Importance of albumen during embryonic development in avian species, with emphasis on domestic chicken

References

• AHN, D.U., KIMAND, S.M. and SHU, H. (1997) Effect of egg size and strain and age of hens on the solids content of chicken eggs. Poultry Science 76: 914–919.
   PubMed Web of Science ®Google Scholar
• AKBAR, M.K., GAVORA, J.S., FRIARS, G.W. and GOWE, R.S. (1983) Composition of eggs by commercial size categories: effects of genetic group, age and diet. Poultry Science 62: 925–933.
   Web of Science ®Google Scholar
• AMUNDSEN, T. and STOKLAND, J.N. (1990) Egg size and parental quality influence in nestling growth in the Shag. Auk 107: 410–413.
   Web of Science ®Google Scholar
• AR, A. (1991) Egg water movements during incubation, in: TULLETT, S.G. (Ed) Avian Incubation, pp. 157–174 (London, Butterworth-Heinemann).
   Google Scholar
• AR, A. and YOM-TOV, Y. (1978) The evolution of parental care in birds. Evolution 32: 655–669.
   PubMed Web of Science ®Google Scholar
• BAINTNER, K. Jr and FEHÉR, G. (1974) Fate of egg white trypsin inhibitor and start of proteolysis in developing chick embryo and newly hatched chick. Developmental Biology 36: 272–278.
   PubMed Web of Science ®Google Scholar
• BOARD, R.G. (1966) The course of microbial infection of the hen's egg. Journal of Applied Bacteriology 29: 319–341.
   PubMedGoogle Scholar
• BOARD, R.G. and FULLER, R. (1974) Non-specific antimicrobial defenses of the avian egg, embryo, and neonate. Biological Reviews 49: 15–49.
   PubMed Web of Science ®Google Scholar
• BONISOLI-ALQUATI, A., MARTINELLI, R., RUBOLINI, D., ROMANO, M., BONCORAGLIO, G., FASOLA, M. and SAINO, N. (2007) Effects of egg albumen removal on yellow-legged gull chick phenotype. Functional Ecology 21: 310–316.
   Web of Science ®Google Scholar
• BONISOLI-ALQUATI, A., MARTINELLI, R., RUBOLINI, D. and SAINO, N. (2008) Sex-specific effects of albumen removal and nest environment manipulation on barn swallow nestlings. Ecology 89: 2315–2324.
   PubMed Web of Science ®Google Scholar
• BYERLY, T.C. (1932) Growth of the chick embryo in relation to its food supply. Journal of Experimental Zoology 9: 15–44.
   Google Scholar
• CAREY, C., RAHN, H. and PARISI, P. (1980) Calories, water, lipid and yolk in avian eggs. Condor 82: 335–343.
   Web of Science ®Google Scholar
• CARINCI, P. and MANZOLI-GUIDOTTI, L. (1968) Albumen absorption during chick embryogenesis. Journal of Embryology and Experimental Morphology 20: 107–118.
   PubMedGoogle Scholar
• CHRISTENSEN, V.L., GRIMES, J.L., DONALDSON, W.E. and LERNER, S. (2000) Correlation of body weight with hatchling blood glucose concentration and its relationship to embryonic survival. Poultry Science 79: 1817–1822.
   PubMed Web of Science ®Google Scholar
• CHRISTIANS, J.K. (2002) Avian egg size: variation within species and inflexibility within individuals. Biological Reviews 77: 1–26.
   PubMed Web of Science ®Google Scholar
• DAVIS, T.A. and ACKERMAN, R.A. (1987) Effects of increased water loss on growth and water content of the chick embryo. Journal of Experimental Zoology Supplement 1: 357–396.
   PubMedGoogle Scholar
• DEEMING, D.C. (1989a) Characteristics of unturned eggs: critical period, retarded embryonic growth and poor albumen utilisation. British Poultry Science 30: 239–249.
   PubMed Web of Science ®Google Scholar
• DEEMING, D.C. (1989b) Importance of sub-embryonic fluid and albumen in the embryo's response to turning of the egg during incubation. British Poultry Science 30: 591–606.
