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Nutrition of the Developing Embryo and Hatchling¹

Department of Poultry Science, Auburn University, AL 36849

² Corresponding author: moranet{at}auburn.edu

	ABSTRACT

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Nutrient needs central to satisfactory egg incubation well-being undergo several major changes from fertilization until the reliance of the chick on feed. Glucose is central, with the initiation of incubation until the chorioallantois accesses O₂ to use for fatty acid oxidation. Nutrient recovery from albumen and yolk is largely commensurate with body assembly through to completion of the embryo by 14 d. Remaining albumen mixes with the amniotic fluid and is orally consumed until initiation of emergence. A portion of the albumen is absorbed by the small intestine to expand body glycogen reserves. The residual not absorbed contains digestive enzyme contributions and enters the yolk sac through its stalk at the jejunum and ileum. Interaction of the albumen-amnion digestive enzyme mixture with yolk sac contents leads to diverse alterations that influence subsequent use of lipids. Rapid removal of very low-density lipoprotein ensues, until pipping with triglycerides, expanding body fat depots while cholesterol deposits in the liver. A concurrent translocation of Ca from shell mineralizes the skeletal system while also crossing yolk sac villi for deposition on phosvitin-based granules accruing in its lumen. Loss of chorioallantois with pipping and the start of pulmonary respiration predispose a dependence on glycolysis to support emergence. Small intestinal villi progressively reorient their enterocytes from macromolecule transfer to competence at digestion and absorption after hatching. Mobilization of body fat complements contributions from the yolk sac to provide fatty acids for generating energy, heat, and water while also combining with hepatic cholesterol for membrane expansion and continued development. Calcified granules evacuate the yolk sac to further skeletal mineralization in the absence of shell contributions. Egg mass, its interior quality, and turning during early incubation directly influence the ability of the embryo to access nutrients and provide resources to support emergence and the transition of the chick to self-sufficiency.

Key Words: albumen • embryo nutrition • incubation • yolk sac

	INTRODUCTION

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Feeding essential nutrients to the hen must be followed with their placement in the egg (Wilson, 1997). Then, a synchronized progression of events ensues to ultimately realize a viable chick. Access to O₂, diversified energy sourcing, accommodating metabolic patterns, and emphasis at mineralization are particularly important and may be dramatically altered with each event. Their importance is emphasized by an accentuation of deaths at each transition to emphasize the magnitude of changes. Essentially, the germ is established during the first third of incubation, and completion of the embryo form follows through the second third. Preparation for emergence and actual hatching become the objectives during the final third. Finally, establishing an independent chick depends on embryonic reserves in place to fuel its transition to feed. Considerable poetic license has been taken to assemble a multitude of isolated research observations into a holistic view of embryo and hatchling nutrition. Providing a multidisciplinary model rationalizes existing strategies known to improve hatchability and subsequent chick performance.

	ESTABLISH GERM

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Germ development is initiated with ovum fertilization in the infundibulum of the hen and continues with incubation of the subsequent egg. Nutrients initially supporting of the germ are recovered from adjacent yolk (Tezuka et al., 1974; Litke and Low, 1975; Lemanski and Aldoroty, 1977) and albumen (Deeming, 1989a) by an expanding vascular system (Ribatti, 1995). Although a germ vascular system is visually apparent with candling shortly after incubation, O₂ access is limited to simple diffusion aided by a primitive hemoglobin (Cirotto and Arangi, 1989; Baumann and Meuer, 1992). Energy expended at this time largely arises by glycolysis of accessible glucose, and a transient increase of lactic acid occurs until the chorioallantois becomes functional (Kucera et al., 1984). Glucose in albumen appears to be largely recovered from the outer thin and put in place during uterine plumping before shell formation. Simplistically, invagination during early development of the germ leads to the chorionic sac and allantoic cavity. In turn, their membranes eventually converge at the shell to favor distribution at the air-cell end of the egg (Sethi and Brookes, 1971; Fancsi and Feher, 1979). Vascular development adjacent to these membranes enables a rapid exchange of CO₂ and O₂ with shell air pores (Tazawa and Ono, 1974; Lomholt, 1976; Tullety and Board, 1976). Access to O₂ fully supports complete combustion of fatty acids, used as the primary source of energy and the basis for embryo development.

