Hostname: page-component-77c89778f8-cnmwb Total loading time: 0 Render date: 2024-07-17T16:09:14.492Z Has data issue: false hasContentIssue false

Gas exchange during storage and incubation of Avian eggs: effects on embryogenesis, hatchability, chick quality and post-hatch growth

Published online by Cambridge University Press:  08 February 2008

O. ONAGBESAN*
Affiliation:
Laboratory for Physiology and Immunology of Domestic Animals, Catholic University, Kasteelpark Arenberg 30, Heverlee, B-3001Belgium
V. BRUGGEMAN
Affiliation:
Laboratory for Physiology and Immunology of Domestic Animals, Catholic University, Kasteelpark Arenberg 30, Heverlee, B-3001Belgium
L. DE SMIT
Affiliation:
Laboratory for Physiology and Immunology of Domestic Animals, Catholic University, Kasteelpark Arenberg 30, Heverlee, B-3001Belgium
M. DEBONNE
Affiliation:
Laboratory for Physiology and Immunology of Domestic Animals, Catholic University, Kasteelpark Arenberg 30, Heverlee, B-3001Belgium
A. WITTERS
Affiliation:
Laboratory for Physiology and Immunology of Domestic Animals, Catholic University, Kasteelpark Arenberg 30, Heverlee, B-3001Belgium
K. TONA
Affiliation:
Laboratory for Physiology and Immunology of Domestic Animals, Catholic University, Kasteelpark Arenberg 30, Heverlee, B-3001Belgium
N. EVERAERT
Affiliation:
Laboratory for Physiology and Immunology of Domestic Animals, Catholic University, Kasteelpark Arenberg 30, Heverlee, B-3001Belgium
E. DECUYPERE
Affiliation:
Laboratory for Physiology and Immunology of Domestic Animals, Catholic University, Kasteelpark Arenberg 30, Heverlee, B-3001Belgium
*
Get access

Abstract

Embryonic development is a dynamic process that requires a fine balance between several factors in order to achieve an optimum hatchability and chick quality. These factors include the background of the embryo, such as genetic line of the breeders, the age of the breeder, egg weight, and factors related to the environment in which the egg is stored and incubated, such as temperature, humidity, gas levels and altitude. Gas exchanges are of fundamental importance for embryonic development during incubation and may affect the livability of the embryo. This paper reviews the roles of the gaseous environment (i.e. O2 and CO2) around hatching eggs during storage and during incubation and the effect it might have on the survival of the developing embryos and the chicks that hatch. The state of the art on the different attempts to establish the optimum requirements of different gases that promote the optimal developmental trajectories at different periods during incubation is presented. The roles and consequences of different levels of O2 and CO2 during storage and incubation on hatchability, incubation duration, hatching process, embryo growth, embryo mortality, organ development and morphology, metabolism, blood acid-base balance, chick quality and chick post-hatch growth are reviewed.

Type
Research Article
Copyright
Copyright © World's Poultry Science Association 2007

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

ALTIMIRAS, J. and PHU, L. (2000) Lack of physiological plasticity in the early chicken embryo exposed to acute hypoxia. Journal of Experimental Zoology 286: 450456.3.0.CO;2-Y>CrossRefGoogle ScholarPubMed
AR, A., PAGANELLI, C.V., REEVES, R.B., GREENE, D.G. and RAHN, H. (1974) The avian egg: water vapor conductance, shell thickness and functional pore area. The Condor 76: 153158.CrossRefGoogle Scholar
ASSON-BATRES, M.A., STOCK, M.K., HARE, J.F. and METCALFE, J. (1989) O2 effect on composition of chick embryonic heart and brain. Respiratory Physiology 77: 101109.CrossRefGoogle ScholarPubMed