   PubMed Web of Science ®Google Scholar
• DEEMING, D.C. (1991) Reasons for the dichotomy in egg turning in birds and reptiles, in: DEEMING, D.C. & FERGUSON, M.W.J. (Eds) Egg Incubation: Its Effects on Embryonic Development in Birds and Reptiles, pp. 307–323 (Cambridge, Cambridge University Press).
   Google Scholar
• DEEMING, D.C. (2002) Avian Incubation: Behaviour, Environment and Evolution (Oxford, Oxford University Press).
   Google Scholar
• DEEMING, D.C. (2007) Allometry of mass and composition in bird eggs: effects of phylogeny and hatchling maturity. Avian & Poultry Biology Reviews 18: 71–86.
   Google Scholar
• EVERAERT, N., WILLEMSEN, H., DE SMIT, L., WITTERS, A., DE BAERDEMAEKER, J., DECUYPERE, E. and BRUGGEMAN, V. (2008) Comparison of a modern broiler and layer strain during embryonic development and the hatching process. British Poultry Science 49: 574–582.
   PubMed Web of Science ®Google Scholar
• EVERAERT, N., MÉTAYER-COUSTARD, S., WILLEMSEN, H., HAN, H., SONG, Z., ANSARI, Z., DECUYPERE, E., BUYSE, J. and TESSERAUD, S. (2013) The effect of albumen removal before incubation (embryonic protein undernutrition) on the post-hatch performance, regulators of protein translation activation and proteolysis in neonatal broilers. British Journal of Nutrition 110: 265–274.
   PubMed Web of Science ®Google Scholar
• FERRARI, R.P., MARTINELLI, R. and SAINO, N. (2006) Differential effects of egg albumen content on barn swallow nestlings in relation to hatch order. Journal of Evolutionary Biology 19: 981–993.
   PubMed Web of Science ®Google Scholar
• FINKLER, M.S., VAN ORMAN, J.B. and SOTHERLAND, P.R. (1998) Experimental manipulation of egg quality in chickens: influence of albumen and yolk on the size and body composition of near-term embryos in a precocial bird. Journal of Comparative Physiology B168: 17–24.
   Web of Science ®Google Scholar
• FISHER, C. (1969) The effects of a protein deficiency on egg composition. British Poultry Science 10: 149–154.
   PubMed Web of Science ®Google Scholar
• FLETCHER, D.L., BRITTON, W.M., RAHN, A.P. and SAVAGE, S.I. (1981) The influence of layer flock age on egg component yields and solids content. Poultry Science 60: 983–987.
   Web of Science ®Google Scholar
• FLETCHER, D.L., BRITTON, W.M., PESTI, G.M., RAHN, A.P. and SAVAGE, S.I. (1983) The relationship of layer flock age and egg weight on egg component yields and solids content. Poultry Science 62: 1800–1805.
   Web of Science ®Google Scholar
• FREEMAN, B.M. and VINCE, M.A. (1974) Development of the avian embryo: a behavioural and physiological study (London, Chapman and Hall).
   Google Scholar
• FRENCH, N.A. and TULLET, S.G. (1991) Variation in the eggs of poultry species, in: TULLETT, S.G. (Ed.) Avian Incubation, pp. 59–77 (London, Butterworth-Heinemann).
   Google Scholar
• GUERIN-DUBIARD, C., PASCO, M., MOLLE, D., DESERT, C., CROGUENNEC, T. and NAU, F. (2006). Proteomic analysis of hen egg white. Journal of Agricultural and Food Chemistry 54: 3901–3910.
   PubMed Web of Science ®Google Scholar
• GUIBERT, F., RICHARD-YRIS, M.A., LUMINEAU, S., KOTRSCHAL, K., BERTIN, A., PETTON, C., MÖSTL, E. and HOUDELIER, C. (2011) Unpredictable mild stressors on laying females influence the composition of Japanese quail eggs and offspring's phenotype. Applied Animal Behaviour Science 132: 51–60.