Albumen structure is a dominant factor to the successful transition of the germ from anaerobic to aerobic metabolism (Christensen, 2001). Essentially, the chalaza, along with thick albumen, restricts ovum movement to rotation within the inner thin of the egg (Tullet and Deeming, 1987; Deeming, 1989b). Extensive lipid content encourages the yolk to rise within this aqueous system such that chorion and amnion membranes favor juxtaposition at the inner eggshell membrane while improving survival by proximity to glucose in the outer thin. Although differential pressure treatment of turkey eggs before incubation can be used to increase egg glucose content, Moran and Reinhart (1981) did not observe a relief in dead-germ loss as much as increased poult weight. Frequent egg turning by the hen throughout early incubation fosters a uniformly distributed chorioallantois through the top half of the egg while continuing glucose access from the outer thin. Success of this transition is substantially dependent on albumen integrity. Long holding, poor holding, or both conditions before incubation not only impair formation of a fully functional chorioallantois but adversely define the albumen sac that concurrently forms at the small end and recovery of its nutrients (Hall and Van Wagenen, 1936; Christensen et al., 2001; Tona et al., 2005).

	EMBRYO COMPLETION

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The vascular system is fully developed shortly after the chorioallantois is complete to assure O₂-CO₂ exchange (Levinsohn et al., 1984). In turn, fatty acid use represents the most favorable energy source for completion of the embryo in its final form (Sato et al., 2006). A continuous low respiratory quotient infers that carbohydrate is being conserved to the extent that ketone body accumulation does not occur. Not only is adenosine triphosphatase provided in major amounts as the driver of synthetic processes, but major amounts of by-product heat and water also evolve in support of incubation (Whittow and Tarazawa, 1991). An increased proportion of the essential fatty acids appearing in egg contents with the progression of incubation indicates their devotion to membrane formation in embryonic assembly while saturates with their greater caloric value are consumed (Donaldson, 1964; Maldjian et al., 1995; Murray et al., 1999; Speake et al., 2003; Speake and Deans, 2004). Nutritional deficiencies imposed on the breeder during egg formation may have repercussions at any time, but embryonic deaths during this interval usually relate to marginal breeder feed inadequacies. Inadequacies of pantothenic acid and riboflavin may occur in practice, and accentuated deaths at 12 d of incubation together with clubbed down are observed. Although the embryo is structurally complete by 14 d of incubation, providing the wherewithal to support the transition to an independent chick in the last 7 d is very demanding as well.

	PREPARATIONS FOR EMERGENCE

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Embryo expansion within the amniotic sac together with its physical movements initiate preparations for emergence. Albumen previously compartmentalized at the small end of the egg has its seroamniotic connection rupture (Feher, 1984). Free albumen can now enter the amniotic sac and form a composite of both contents. Pressure differential created by a continuing embryonic growth enhances an oral consumption of this mixture that passes through the gastrointestinal system (Oegema and Jourdian, 1974; Sugimoto et al., 1999). Partial absorption of proteins from the albumen-amniotic mixture occurs by enterocytes capable of macromolecular absorption during transit through the duodenum and jejunum. Antitrypsin factors strongly inhibit digestion, even though a full complement of pancreatic enzymes is present (Holdsworth and Wilson, 1967; Marchaim and Kulka, 1967; Yoshizaki et al., 2002). Albumen, together with the pancreatic enzyme composite, enters the yolk sac through its stalk with the aid of antiperistaltic activity of the colon (Sugimoto et al., 1989; Bryk and Gheri, 1990). Recovery of macromolecules during passage through the duodenum and jejunum is parallel to that of colostrums with postparturient mammals. Chick embryonic villi also have unique enterocytes that are capable of fluid and macromolecular transfer to greatly expand the vascular system with the appearance of albumen proteins. Such consumption and absorption is continuous until the albumen-amniotic fluid disappears and internal pipping begins. Ovomucoid is a prominent albumen protein that appears in blood and continues to be detectable after hatching. This protein is one of several in albumen that has extensive amounts of carbohydrate. Gluconeogenesis from albumen proteins focuses on using the inherent carbohydrate to form glycogen while conserving amino acids per se for protein synthesis (Scott et al., 1981; Muramatsu et al., 1990). As a result, blood glucose progressively increases to support escalating liver and muscle glycogen deposition.

