Hostname: page-component-586b7cd67f-t8hqh Total loading time: 0 Render date: 2024-11-23T04:28:06.313Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  29 August 2014

E. WILLEMS ,
E. DECUYPERE ,
J. BUYSE  and
N. EVERAERT
E. WILLEMS
Affiliation:
Laboratory of Livestock Physiology, Department of Biosystems, KU Leuven, Kasteelpark Arenberg 30 box 2456, 3001 Leuven, Belgium
E. DECUYPERE
Affiliation:
Laboratory of Livestock Physiology, Department of Biosystems, KU Leuven, Kasteelpark Arenberg 30 box 2456, 3001 Leuven, Belgium
J. BUYSE*
Affiliation:
Laboratory of Livestock Physiology, Department of Biosystems, KU Leuven, Kasteelpark Arenberg 30 box 2456, 3001 Leuven, Belgium
N. EVERAERT
Affiliation:
Laboratory of Livestock Physiology, Department of Biosystems, KU Leuven, Kasteelpark Arenberg 30 box 2456, 3001 Leuven, Belgium University of Liège, Gembloux Agro-Bio Tech, Animal Science Unit, Passage des Déportés 2, 5030, Gembloux, Belgium
*
Corresponding author: [email protected]
Get access

Abstract

Depending on the bird species, about 33-86% of the egg content consists of albumen. In eggs from domestic fowl, albumen contains about 10.5% protein and 88.5% of water and may be regarded as the main water source for the developing embryo. Besides carbohydrates, lipids, and inorganic ions, over 90% of the solids in the albumen are proteins. Several factors are known to influence the amount and composition of the albumen: egg weight, age and genetics of the parent flock, amount and quality of the feed provided, environmental factors (e.g. temperature, light), position in laying sequence, and also storage conditions of eggs prior to incubation. The albumen content of an egg plays an important role during embryonic development. Not only for formation of sub-embryonic fluid, but albumen proteins are known to flow into the amniotic cavity, the yolk sac and finally the digestive tract of the embryo and are used as the main source of proteins for tissue synthesis. Partial removal of albumen had negative consequences on chick weight at hatch, reduced the amount of amniotic and allantoic fluid and may reduce the water content of the chick and the residual yolk. Replacing the removed albumen with saline, however, reduced the residual yolk weight without differences in water content, suggesting increased uptake and utilisation of yolk, possibly as a compensation for the removed albumen proteins. In addition to reduced chick weight at hatch, some authors report an asymmetric growth restriction where nutrients are diverted away from non-vital organs in favour of brain and heart, with a relative ‘sparing’ of these latter two organs. Partial albumen removal led to a reduced whole-body protein synthesis, similar to eggs containing naturally less albumen. Importantly, several studies reported some long-term effects of albumen removal on growth, indicating that prenatal environment will have life-long consequences.

Keywords

albumenalbumen compositionproteineggembryonic developmentalbumen removalaviandomestic chicken
Type
Review Article
Information
World's Poultry Science Journal , Volume 70 , Issue 3 , September 2014 , pp. 503 - 518
Copyright
Copyright © World's Poultry Science Association 2014 

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

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.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.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.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.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.CrossRefGoogle ScholarPubMed
BOARD, R.G. (1966) The course of microbial infection of the hen's egg. Journal of Applied Bacteriology 29: 319-341.Google Scholar
BOARD, R.G. and FULLER, R. (1974) Non-specific antimicrobial defenses of the avian egg, embryo, and neonate. Biological Reviews 49: 15-49.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.CrossRefGoogle 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.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.CrossRefGoogle Scholar
CARINCI, P. and MANZOLI-GUIDOTTI, L. (1968) Albumen absorption during chick embryogenesis. Journal of Embryology and Experimental Morphology 20: 107-118.Google 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.Google Scholar
CHRISTIANS, J.K. (2002) Avian egg size: variation within species and inflexibility within individuals. Biological Reviews 77: 1-26.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.Google Scholar
DEEMING, D.C. (1989a) Characteristics of unturned eggs: critical period, retarded embryonic growth and poor albumen utilisation. British Poultry Science 30: 239-249.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.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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.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.Google Scholar
FISHER, C. (1969) The effects of a protein deficiency on egg composition. British Poultry Science 10: 149-154.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.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.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.CrossRefGoogle ScholarPubMed
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.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.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.Google Scholar
HILL, W.L. (1993) Importance of prenatal nutrition to the development of a precocial chick. Developmental Psychobiology 26: 237-249.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.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.CrossRefGoogle ScholarPubMed
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.Google Scholar
KRAMER, T.T. and CHO, H.C. (1970) Transfer of immunoglobulins and antibodies in the hen's egg. Immunology 19: 157-167.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.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.Google Scholar
MANN, K. (2007) The chicken egg white proteome. Proteomics 7: 3558-3568.CrossRefGoogle ScholarPubMed
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.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.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.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.Google Scholar
MORAN, E.T. Jr (2007) Nutrition of the developing embryo and hatchling. Poultry Science 86: 1043-1049.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.Google Scholar
NABER, E.C. (1979) The effect of nutrition on the composition of eggs. Poultry Science 58: 518-528.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.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.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.CrossRefGoogle ScholarPubMed
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.Google Scholar
PARSONS, J. (1976) Factors determining the number and size of eggs laid by the Herring Gull. Condor 78: 481-492.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.Google Scholar
RICKLEFS, R.E. (1984) Variation in the size and composition of eggs of the European Starling. Condor 86: 1-6.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.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.CrossRefGoogle ScholarPubMed
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.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.CrossRefGoogle ScholarPubMed
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.Google 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.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.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.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.CrossRefGoogle ScholarPubMed
SIMKISS, K. (1980) Eggshell porosity and the water metabolism of the chick embryo. Journal of Zoology London 192: 1-8.Google Scholar
SOTHERLAND, P.R. and RAHN, H. (1987) On the composition of bird eggs. Condor 89: 48-65.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.Google 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.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.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.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.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.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.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.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.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.Google Scholar
VIÑUELA, J. (1997) Adaptation vs. constraint: intraclutch egg-mass variation in birds. Journal of Animal Ecology 66: 781-792.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.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.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.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.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.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.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.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.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.Google Scholar