BAMELIS, F.R., TONA, K., DE BAERDEMAEKER, J. and DECUYPERE, E. (2001) Increasing chicken eggs hatchability by matching incubator humidity to eggshell conductance. Proceedings Incubation and Fertility Research Group, Oxford, UK; 11–12 Sept. 2001. International Hatchery Practice 16 (3): 24.Google Scholar
BAMELIS, F.R. (2003) Non-invasive assessment of eggshell conductance at different developmental stages during incubation of eggs. PhD thesis, Catholic University, Leuven, Belgium.Google Scholar
BARROT, H.G. (1937) Effect of temperature, humidity, and other factors on hatch of hens' eggs and on energy metabolism of chick embryos. USDA Technical Bulletin 553: 145.Google Scholar
BAUMANN, R., PADEKEN, S., HALLER, E.A. and BRILMAYER, T. (1983) Effects of hypoxia on oxygen affinity, haemoglobin pattern, and blood volume of early chicken embryos. American Physiology 244: R733R741.Google Scholar
BECKER, W.A. (1964) The storage of White Leghorn hatching eggs in plastic bags. Poultry Science 43: 11091112.CrossRefGoogle Scholar
BECKER, W.A., SPENCER, J.V. and SWARTWOOD, J.L. (1964) The pre-incubation storage of turkey eggs in closed environments. Poultry Science 43: 15261534.CrossRefGoogle Scholar
BECKER, W.A., SPENCER, J.V. and SWARTWOOD, J.L. (1968) Carbon dioxide during storage of chicken and turkey hatching eggs. Poultry Science 47: 251258.CrossRefGoogle ScholarPubMed
BENTON, C.E. and BRAKE, J. (1996) The effect of broiler breeder flock age and length of storage on egg albumen during early incubation. Poultry Science 75: 10691075.CrossRefGoogle ScholarPubMed
BLACKER, H.A., ORGEIG, S. and DANIELS, C.B. (2004) Hypoxic control of the development of the surfactant system in the chicken: evidence for physiological heterokairy. American Journal of Physiology Regulatory Integrative and Comparative Physiology 287: 403410.CrossRefGoogle ScholarPubMed
BOSE, S. and STEWART, G.F. (1948) Comparative and complementary effects of heat treating and oiling shell eggs on their keeping quality. Poultry Science 27: 228234.CrossRefGoogle Scholar
BOUTILIER, R.G., GIBSON, M.A., TOEWS, D.P. and ANDERSON, W. (1977) Gas exchanges and acid-base regulation in the blood and extraembryonic fluids of the developing chicken embryo. Respiration Physiology 31: 8189.CrossRefGoogle ScholarPubMed
BRAKE, J., WALSH, T.J. and VICK, S.V. (1993) Relationship of egg storage time, storage conditions, flock age, eggshell and albumen characteristics, incubation conditions, and machine capacity to broiler hatchability-Review and model synthesis. Zootechnical International 16: 3041.Google Scholar
BROOKS, J. and PACE, J. (1938) The distribution of carbon dioxide in the hen's egg. Proceedings of Royal Society London, series B, Biological Sciences 126: 196210.Google Scholar
BRUGGEMAN, V., WITTERS, A., DE SMIT, L., DEBONNE, M., EVERAERT, N., KAMERS, B., ONAGBESAN, O.M., DEGRAEVES, P. and DECUYPERE, E. (2006) Changes in parameters related to acid-base balance in chicken embryos (Gallus domesticus) incubated under normal or high CO2 concentrations during the first ten days of incubation. Respiratory Physiology and Neurobiology (in press).Google Scholar
BURKE, E. (1925) A study of incubation. Bulletin of University of Montana Agricultural Experimental Station 178: 143.Google Scholar
BURLEY, R.W. and VADEHRA, D.V. (1989) The avian egg: Chemistry and Biology. John Wiley and Sons, NY.Google Scholar
BURTON, G.F., STEVENSON, J.M. and TULLETT, S.G. (1989) The relationship between eggshell porosity and air space gas tensions measured before and during the parafoetal period and their effects on the hatching process in the domestic fowl. Respiration Physiology 77: 89100.CrossRefGoogle ScholarPubMed