Residual albumen-allantoic fluid entering the yolk continues to express digestive enzymes released en route through the gastric and small intestinal systems (Bainter and Feher, 1974; Sugimoto et al., 1978; Sugimoto and Yamada, 1986a,b; Ikeno and Ikeno, 1991). Ovomucoid is known to strongly inhibit trypsin; however, subsequent encounters of the enzyme composite with lipoproteins in the yolk sac appear to foster major molecular changes. The yolk sac has villi that expand surface area in parallel to the intestine (Holdsworth and Wilson, 1967). Similarly, core vessels have an extensive vascular system to facilitate exchange dynamics; however, yolk sac cells on villi use receptor-mediated endocytosis to absorb intact very low density lipoproteins (VLDL) rather than transport digestion products (Lambson, 1970; Noble et al., 1988). These cells also have a diverse array of enzymes capable of altering the absorbed lipid before release into circulation (Kusuhara and Ishida, 1974; Powell et al., 2004). Very low-density lipoprotein uptake by the yolk sac becomes greatly accentuated beyond simple needs once the albumen-allantoic digestive enzyme composite is encountered (Speake et al., 1992). Specialized depots that develop in many subdermal locations of the embryo accept this additional transfer of triglycerides, whereas associated cholesterol preferentially locates in the liver to exaggerate its size and create a distinctive light yellow appearance (McGreal, 1956; Langslow and Lewis, 1972; Speake et al., 1998; Peebles et al., 1999).

Phosvitin and lipovitellin are yolk high-density lipoproteins formed from vitellogenin during transfer through the ovum wall. Associated changes lead to molecular rearrangement into granules that aggregate into spheres apart from the aqueous dispersion of VLDL. Concurrent with entry of albumen-allantoic fluid enzymes in the yolk sac, sphere appearance changes from an accrual of granules to a lamination of layers from surface to core (Cheville and Coignoul, 1984). Phosvitin has a large amount of phosphate esterified to serine (Shainkin and Perlmann, 1971a,b; Perlmann, 1973), and lamination appears to enable to direct exposure of large amounts of these phosphates at the surface. Calcium can be transferred through yolk sac villi from its vascular system to adhere to the surface of the sphere. Calcified granules are not absorbed but accrue within the confines of the yolk sac until pipping.

Calcium in circulation increases dramatically, concurrent with the transfer of VLDL from the yolk sac to embryo depots and sphere calcification. Dissolution of mammary knobs adjacent to the chorioallantois-shell membrane interface represents the dominant source of blood Ca (Bond et al., 1988; Dieckert et al., 1989; Abdel-Salam et al., 2006). Exchange of CO₂ in conjunction with carbonic anhydrase creates acid conditions for the dissolution of the shell and transfer of Ca to circulation (Narbaitz, 1974; Tuan, 1984, 1987; Tuan and Ono, 1986). Calcium so recovered not only calcifies yolk sac spheres but has the intention of concurrently mineralizing a developing skeleton that was previously cartilage (Roufosse, 1979).

	IMPLEMENTING RESOURCES FOR EMERGENCE

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Internal pipping initiates emergence by piercing the chorioallantois and inner shell membrane at the air cell periphery. Loss of ready O₂ access necessitates a concurrent transition to pulmonary respiration, because the outer shell membrane and shell are progressively circumscribed (Vince, 1976; Menna and Mortola, 2002; Villamor et al., 2002). Essentially, shell piercing by the beak is driven by the hatching muscle as facilitated by the egg "tooth" of the beak and body rotation (Bakhuis, 1974; Feher, 1988). Hatching muscle fibers are exclusively anaerobic, very well provided with glycogen, and have a special nervous system for coordination (Fazekas et al., 1985; Gross, 1985; John et al., 1987). Maximum vascularization at the air cell-shell interface also lead to shell areas weakened during the 14 to 19 d of accentuated Ca recovery commensurate with areas fractured (Waters, 1935).

Cessation of shell Ca access with chorioallantois destruction initiates the recovery of Ca phosphate high-density lipoprotein spheres from the yolk sac (Cheville and Coignoul, 1984). Transition from sourcing Ca at the shell to both Ca and P in the yolk sac provides a continued mineralization and skeletal development through to feed dependence. Continual skeletal reinforcement is paramount to supporting body emergence from the shell and subsequent locomotion (Pageze et al., 1996). Sphere CaP access largely diminishes within 3 to 4 d after hatch with yolk sac depletion, and its amount likely influences early feed macromineral requirements. Hen dietary P seems to influence vitellogenin formation and sphere levels during ovum formation. Small egg mass may be of substantial influence in this respect (El Boushy, 1979a,b; Triyuwanta et al., 1992).

The physical demands of emergence are extensive when O₂ availability is marginal (Tazawa et al., 1983). Muscles most active at this time exclusively use glycolysis from glucose provided from glycogen reserves (Freeman, 1969). The transient increase of lactic acid occurring at this time disappears once pulmonary functioning provides adequate O₂ for fatty acid catabolism to resume as a source of energy (Garcia et al., 1986; Hoiby et al., 1987). Although respiratory quotient indicates that fatty acid oxidation dominates energy production once emergence is complete, access to glucose remains important to fully combust fatty acids without ketone body accumulation (Best, 1966; Beis, 1985; Ohtsu et al., 2003). By-product heat from fatty acid combustion is substantial and assists in transition of the neonate from being a poikilotherm to homeothermy, whereas the associated production of water production minimizes dehydration until external sources become available.