   Web of Science ®Google Scholar
• HARTMANN, C., JOHANSSON, K., STRANDBERG, E. and RYDHMER, L. (2003) Genetic correlations between the maternal genetic effect on chick weight and the direct genetic effects on egg composition traits in a White Leghorn line. Poultry Science 82: 1–8.
   PubMed Web of Science ®Google Scholar
• HEPP, G.R., STANGOHR, D.J., BAKER, L.A. and KENNAMER, R.A. (1987) Factors affecting variation in the egg and duckling components of wood ducks. Auk 104: 435–443.
   Web of Science ®Google Scholar
• HILL, W.L. (1993) Importance of prenatal nutrition to the development of a precocial chick. Developmental Psychobiology 26: 237–249.
   PubMed Web of Science ®Google Scholar
• HILL, W.L. (1995) Intraspecific variation in egg composition. Wilson Bulletin 107: 382–387.
   Google Scholar
• HILLSTROM, L. (1999) Variation in egg mass in the Pied Flycatcher, Ficedula hypoleuca: an experimental test of the brood survival and brood reduction hypotheses. Evolutionary Ecology Research 1: 753–768.
   Web of Science ®Google Scholar
• KESHAVARZ, K. and NAKAJIMA, S. (1995) The effect of dietary manipulations of energy, protein and fat during the growing and laying periods on early egg weight and egg components. Poultry Science 74: 50–61.
   PubMed Web of Science ®Google Scholar
• KILPI, M., HILLSTROM, L. and LINDSTROM, K. (1996) Egg-size variation and reproductive success in the herring gull Larus argentatus: adaptive or constrained size of the last egg? Ibis 138: 212–217.
   Web of Science ®Google Scholar
• KRAMER, T.T. and CHO, H.C. (1970) Transfer of immunoglobulins and antibodies in the hen's egg. Immunology 19: 157–167.
   PubMed Web of Science ®Google Scholar
• LAKSHMANAN, N., HAWES, R.O. and KLING, L.J. (1992) Research note: influence of ahemeral light:dark cycles on egg traits in brown egg pullets. Poultry Science 71: 565–569.
   PubMed Web of Science ®Google Scholar
• LI, F., XU, L.M., SHAN, A.S., HU, J.W., ZHANG, Y.Y. and LI, Y.H. (2011) Effects of daily feed intake in laying period on laying performance, egg quality and egg composition of genetically fat and lean lines of chickens. British Poultry Science 52: 163–168.
   PubMed Web of Science ®Google Scholar
• MANN, K. (2007) The chicken egg white proteome. Proteomics 7: 3558–3568.
   PubMed Web of Science ®Google Scholar
• MARION, W.W., NORDSKOG, A.W., TOLMAN, H.S. and FORSYTHE, R.H. (1964) Egg composition as influenced by breeding, egg size, age and season. Poultry Science 43: 255–264.
   Web of Science ®Google Scholar
• MARSHALL, M.E. and DEUTSCH, H.F. (1950) Some protein changes in fluids of the developing chick embryo. Journal of Biological Chemistry 185: 155–161.
   PubMed Web of Science ®Google Scholar
• MARSHALL, M.E. and DEUTSCH, H.F. (1951) Distribution of egg white proteins in chicken blood serum and egg yolk. Journal of Biological Chemistry 189: 1–9.
   PubMed Web of Science ®Google Scholar
• McINDOE, W.M. (1960) Changes in the protein content of yolk during chick embryogenesis. Journal of Embryology and Experimental Morphology 8: 47–53.
   Google Scholar
• MILLER, S.L., GREEN, L.R., PEEBLES, D.M., HANSON, M.A. and BLANCO, C.E. (2002) Effect of chronic hypoxia and protein malnutrition on growth in the developing chick. American Journal of Obstetrics and Gynecology 186: 261–267.
   PubMed Web of Science ®Google Scholar
• MORAN, E.T. Jr (2007) Nutrition of the developing embryo and hatchling. Poultry Science 86: 1043–1049.