BURTON, G.J. and PALMER, M.E. (1992) Development of the chick chorioallantoic capillary plexus under normoxic and normobaric hypoxic and hyperoxic conditions: a morphometric study. Journal of Experimental Zoology 262: 291298.CrossRefGoogle Scholar
BURTON, F.G. and TULLETT, S.G. (1983) A comparison of the effects of eggshell porosity on the respiration and growth of domestic fowl, duck and turkey embryos. Comparative Biochemistry and Physiology 75A: 167174.CrossRefGoogle Scholar
BUYS, N., DEWIL, E., GONZALES, E. and DECUYPERE, E. (1998) Different CO2 levels during incubation interact with hatching time and ascites susceptibility in two broiler lines selected for different growth rate. Avian Pathology 27: 605612.CrossRefGoogle ScholarPubMed
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 and Neurobiology 145: 251263.CrossRefGoogle ScholarPubMed
CHWALIBOG, A., TAUSON, A-H., ALI, A., MATTHIESEN, C, THORHAUGE, K. and THORBEK, G. (2006) Gas exchange, heat production and oxidation of fat in chicken embryos from fast or slow growing line. Comparative Biochemistry and Physiology A (doi: 10.1016/j.cbpa.2006.10.035).Google ScholarPubMed
COTTERILL, O.J. and GARDNER, F. (1957) Retarding thick white deterioration by holding shell eggs in sealed containers. Poultry Science 34: 196206.CrossRefGoogle Scholar
COTTERILL, O.J., GARDNER, F.A., FUNK, E.M. and CUNNINGHAM, F.E. (1958) Relationship between temperature and carbon dioxide loss from shell eggs. Poultry Science 37: 479483.CrossRefGoogle Scholar
CROSSLEY, D.A. II, BURGGREN, W.W. and ALTIMIRAS, J. (2003) Cardiovascular regulation during hypoxia in embryos of the domestic chicken, Gallus gallus. American Journal of Physiology Regulatory Integrative and Comparative Physiology 284: 219226.CrossRefGoogle ScholarPubMed
CRUZ, S.R. and ROMANOFF, A.L. (1944) Effect of oxygen concentration on the development of the chick embryo. Physiological Zoology 17: 184187.CrossRefGoogle Scholar
DAWES, CM. (1975) Acid-base relationships within the avian egg. Biological Review 50: 351371.CrossRefGoogle ScholarPubMed
DAWES, CM. and SIMKISS, K. (1969) The acid base status of the blood of the developing chick embryo. Journal of Experimental Biology 50: 7986.CrossRefGoogle Scholar
DAWES, CM. and SIMKISS, K. (1971) The effects of respiratory acidosis in the chick embryo. Journal of Experimental Biology 55: 7784.CrossRefGoogle Scholar
DE SMIT, L., BRUGGEMAN, V., DEBONNE, M., TONA, K., ONAGBESAN, O., ARCKENS, L., DE BAERDEMAEKER, J. and DECUYPERE, E. (2007) The effects of non-ventillation during early incubation on the development of chick embryos of two commercial broiler strains. British Poultry Science (submitted for publication).Google Scholar
DE SMIT, L., BRUGGEMAN, V., DEBONNE, M., TONA, K., ONAGBESAN, O., ARCKENS, L., DE BAERDEMAEKER, J. and DECUYPERE, E. (2007) The effects of non-ventillation during early incubation on posthatch performance and ascites susceptibility of two commercial broiler strains. Avian Pathology (submitted for publication).Google Scholar
DE SMIT, L., BRUGGEMAN, V., TONA, K., DEBONNE, M., ONAGBESAN, O., ARCKENS, L., DE BAERDEMAEKER, J. and DECUYPERE, E. (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 A. Molecular and Integrative Physiology 145: 166175.CrossRefGoogle ScholarPubMed
DE SMIT, L., TONA, K., BRUGGEMAN, V., ONAGBESAN, O., HASSANZADEH, M., ARKENS, L. and DECUYPERE, E. (2005) Comparison of three lines of broilers differing in ascites susceptibility or growth rate. 2. Egg weight loss, gas pressures, embryonic heat production, and physiological hormone levels. Poultry Science 84: 14461452.CrossRefGoogle ScholarPubMed
DECUYPERE, E., DEWIL, E. and KUHN, E.R. (1991) The hatching process and the role of hormones. In: Avian Incubation. Ed. Tullett, S.G.. Butterworth-Heinemann, London.Google Scholar