Although yolk sac lipoproteins continue to be an important nutrient source at this time (Romanoff, 1944; Noble and Ogunyemi, 1989; Castillo et al., 1992; Murakami et al., 1992; Nir and Levanon, 1993; Ding and Lilburn, 1996; Puvadolpirod et al., 1997), fatty acid recovery from preformed body depots appears to dominate (Langslow, 1972) given the minimal repercussion of deutectomy (Harvey et al., 1955; Baranyiova, 1972; Baranyiova and Standara, 1980). Extensive hepatic cholesterol in place at hatch rapidly dissipates along with the depots (Svanberg, 1971; Baranyiova and Holman, 1972; Tarugi et al., 1994). Immediate access to cholesterol appears to relieve its synthesis. Cholesterol, together with depot essential fatty acids, enables continued membrane formation and growth. A high concurrent demand for glucose appears to reside with its need to support growth of glycolytic muscle (Baranyiova and Holub, 1977; Latour et al., 1995, 1996; Uni et al., 2005). End-product pyruvic acid (Ala) recycles for regeneration in the liver using fatty acid energy.

	TRANSITION TO FEED

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The gastrointestinal system must assume responsibility for nutrition of the chick as reserves originating from the egg deplete (Jin et al., 1998; Vieira and Moran, 1999). Enterocytes in place with the villi of the embryo are intended for macromolecular transfer; however, those arising from the crypts shortly replace embryonic ones to provide competence at digestion-absorption (Uni et al., 1998, 2003a,Uni et al., b). A mosaic of both type of enterocytes exists at emergence, and another several days must ensue before effective feed utilization is possible (Raheja et al., 1977; Sulistiyanto et al., 1999; Batal and Parsons, 2002; Sklan, 2003). Essentially, the entire surface makes this transition within 2 wk, and all remnants of the embryonic population are extruded. Growth of the mucosa through this period almost exclusively represents villi, and the increased appearance of enzymes that finalize digestion correspond to surface maturation (Baranyiova and Holman, 1976; Noy and Sklan, 1995; Uni et al., 1995; Chotinsky et al., 2001; Iji et al., 2001). Loss of yolk sac, disappearance of subdermal depots, and resumption of liver color must be in phase with the ability of the gastrointestinal system to recover nutrients from feed. Most starveouts fail to make the transition and commonly maximize around 3 to 4 d posthatch. The multitude of strategies that provide early nutrition to either an embryo or postemergent chick provide an advantage to this transition, thereby improving performance (Baranyiova, 1987; Noy and Pinchasov, 1993; Ohta et al., 1999; Tako et al., 2004; Foye et al., 2006a,b).

	OVERVIEW

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A holistic view of embryo and hatchling nutrition indicates a central role for carbohydrate, fatty acids, and Ca and P. Transient access to O₂ until establishment of the germ and again during emergence of the chick favors anaerobic catabolism of glucose for energy. Internal egg quality and turning during early incubation are mutually necessary for favorable formation of the chorioallantois and compartmentalizing remaining albumen. Effective retrieval of O₂ enables fatty acid oxidation to dominate energy production during the interim until emergence and immediately after its completion. Oral consumption of albumen once the embryo is formed and partial absorption of the protein provides for gluconeogenesis and storage of glycogen to fuel emergence. Remaining albumen together with digestive enzymes enter the yolk sac to facilitate other changes. Yolk VLDL are rapidly absorbed to expand body depots while cholesterol accrues in the liver. Transfer of Ca from the eggshell periphery weakens these areas for pipping. Part of this Ca mineralizes the skeleton, whereas a significant amount is also transferred onto phosvitin-based platelets in the yolk sac. Calcium phosphate platelets provide continued skeletal mineralization after loss of the chorioallantois. Upon hatching, enterocytes competent at food assimilation subsequently cover the surface of the intestine. Body depots and hepatic cholesterol in the posthatch chick are recalled as the yolk sac depletes and provide continued body development during the transition to self-sufficiency.

	FOOTNOTES

 
¹ Presented as part of the Embryo Symposium: Managing the Embryo for Performance, July 19, 2006, at the Poultry Science Association Annual Meeting, Edmonton, Alberta, Canada.

Received for publication November 13, 2006. Accepted for publication November 19, 2006.

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