   PubMed Web of Science ®Google Scholar
• MURAMATSU, T., HIRAMOTO, K., KOSHI, N., OKUMURA, J., MIYOSHI, S. and MITSUMOTO, T. (1990) Importance of albumen content in whole-body protein synthesis of the chicken embryo during incubation. British Poultry Science 31: 101–106.
   PubMed Web of Science ®Google Scholar
• NABER, E.C. (1979) The effect of nutrition on the composition of eggs. Poultry Science 58: 518–528.
   Web of Science ®Google Scholar
• NELSON, T.C., GROTH, K.D. and SOTHERLAND, P.R. (2010) Maternal investment and nutrient use affect phenotype of American alligator and domestic chicken hatchlings. Comparative Biochemistry and Physiology A157: 19–27.
   Web of Science ®Google Scholar
• NISBET, I.C.T. (1978) Dependence of fledgling success on egg-size, parental performance and egg-composition among Common and Roseate Terns, Sterna hirundo and S. dougallii. Ibis 120: 207–215.
   Web of Science ®Google Scholar
• NOVAK, C., YAKOUT, H. and SCHEIDELER, S. (2004) The combined effects of dietary lysine and total sulfur amino acid level on egg production parameters and egg components in Dekalb Delta laying hens. Poultry Science 83: 977–984.
   PubMed Web of Science ®Google Scholar
• OOSTERWOUD, A. (1987) Effect of egg handling on egg quality, in: WELLS, R.G. & BELYAVIN, C.G. (Eds) Egg Quality: Current problems and recent advances, pp. 283–292 (London, Butterworths).
   Google Scholar
• PALMER, B.D. and GUILLETTE, L.J. (1991) Oviductal proteins and their influence on embryonic development in birds and reptiles, in: DEEMING, D.C. & FERGUSON, M.W.J. (Eds) Egg Incubation: Its Effects on Embryonic Development in Birds and Reptiles, pp. 29–46 (Cambridge, Cambridge University Press).
   Google Scholar
• PAN, C., ZHAO, Y., LIAO, S.F., CHEN, F., QIN, S., WU, X., ZHOU, H. and HUANG, K. (2011) Effect of selenium-enriched probiotics on laying performance, egg quality, egg selenium content, and egg glutatione peroxidase activity. Journal of Agricultural and Food Chemistry 59: 11424–11431.
   PubMed Web of Science ®Google Scholar
• PARSONS, J. (1976) Factors determining the number and size of eggs laid by the Herring Gull. Condor 78: 481–492.
   Web of Science ®Google Scholar
• PROCHASKA, J.F., CAREY, J.B. and SHAFER, D.J. (1996) The effect of L-lysine intake on egg component yield and composition in laying hens. Poultry Science 75: 1268–1277.
   PubMed Web of Science ®Google Scholar
• RICKLEFS, R.E. (1984) Variation in the size and composition of eggs of the European Starling. Condor 86: 1–6.
   Web of Science ®Google Scholar
• RODDA, D.D., FRIARS, G.W., GAVORA, J.S. and MERRIT, E.S. (1977) Genetic parameters estimates and strain comparisons of egg compositional traits. British Poultry Science 18: 459–473.
   Web of Science ®Google Scholar
• RODRICKS, C.L., ROSE, I.A., CAMM, E.J., JENKIN, G., MILLER, S.L. and GIBBS, M.E. (2004) The effect of prenatal hypoxia and malnutrition on memory consolidation in the chick. Developmental Brain Research 148: 113–119.
   PubMedGoogle Scholar
• ROHWER, F.C. (1986) Composition of Blue-winged Teal eggs in relation to egg size, clutch size and the timing of laying. Condor 88: 513–519.
   Web of Science ®Google Scholar
• ROMANOFF, A.L. and ROMANOFF, A.J. (1949) The Avian Egg. (New York, John Wiley & Sons Inc).
   Google Scholar
• ROMANOFF, A.L. (1960) The avian embryo: Structural and functional development. (New York, The MacMillan Company).