DECUYPERE, E., HASSANZADEH, E., BUYS, N. and BUYSE, J. (2005) Further insights into the susceptibility of broilers to ascites. Veterinary Journal 169: 319320.CrossRefGoogle ScholarPubMed
DEEMING, D.C. (1989) Importance of sub-embryonic fluid and albumen in the embryo's response to turning of the egg during incubation. British Poultry Science 30: 591606.CrossRefGoogle Scholar
DEWIL, E., BUYS, N., ALBERS, G.A.A. and DECUYPERE, E. (1996) Different characteristics in chick embryos of two broiler lines differing in susceptibility to ascites. British Poultry Science 37: 10031013.CrossRefGoogle ScholarPubMed
DIETZ, M.W., VANKAMPEN, M., VANGRIESVEN, M.J.M. and VANMOURIK, S. (1998) Daily energy budgets of avian embryos: The paradox of the plateau phase in egg metabolic rate. Physiological Zoology 71: 147156.CrossRefGoogle ScholarPubMed
DUSSEAU, J.W. and HUTCHINS, P.M. (1988) Hypoxia-induced angiogenesis in chick chorioallantoic membranes: a role for adenosine. Respiration Physiology 71: 3344.CrossRefGoogle ScholarPubMed
DUNKER, H.R. (1978) Development of the avian respiratory and circulatory systems. In: Respiratory functions in birds, adult and embryonic (Ed. Piiper, J.), pp. 260273.Springer-Verlag, Berlin.CrossRefGoogle Scholar
DZIALOWSKI, E., VON PLETTENBERG, D., ELMONOUFY, N.A. and BURGGREN, W.W. (2002) Chronic hypoxia alters the physiological and morphological trajectories of developing chicken embryos. Comparative Biochemistry and Physiology A Molecular and Integrative Physiology 131: 713724.CrossRefGoogle ScholarPubMed
EL-IBIARY, H.M., SHAFFNER, C.S. and GODFREY, E.F. (1966) Pulmonary ventilation in a population of hatching chick embryos. British Poultry Science 7: 165176.CrossRefGoogle Scholar
EVERAERT, N., DEBONNE, M., WITTERS, A., DE SMIT, L., KAMERS, B., DECUYPERE, E., BRUGGEMAN, V. (2007) Changes in acid-base balance and related physiological responses as a result of external hypercapnia during the second half of incubation in the chicken embryo. Poultry Science (in press).Google Scholar
FLETCHER, D.A., ORR, H.L., SNYDER, E.S. and NICHOLSON, A.O. (1959) Effect of oiling, packaging materials and addition of CO2 on quality of shell eggs held in storage. Poultry Science 38: 106111.CrossRefGoogle Scholar
FREEMAN, B.M., VINCE, M.A. (1974) Development of the avian embryo. Chapman and Hall. London.CrossRefGoogle Scholar
GEFEN, E and AR, A. (2001) Gas exchange and energy metabolism of the ostrich (Struthio camelus) embryo. Comparative Biochemistry and Physiology A Molecular and Integrative Physiology 130: 689699.CrossRefGoogle ScholarPubMed
GILDERSLEEVE, R.P. and BOESCHEN, D.P. (1983) The effect of incubator carbon dioxide on turkey hatchability. Poultry Science 62: 779784.CrossRefGoogle ScholarPubMed
GILLESPIE, J.I. and MCHANWELL, S. (1987) Measurements of intra embryonic pH during early stages of development in the chick embryo. Cell Tissue Research 247: 445451.CrossRefGoogle ScholarPubMed
GODWIN, T.L., WILSON, M.L. and STADELMAN, W.J. (1962) The effects of oiling, storage position and storage time on the condition of shell eggs. Poultry Science 41: 840844.CrossRefGoogle Scholar
GONYA, T. and STOKES, B.T. (1978) A neurophysiological analysis of the effects of hypercapnia on the embryonic spinal cord. Developmeantal Neuroscience 1: 164171.Google ScholarPubMed
HAMILTON, R.M.G. (1978) Observations on the changes in physical characteristics that influence egg shell quality in ten strains of white leghorns. Poultry Science 57: 11921197.CrossRefGoogle Scholar
HARING, O.H., PATTERSON, J.R. and SARCHE, M.A. (1970) Prenatal development of the cardiovascular system in the chicken. Archives of Pathology 89: 537547.Google ScholarPubMed
