, 64, 581-598. https://doi.org/10.1017/s0043933908000214
[61]
Burggren, W.W., Andrewartha, S.J. and Tazawa, H. (2012) Interactions of Acid-Base Balance and Hematocrit Regulation during Environmental Respiratory Gas Challenges in Developing Chicken Embryos (Gallus gallus). Respiratory Physiology & Neurobiology, 183, 135-148. https://doi.org/10.1016/j.resp.2012.06.011
[62]
Sadler, W.W., Wilgus, H.S. and Buss, E.G. (1954) Incubation Factors Affecting Hatchability of Poultry Eggs. Poultry Science, 33, 1108-1115. https://doi.org/10.3382/ps.0331108
[63]
Latter, G.V. and Baggott, G.K. (2002) Role of Carbon Dioxide and Ion Transport in the Formation of Sub-Embryonic Fluid by the Blastoderm of the Japanese Quail. British Poultry Science, 43, 104-116. https://doi.org/10.1080/00071660120109944