   Google Scholar
• ROMANOFF, A.L. (1967) Biochemistry of the avian egg. (New York, Wiley).
   Google Scholar
• 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: 573–579.
   PubMed Web of Science ®Google Scholar
• SAITO, Z., MARTIN, W.G. and COOK, W.H. (1965) Changes in the major macromolecular fractions of egg yolk during embryogenesis. Canadian Journal of Biochemistry 43: 1755–1770.
   PubMedGoogle Scholar
• SCHLESINGER, A.B. (1958) The structural significance of the avian yolk in embryogenesis. Journal of Experimental Zoology 138: 223–258.
   Google Scholar
• SCHMIDT, G. (1937) On the growth stimulating effect of egg-white and its importance for embryonic development. Enzymologia 4: 40–48.
   Google Scholar
• SCOTT, T.R., JOHNSON, W.A., SATTERLEE, D.G. and GILDERSLEEVE, R.P. (1981) Circulating levels of corticosterone in the serum of developing chick embryos and newly hatched chicks. Poultry Science 60: 1314–1320.
   PubMed Web of Science ®Google Scholar
• SCOTT, T.A. and SILVERSIDES, F.G. (2000) The effect of storage and strain of hen of egg quality. Poultry Science 79: 1725–1729.
   PubMed Web of Science ®Google Scholar
• SHAFER, D.J., CAREY, J.B. and PROCHASKA, J.F. (1996) Effect of dietary methionine intake on egg component yield and composition. Poultry Science 75: 1080–1085.
   PubMed Web of Science ®Google Scholar
• SHAFER, D.J., CAREY, J.B., PROCHASKA, J.F. and SAMS, A.R. (1998) Dietary methionine intake effects on egg component yield, composition, functionality and texture profile analysis. Poultry Science 77: 1056–1062.
   PubMed Web of Science ®Google Scholar
• SIMKISS, K. (1980) Eggshell porosity and the water metabolism of the chick embryo. Journal of Zoology London 192: 1–8.
   Web of Science ®Google Scholar
• SOTHERLAND, P.R. and RAHN, H. (1987) On the composition of bird eggs. Condor 89: 48–65.
   Web of Science ®Google Scholar
• SOTHERLAND, P.R., WILSON, J.A. and CARNEY, K.M. (1990) Naturally occurring allometric engineering experiments in avian eggs. American Zoologist 30: 86A.
   Google Scholar
• SPRATT, N.T. (1947) Development in vitro of the early chick blastoderm explanted on yolk and albumen extract saline-agar substrata. Journal of Experimental Zoology 106: 345–366.
   PubMedGoogle Scholar
• STADELMAN, W.J. and PRATT, D.E. (1989) Factors influencing composition of the hen's egg. World's Poultry Science Journal 45: 247–266.
   Web of Science ®Google Scholar
• STAR, L., DECUYPERE, E., PARMENTIER, H.K. and KEMP, B. (2008) Effect of single or combined climatic and hygienic stress in four layer lines: 2. Endocrine and oxidative stress responses. Poultry Science 87: 1031–1038.
   PubMed Web of Science ®Google Scholar
• STARCK, J.M. (1998) Structural variants and invariants in avian embryonic and postnatal development, in: STARCK, J.M. & RICKLEFS, R.E. (Eds) Avian growth and development pp.59–88 (Oxford, Oxford University Press).
   Google Scholar
• ST. CLAIR, C.C. (1996) Multiple mechanisms of reverse hatching asynchrony in rockhopper penguins. Journal of Animal Ecology 65: 485–494.
   Web of Science ®Google Scholar
• STERN, C.D. (1991) The sub-embryonic fluid of the egg of the domestic fowl and its relationship to the early development of the embryo, in: TULLET, S.G. (Ed) Avian Incubation (London, Butterworth-Heinemann).
   Google Scholar
• STOKLAND, J.N. and AMUNDSEN, T. (1988) Initial size hierarchy in broods of the Shag: relative significance of egg size and hatchling asynchrony. Auk 105: 308–315.