HASSANZADEH, M., BUYSE, J. and DECUYPERE, E. (2002) Further evidence for the involvement of cardiac B-adrenergic receptors in right ventricle hypertrophy and ascites in broiler chickens. Avian Pathology 31: 177181.CrossRefGoogle Scholar
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: 558564.CrossRefGoogle ScholarPubMed
HOGG, A. (1997) Single stage incubation trials. Poultry and Avian Biology Review 8: 168.Google Scholar
HOPER, J. and HAHN, H. (1995) Influence of environmental oxygen concentration on growth and vascular density of the vasculosa in the chick embryos. International Journal of Microcirculation and Clinical Experimentation 15: 186192.CrossRefGoogle ScholarPubMed
HURWITZ, S. (1987) Effect of nutrition on egg quality. In: Egg quality – Current problems and recent advances. Ed. Wells, R.G. and Belyavin, C.G.. Butterworths, London.Google Scholar
JANKE, O., TZSCHENTKE, B. and BOERJAN, M.L. (2004) Comparative investigation of heat production and body temperature in embryos of modern chicken breeds. Avian and Poultry Biology Reviews 15: 191196.CrossRefGoogle Scholar
JULIAN, R.J. (1989) Lung volume of meat type chickens. Avian Diseases 33: 174176.CrossRefGoogle Scholar
JULIAN, R.J. (1993) Ascites in poultry. Avian Pathology 22: 419545.CrossRefGoogle Scholar
JULIAN, R.J. (2000) Physiological management and environmental triggers of the ascites syndrome: a review. Avian Pathology 29: 519527.CrossRefGoogle ScholarPubMed
KIRK, S., EMMANS, G.C., MCDONALD, R. and ARNOT, D. (1980) Factors affecting the hatchability of eggs from broiler breeders. British Poultry Science 21: 3753.CrossRefGoogle Scholar
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: 104116.CrossRefGoogle ScholarPubMed
LUNDY, H. (1969) A review of the effects of temperature, humidity, turning and gaseous environment in the incubator on the hatchability of the hen's egg. In: Fertility and Hatchability of the hen's egg. Ed Carter, T.C. and Freeman, B.M.. Liver and Beard, Edinburgh. Pp 143176.Google Scholar
MATHER, CM. and LAUGHLIN, K.F. (1976) Storage of hatching eggs: the effect on total incubation period. British Poultry Science 17: 471479.CrossRefGoogle Scholar
MATHER, CM. and LAUGHLIN, K.F. (1979) Storage of hatching eggs: the interaction between parental age and early embryonic development. British Poultry Science 20: 595604.CrossRefGoogle Scholar
MCCUTCHEON, I.E., METCALFE, J., METZENBERG, A.B. and ETTINGER, T. (1982) Organ growth in hyperoxic and hypoxic chick embryos. Respiratory Physiology 50: 153163.CrossRefGoogle ScholarPubMed
MCDANIEL, G.R., ROLAND, D.A. and COLEMAN, M.A. (1979) The effect of egg shell quality on hatchability and embryonic mortality. Poultry Science 58: 1013.CrossRefGoogle Scholar
MENNA, T.M. and MORTOLA, J.P. (2003) Ventilatory chemosensitivity in the chick embryo. Respiratory Physiology and Neurobiology 137: 6979.CrossRefGoogle ScholarPubMed
MEUER, H.J. and BAUMANN, R. (1988) Oxygen pressure in intra- and extra-embryonic blood vessels of early chick embryos. Respiration Physiology 71: 331342.CrossRefGoogle Scholar
MEUER, H.J., SIEGER, U. and BAUMANN, R. (1989) Measurement of pH in blood vessels and interstitium of 4 and 6 days old chick embryos. Journal of Developmental Physiology 11: 354359.Google ScholarPubMed
MORTOLA, J.P. (2004) Ventilatory response to hypoxia in the chick embryo. Comparative Biochemistry and Physiology A. Molecular Integrative Physiology 137: 723730.CrossRefGoogle Scholar
PAGANELLI, C.V., SOTHERLAND, P.R., OLSZOWKA, A. and RAHN, H. (1988) Regional differences in diffusive conductance/perfusion ratio in the shell of the hen's egg. Respiration Physiology 71: 4556.CrossRefGoogle ScholarPubMed
