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Chapter 32 – the Physiology of the Avian Embryo

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Chapter 32 – the Physiology of the Avian Embryo Chapter 32 The Physiology of the Avian Embryo Casey A. Mueller, Warren W. Burggren and Hiroshi Tazawa Developmental and Integrative Biology, Department of Biological Science, University of North Texas, Denton, TX, USA ABBREVIATIONS Tegg egg temperature tc contact time of erythrocytes in chorioallantoic capillary with O2 A effective pore area p Vc capillary volume CAM chorioallantoic membrane − [HCO3 ] bicarbonate concentration CO cardiac output [La − ] lactate concentration CO2 carbon dioxide dCO2 carbon dioxide diffusion coefficient dH2O water vapor diffusion coefficient 32.1 INTRODUCTION dO2 oxygen diffusion coefficient The freshly laid avian egg contains most of the materials DO2 oxygen diffusing capacity needed for embryonic growth and development, but lacks EP external pipping the oxygen and heat needed for successful development. FcOX mean corpuscular oxygenation velocity Microscopic pores in the eggshell allow O2 to diffuse into GCO2 carbon dioxide conductance the egg from the environment and water vapor and CO pro- GH2O water vapor conductance 2 GO2 oxygen conductance duced by the embryo to diffuse out. The adult bird has a key Hb hemoglobin role in incubation, providing not only the heat necessary Hct hematocrit for embryonic development but also controlling the micro- HR heart rate climate of the egg. In the poultry industry and for research I incubation period purposes, the adult bird can be conveniently replaced by IHR instantaneous heart rate an incubator. The majority of research on avian incubation IP internal pipping is undertaken using artificially incubated chicken (Gallus IRR instantaneous respiratory rate gallus domesticus) eggs. Thus, in this chapter, the chicken L shell thickness embryo is used to elucidate the development of physi- MCO˙ 2 carbon dioxide elimination rate MHR mean heart rate ological function during avian incubation, supplemented by MH˙ 2O rate of water loss additional species when data are available. Developmental MO˙ 2 oxygen consumption rate physiology of the gas exchange, acid–base, cardiovascular, O2 oxygen osmoregulatory and thermoregulatory systems are exam- PaCO2 arterialized blood carbon dioxide partial pressure ined. The optimal conditions for artificial incubation are PaO2 arterialized blood oxygen partial pressure outlined and embryonic responses to incubation extremes PACO 2 airspace carbon dioxide partial pressure are described. PAO 2 airspace oxygen partial pressure PB atmospheric pressure PcO2 mean capillary oxygen partial pressure 32.2 THE FRESHLY LAID EGG PH O water vapor pressure 2 The mass of the freshly laid bird egg ranges from ∼0.8 g in PICO2 effective environmental carbon dioxide partial pressure the bee hummingbird (Mellisuga helenae) to 2 kg in the PIO effective environmental oxygen partial pressure ∼ 2 ostrich (Struthio camelus). The egg is composed of the egg- P arterial blood pressure a shell and outer and inner shell membranes that encompass Psys systolic blood pressure ˙ the albumen, which serves as a source of water and pro- Qa allantoic blood flow Q10 temperature coefficient tein; and yolk, a source of necessary nutrients. The com- R gas constant position of the freshly laid egg is related to the maturity of Ta ambient temperature the hatchling, which differs considerably between species. Sturkie’s Avian Physiology. Copyright © 2015 Elsevier Inc. All rights reserved. 739 740 PART | VI Reproductive Theme Hatchlings are divided into four major categories based on 32.3.2 Egg Water Content and Shell criteria such as mobility, amount of down, ability to feed, Conductance and locomotion. Precocial species are the most mature, and can walk, swim, or dive soon after hatching, while altri- As the embryo grows within the egg, water is lost and both cial species are the least mature and hatch naked, with the yolk and albumen diminish in mass. However, metabolic eyes closed and are incapable of coordinated locomotion. water is produced when fat in the yolk is oxidized. Part of Two intermediate categories—semi-precocial and semi- the water is inevitably lost by diffusion through the pores in altricial—describe species that are within these extremes. the shell to the microclimate of the egg. The rate of water ˙ The amount of yolk in the freshly laid egg is much greater loss MH2O , mg /day is determined by two factors: the water vapor conductance of the shell and shell membranes in precocial species than in altricial species (Sotherland ( ) and Rahn, 1987). The yolk is only 16% of egg mass in the (GH2O, mg/day/kPa) and the difference in water vapor altricial red-footed booby (Sula sula), while in the highly pressure between the contents of the egg and the environ- precocial kiwi (Apteryx australis) it is 69% of egg mass. ment (ΔPH2O, kPa) (Rahn and Ar, 1974): As most of the energy contained in