   Web of Science ®Google Scholar
• SUGIMOTO, Y., SAITO, A., KUSAKABE, T., HORI, K. and KOGA, K. (1989) Flow of egg white ovalbumin into the yolk sac during embryogenesis. Biochimica et Biophysica Acta 992: 400–403.
   PubMed Web of Science ®Google Scholar
• TADTIYANANT, C., LYONS, J.J. and VANDEPOPULIERE, J.M. (1991) Influence of wet and dry feed on laying hens under heat stress. Poultry Science 70: 44–52.
   PubMed Web of Science ®Google Scholar
• TULLETT, S.G. and BURTON, F.G. (1982) Factors affecting the weight and water status of the chick at hatch. British Poultry Science 23: 361–369.
   Web of Science ®Google Scholar
• TULLETT, S.G. and DEEMING, D.C. (1987) Failure to turn eggs during incubation: effects on embryo weight, development of the chorioallantois and absorption of albumen. British Poultry Science 28: 239–243.
   PubMed Web of Science ®Google Scholar
• VARQUEZ-MONTERO, G., SARMIENTO-FRANCO, L., SANTOS-RICALDE, R. and SEGURA-CORREA, J. (2012) Egg production and quality under three housing systems in the tropics. Tropical Animal Health and Production 44: 201–204.
   PubMed Web of Science ®Google Scholar
• VIÑUELA, J. (1997) Adaptation vs. constraint: intraclutch egg-mass variation in birds. Journal of Animal Ecology 66: 781–792.
   Web of Science ®Google Scholar
• WALKER, L.A., WANG, T., XIN, H. and DOLDE, D. (2012) Supplementation of laying-hen feed with palm tocos and algae astaxanthin for egg yolk nutrient enrichment. Journal of Agricultural and Food Chemistry 60: 1989–1999.
   PubMed Web of Science ®Google Scholar
• WEATHERUP, S.T.C. and FOSTER, W.H. (1980) A description of the curve relating egg weight and age of hen. British Poultry Science 21: 511–519.
   Web of Science ®Google Scholar
• WILLEMS, E., WANG, Y., WILLEMSEN, H., LESUISSE, J., FRANSSENS, L., GUO, X., KOPPENOL, A., BUYSE, J., DECUYPERE, E. and EVERAERT, N. (2013) Partial albumen removal early during embryonic development of layer-type chickens has negative consequences on laying performance in adult life. Poultry Science 92: 1905–1915.
   PubMed Web of Science ®Google Scholar
• WILLIAMS, T.D., LANK, D.B., COOKE, F. and ROCKWELL, R.F. (1993) Fitness consequences of egg-size variation in the lesser snow goose. Oecologia 96: 331–338.
   PubMed Web of Science ®Google Scholar
• WILLIAMS, T.D. (1994) Intraspecific variation in egg size and egg composition in birds: effects on offspring fitness. Biology Reviews 68: 35–59.
   Web of Science ®Google Scholar
• WISE, R.W., KETTERER, B. and HANSE, I.A. (1964) Pre-albumins of embryonic chick plasma. Comparative Biochemistry and Physiology 12: 439–433.
   PubMed Web of Science ®Google Scholar
• WU, G., BRYANT, M.M., GUNAWARDANA, P. and ROLAND, D.A. Sr (2007) Effect of nutrient density on performance, egg components, egg solids, egg quality, and profits in eight commercial leghorn strains during phase one. Poultry Science 86: 691–697.
   PubMed Web of Science ®Google Scholar
• YASUMASU, S., MAO, K.M., SULTANA, F., SAKAGUCHI, H. and YOSHIZAKI, N. (2005) Cloning of a quail homologue of hatching enzyme: its conserved function and additional function in egg envelope digestion. Development Genes and Evolution 215: 489–498.
   PubMed Web of Science ®Google Scholar
• YOSHIZAKI, N., ITO, Y., HORI, H., SAITO, H. and IWASAWA, A. (2002) Absorption, transportation and digestion of egg white in quail embryos. Developmental Growth and Differentiation 44: 11–22.
   PubMed Web of Science ®Google Scholar