PEACOCK, A.J., PICKETT, C, MORRIS, K. and REEVES, J.T. (1990) Spontaneous hypoxemia and right ventricular hypertrophy in fast growing broiler chickens reared at sea level. Comparative Biochemistry and Physiology A Molecular Integrative Physiology 97: 537547.CrossRefGoogle ScholarPubMed
PEEBLES, E.D. and BRAKE, J. (1987) Eggshell quality and hatchability in broiler breeder eggs. Poultry Science 66: 596604.CrossRefGoogle Scholar
PROUDFOOT, F.G. (1964) The effects of plastic packaging and other treatments on hatching eggs. Canadian Journal of Animal Science 44: 8795.CrossRefGoogle Scholar
PROUDFOOT, F.G. (1965) The effect of film permeability and concentration of nitrogen, oxygen and helium gases on hatching eggs stored in polyethylene and Cryovac bags. Poultry Science 44: 636644.CrossRefGoogle ScholarPubMed
RAHN, R. (1981) Gas exchange of avian eggs with special reference to turkey eggs. Poultry Science 60: 19711980.CrossRefGoogle Scholar
RAHN, H. and AR, A. (1980) Gas exchange of the avian egg: time, structure and function. American Zoology 20: 477484.CrossRefGoogle Scholar
RAHN, H., CHRISTENSEN, V.L. and EDENS, F.W. (1981) Changes in shell conductance, pores and physical dimensions of egg and shell during the first breeding cycle of the turkey hens. Poultry Science 60: 25362541.CrossRefGoogle Scholar
REIZIS, A., HAMMEL, I. and AR, A. (2005) Regional and developmental variations of blood vessels morphometry in the chick embryo chorioallatoic membrane. Journal of Experimental Biology 208: 24832488.CrossRefGoogle Scholar
REMOTTI, E. (1933) Adattamento respiratorio e suo substrato morfologico nello sviluppo embrionale degli Uccelli. Boll. Mus. Zool. E Anat. Comp. R. Univ. Genova. Ser. II. 13, 321.Google Scholar
RICHARDS, M.P., STOCK, M.K. and METCALFE, J. (1991) Effects of brief hypoxia and hyperoxia on tissue trace element levels in the developing chick embryo. Magnesium Trace Element 10: 305320.Google ScholarPubMed
RIDDLE, O. (1924) On the necessary gaseous environment of the bird embryo. Ecology 5: 348362.CrossRefGoogle Scholar
ROMANOFF, A.L. (1960) The avian embryo: structure and functional development. McMillan, Ney York, NY.Google Scholar
ROMANOFF, A.L. (1967) Biochemistry of avian embryo. Interscience Publishers. Ney York.Google Scholar
ROMANOFF, A.L. and ROMANOFF, A.J. (1933) Biochemistry and biophysics of the developing hen's egg. II. Influence of composition of air. Cornell University, Agricultural experimental station. Bulletin 150: 136.Google Scholar
ROMANOFF, A.L. and ROMANOFF, A.J. (1949) The avian egg. John Willey and Sons, Ney York.Google Scholar
ROQUE, L. and SOARES, M.C. (1994) Effects of eggshell quality and broiler breeder age on hatchability. Poultry Science 73: 18381845.CrossRefGoogle ScholarPubMed
ROUWET, E.V., TINTU, A.N., SCHELLINGS, M.W., VAN BILSEN, M., LUYGEN, E., HOFSTRA, L., SLAAF, D.M., RAMSAY, G. and LE NOBLE, F.A. (2002) Hypoxia induces aortic hypertrophic growth, left ventricular dysfunction, and sympathetic hyperinnervation of peripheral arteries in the chick embryo. Circulation 105: 27912796.CrossRefGoogle ScholarPubMed
RUCKMAN, R.N., ROSENQUIST, G.C., RADEMAKER, D.A., MORSE, D.E. and GETSON, P.R. (1985) The effect of graded hypoxia on the embryonic chick heart. Teratology 32: 463472.CrossRefGoogle ScholarPubMed
RUIJTENBEEK, K., KESSELS, L.C.G.A., DE MEY, J.G.R. and BLANCO, C.E. (2003) Chronic moderate hypoxia and protein malnutrition both induce growth retardation, but have distinct effects on arterial endothelium-dependent reactivity in the chicken embryo. Pediatric Research 53: 573579.CrossRefGoogle ScholarPubMed
RUTHERFORD, P.P. and MURRAY, M.W. (1963). Effect of selected polymers upon the albumen quality of eggs after storage for short periods. Poultry Science 49: 499505.CrossRefGoogle Scholar