the egg is in the lipid ˙ MH2O = GH2O ·ΔPH2O (32.3) fraction, most of which is in the yolk, the energy content of precocial eggs is higher than that of altricial eggs. Further- GH2O is a function of multiple factors, including shell more, most of the water in the egg is in the albumen, and as geometry (effective pore area, Ap, thickness of the shell the yolk/albumen ratio is lower in altricial than in precocial combined with shell membranes, L); water vapor diffusion eggs, altricial eggs have relatively higher water compared coefficient (dH2O); and the inverse product of the gas con- with precocial eggs (Sotherland and Rahn, 1987). stant (R) and absolute temperature (T): GH2O = [(Ap/L) · dH2O] /RT (32.4) 32.3 INCUBATION Both pore area and shell thickness increase in larger eggs (Ar et al., 1974). Although an increase in pore area increases 32.3.1 Incubation Period GH2O, an increase in shell thickness has the opposite effect, Incubation encompasses the prenatal period, prior to “inter- because it lengthens the diffusion pathway for water vapor. nal pipping” (IP), when the embryo penetrates its beak The water lost from the egg is replaced by air, enlarging through the chorioallantoic and inner shell membranes into the air cell at the blunt pole of the egg during develop- the air cell; and the perinatal or paranatal period from IP ment. Upon IP and EP, the rate of water loss from the egg to when the embryo fractures the shell (“external pipping,” increases, as water vapor can diffuse through the cracks EP) and hatches. The incubation period (I, days) increases (pip-hole) in the shell. The water loss from the egg over the with egg size and can be represented as follows: entire incubation period amounts to ∼18% of the mass of 0.22 the freshly laid egg. I = 12 · (Egg mass) (32.1) where egg mass is in g (Rahn and Ar, 1974). In addition, as a first approximation, the product of incubation period and 32.3.3 Heat Transfer O2 consumption MO˙ 2 at the stage where MO˙ 2 remains Many adult birds (typically but not always the female) play unchanged (i.e., plateau) is proportional to egg mass (Rahn an important role in incubation of their eggs, by using their et al., 1974): ( ) body and nesting material to alter the environment of the eggs. Most birds develop a seasonal bare patch of skin, I MO˙ c (Egg mass) (32.2) · 2 = · the brood patch, on part of the thorax and abdomen. This where c is a constant. Thus, for a given egg mass an egg that directly contacts with the eggs, permitting a greater rate of consumes less O2 at the plateau stage needs a longer incu- heat transfer than if the patch were covered with plumage. bation period. Furthermore, because the MO˙ 2 at the plateau Accompanying the loss of feathers is an increase in the size stage is matched to the shell gas conductance, for a given and number of blood vessels in the bare skin. The adult can egg mass an egg with lower shell conductance requires a adjust the rate of heat transfer to the egg by standing over longer incubation period. or leaving the vicinity of the egg, but also by the closeness Apart from these general trends, eggs that are left unat- with which the bird applies its patch to the egg. The bird tended by the incubating parent for a period of time will exhibit responds physiologically to variations in egg temperature cooling, and this results in slower embryonic growth and a lon- (Tegg), increasing its metabolic heat production in response ger incubation period. Some birds, notably tropical seabirds to cooling of the egg (Tøien et al., 1986; Rahn, 1991). and petrels (Procellariiformes), have much longer incuba- The amount of heat transferred to the eggs is directly tion periods than that suggested by the general relationship proportional to the increase in heat production (Tøien et al., (Whittow, 1980), even though they are incubated continuously. 1986). The efficiency of heat transfer to the eggs diminishes Chapter | 32 The Physiology of the Avian Embryo 741 with decreasing ambient temperature and clutch size. Heat end of incubation, the embryo uses energy for active con- stored in the incubating bird while flying and foraging (i.e., trol of body temperature and hatching. Prior to this, it is while not incubating the eggs) can be transferred to the eggs assumed that prenatal MO˙ 2 is used for maintenance, which on return to the nest (Biebach, 1986). If the egg is very cold, is proportional to body mass, and for growth, which is pro- “cold vasodilation” occurs in the brood patch, increasing the portional to growth rate (GR = ΔBody mass/time) as follows patch blood flow and temperature and therefore heat trans- (Vleck et al., 1980; Mortola and Cooney, 2008): fer to the egg (Mitgard et al., 1985). The brood patch tem- MO˙ a (Body mass) b GR (32.6) perature varies from 34.9 °C in the bonin petrel (Pterodroma 2 = · + · hypoleuca) to 42.4 °C in the dusky flycatcher (Empidonax where coefficients a and b express the daily average cost oberholseri).
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