SADLER, W.W., WILGUS, H.S. and BUSS, E.G. (1954) Incubation factors affecting hatchability of poultry eggs. Poultry Science 33: 11081115.CrossRefGoogle Scholar
SAUVEUR, B., FERRE, R. and LACASSAGNE, L. (1967) Conservation d'oeufs de poule sous atmosphere enrichie en gaz carbonique. Action sur les resultats d'eclosion. Annals Zootechnic 16: 351356.CrossRefGoogle Scholar
SEYMOUR, R.S. and VISSCHEDIJK, A.H.J. (1988) Effects of variation in total and regional shell conductance on air cell gas tensions and regional gas exchange in chicken eggs. Journal of Comparative Physiology B 158: 229236.CrossRefGoogle Scholar
SHARMA, S.K., LUCITTI, J.L., NORDMAN, C, TINNEY, J.P., TOBITA, K. and KELLER, B.B. (2006) Impact of hypoxia on early chick embryo growth and cardiovascular function. Pediatric Research 59: 116120.CrossRefGoogle ScholarPubMed
SMITH, A.J.M. (1933) Rate of carbon dioxide output by eggs. Dept. Sci. Ind. Research, Camb., Report of the Food Investigation Board for 1932, pp 9597.Google Scholar
SMITH, M. (1931) The relations between yolk and white in the hen's egg. III. Gas exchange in infertile eggs. Journal of Experimental Biology 8: 312318.CrossRefGoogle Scholar
SOLOMON, S.E. (1991) Egg and eggshell quality. Wolfe Publishing Ltd., London.Google Scholar
STOCK, M.K., FRANCISCO, D.L. and METCALFE, J. (1983) Organ growth in chick embryos incubated in 40% or 70% oxygen. Respiration Physiology 52: 111.CrossRefGoogle ScholarPubMed
STOCK, M.K. and METCALFE, J. (1987) Modulation of growth and metabolism of the chick embryo by a brief (72-hr) change in oxygen availability. Journal of Experimental Zoology Supplement 1: 351356.Google ScholarPubMed
STRICK, D.M., WAYCASTER, R.L., MONTANI, J.P., GAY, W.J. and ADAIR, T.H. (1991) Morphometric measurements of chorioallantoic membrane vascularity: effects of hypoxia and hyperoxia. American Journal of Physiology Heart and Circulation Physiology 260: H1385H1389.CrossRefGoogle ScholarPubMed
SWANSON, M.H. and HELBACKA, N.J. (1954) Utilizing carbon dioxide vapour-proof packaging in the preservation of shell egg quality. Poultry Science 33: 10841091.Google Scholar
TAYLOR, L.W. and KREUTZIGER, O. (1965) The gaseous environment of the chick embryo in relation to its development and hatchability. 2. Effects of carbon dioxide and oxygen levels during the period of the fifth through the eighth days of incubation. Poultry Science 44: 98106.CrossRefGoogle ScholarPubMed
TAYLOR, L.W. and KREUTZIGER, O. (1966) The gaseous environment of the chick embryo in relation to its development and hatchability. 3. Effects of carbon dioxide and oxygen levels during the period of the nineth through the twelfth days of incubation. Poultry Science 45: 867884.CrossRefGoogle Scholar
TAYLOR, L.W. and KREUTZIGER, O. (1969) The gaseous environment of the chick embryo in relation to its development and hatchability. 4. Effects of carbon dioxide and oxygen levels during the period of the thirteenth through the sixteenth days of incubation. Poultry Science 48: 871877.CrossRefGoogle ScholarPubMed
TAYLOR, L.W., KREUTZIGER, O. and ABERCROMBIE, G.L. (1971) The gaseous environment of the chick embryo in relation to its development and hatchability. 5. Effects of carbon dioxide and oxygen levels during the terminal days of incubation. Poultry Science 50: 6678.CrossRefGoogle ScholarPubMed
TAYLOR, L.W., SJODIN, R.A. and GUNNS, C.A. (1956) The gaseous environment of the chick embryo in relation to its development and hatchability. 1. Effects of carbon dioxide and oxygen levels during the first four days of incubation upon hatchability. Poultry Science 35: 12061215.CrossRefGoogle Scholar
TAZAWA, H. (1980) Adverse effect of failure to turn the avian egg on the embryo oxygen exchange. Respiration Physiology 41: 137142.CrossRefGoogle ScholarPubMed
TOBITA, K. and KELLER, B.B. (2000) Right and left ventricular wall deformation patterns in normal and left heart hypoplasia chick embryos. American Journal of Physiology Heart and Circulation Physiology 279: H959H969.CrossRefGoogle ScholarPubMed
TONA, K., BAMELIS, F., DE KETELAERE, B., BRUGGEMAN, V. and DECUYPERE, E. (2002) Effect of induced molting on albumen quality, hatchability and chick body weight from breeders. Poultry Science 81: 327332.CrossRefGoogle ScholarPubMed
TONA, K., ONAGBESAN, O., BRUGGEMAN, V., DE SMIT, L., FIGUEIREDO, D. and DECUYPERE, E. (2006) 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 (in press).Google Scholar
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: 507513.CrossRefGoogle ScholarPubMed
TULLETT, S.G. (1978) Pore size versus pore number in avian eggshells. In: Respiratory function in birds, adult and embryonic (Ed Piiper, J.) pp 217226. Springer, Berlin.Google Scholar
TULLETT, S.G. (1981) Theoretical and practical aspects of eggshell porosity. Turkeys 29: 2428.Google Scholar
TULLETT, S.G. (1984) The porosity of avian eggshell. Comparative Biochemistry and Physiology 78A: 513.CrossRefGoogle Scholar
TULLETT, S.G. (1990) The science and art of incubation. Poultry Science 69: 115.CrossRefGoogle ScholarPubMed
TULLETT, S.G. and DEEMING, D.C. (1982) The relationship between eggshell porosity and oxygen consumption of the embryo in the domestic fowl. Comparative Biochemistry and Physiology 72A: 529533.CrossRefGoogle Scholar
VILLAMOR, E., KESSELS, C.G.A., RUIJTENBEEK, K., VAN SUYLEN, R.J., BELIK, J. and BLANCO, C.E. (2004) Chronic in ovo hypoxia decreases pulmonary arterial contractile reactivity and induces biventricular cardiac enlargement in the chicken embryo. American Journal of Physiology Integrative and Comparative Physiology 287: R642R651.CrossRefGoogle ScholarPubMed
VINCE, M.A. and SALTER, S.H. (1967) Respiration and clicking in quail embryos. Nature 216: 582583.CrossRefGoogle ScholarPubMed
VISSCHEDIJK, A.H. (1985) Gas exchange and hatchability of chicken eggs incubated at simulated high altitude. Journal of Applied Physiology 58: 416418.CrossRefGoogle ScholarPubMed
VISSCHEDIJK, A.H.J. (1968a) The air space and embryonic respiration: 1. The pattern of gaseous exchange in the fertile egg during the closing stages of incubation. British Poultry Science 9: 173184.CrossRefGoogle Scholar
VISSCHEDIJK, A.H.J. (1968b) The air space and embryonic respiration: 3. the balance between oxygen and carbon dioxide in the air space of the incubating chicken egg and its role in stimulating pipping. British Poultry Science 9: 197210.CrossRefGoogle ScholarPubMed
VISSCHEDIJK, A.H.J. (1991) Gordon Memorial Lecture: Physics and physiology of incubation. British Poultry Science 32: 320.CrossRefGoogle ScholarPubMed
VLECK, D., VLECK, CM. and HOYT, D.F. (1980) Metabolism of avian embryos: ontogeny of oxygen consumption in the Rhea and Emu. Physiological Zoology 53: 125135.CrossRefGoogle Scholar
WALSH, T.J., RIZK, R.E. and BRAKE, J. (1995) Effects of temperature and carbon dioxide on albumen characteristics, weight loss, and early embryonic mortality of long stored hatching eggs. Poultry Science 74: 14031410.CrossRefGoogle Scholar
WANGENSTEEN, O.D. and RAHN, H. (1970) Respiratory gas exchange by the avian embryo. Respiration Physiology 11: 3145.CrossRefGoogle ScholarPubMed
XU, L.J. and MORTOLA, J.P. (1989) Effects of hypoxia or hyperoxia on the lung of chick embryo. Canadian Journal of Physiology and Pharmacology 67: 515519.CrossRefGoogle ScholarPubMed