Charles V. Paganelli

The Avian Egg: Water Vapor Conductance, Shell Thickness, and Functional Pore Area

Gas exchange in the avian embryo has been shown to be dependent on, and limited by, the diffusive properties of gases across the resistance offered by the shell and shell membranes ( Wangensteen and Rahn 1970-71). For simplicity, we shall use the term “shell’ to denote the entire barrier to diffusion between the interior of the egg and the environment. It has also been shown that under normal conditions the diffusion of water vapor across the egg shell approximates the diffusion equations set forth for ideal gases (Paganelli et al. 1971) and that the weight loss in eggs is almost entirely due to diffusion of water through the shell (Romanoff and Romanoff 1949). The diffusive rate of water loss from eggs is:

Relation of Avian Egg Weight to Body Weight

JUST over 50 years ago Heinroth (1922) published the first extensive list of egg weights and adult body weights for 427 species of birds. Since then additional data have appeared and the most extensive list can now be found in Schonwetters (1960-72) monumental description of bird eggs. With these as a major backlog, and data for the Fringillidae (Amadon 1943); the Sphenisciformes, Anseriformes, and Procellariiformes (Lack 1968); and Falconiformes (Mebs 1964), more than 800 egg weightbody weight correlates are now available. Our endeavor has been to describe the relationship between egg weight and body weight in mathematical terms that are amenable to further refinements when additional data became available. We have not been concerned with explaining the relationship as Lack (1968) has done in his elegant analysis, but have rather attempted to find out what common principles might emerge from this particular relationship. Our analytical approach is basically the same as suggested originally by Huxley (1923-24), namely to plot log (egg weight) against log (body weight) and to derive a regression equation that expresses egg weight, W, as a function of body weight, B, raised to a power: W = aBb. The additional data now available allow one to obtain individual regression equations for many orders and families. As Amadon (1943) had anticipated in his review of Huxleys analysis and as Lack (1968) has recently shown for many orders and families, each group of related birds has its characteristic proportionality constant, a. On the other hand, our analysis indicates that the power, b, is most likely the same for all groups, inamely 0.675. In addition, the relation of incubation time to body weight is derived (Rahn and Ar 1974); incubation time is shown to be proportional to body weight raised to the 0.166 power. Thus a 10-fold increase in body weight is in general associated with a 4.73-fold increase in egg weight and a 1.47-fold increase in incubation time.

The Avian Egg: Surface Area, Volume, and Density

The surface area of the avian egg through which the developing embryo must exchange heat, metabolic gases, and water vapor is a variable of prime importance for quantitation of the permeability of the egg shell to these substances. Surface-area measurements are necessary if one is to compare the permeability properties of shells ranging in size from less than 0.5 g in hummingbirds, to 1.5 kg in the Ostrich (Struthio camelus), and to more than 10 kg in the extinct Aepyornis. In the course of experiments designed to measure and compare the water vapor permeability of eggs of many species (Ar et al. 1974), we found it necessary to develop a method of measuring surface area that was both convenient and accurate.

The avian egg: air-cell gas tension, metabolism and incubation time

Abstract The O 2 and CO 2 tensions in the air cell of incubating eggs just pripr to the pipping stage were analyzed in nine species of birds. These appear to be very similar and average 104 and 37 torr, respectively, for O 2 and CO 2 . The oxygen conductance of the egg shell for each species was calculated from the water vapor conductance previously established, which allows one to calculate the oxygen consumption of the egg as the product of O 2 conductance and ΔP O 2 , across the egg shell. The oxygen uptake of the eggs at this stage of development is proportional to the egg weight raised to the power O.78. A previously derived relationship shows that the incubation time is proportional to the egg weight raised to the power O.22. Combining these two weight functions, one obtains a general relationship between metabolic rate and incubation time; namely in different species of birds that have the same egg weight the natural incubation period is inversely related to the metabolic rate or the egg shell gas conductance.

The Avian Egg: Mass and Strength

In a series of recent works, attention has been paid to the functional properties of the avian eggshell: water vapor and respiratory gas conductances, water loss, metabolic rate and incubation time-all these major physiological characteristics of eggs may be closely and intimately related to egg mass, which, in turn, is allometrically related to eggshell structural properties such as thickness, porosity, mass, density and surface area (Wangensteen 1972, Ar et al. 1974, Rahn and Ar 1974, Paganelli et al. 1974, Rahn et al. 1974, Ar and Rahn 1978). These structural and functional relations of bird eggs reveal some variables of importance to the physiology of the embryo, including the gradient in water vapor pressure between egg and nest, the fractional water loss constant, the constancy of gas composition in the air cell, and total oxygen consumption per gram egg during incubation. The ability to hatch successfully is the outcome of a delicate equilibrium among several factors, some of which are inherited in the structure and function of the egg itself, while others are either imposed on the egg by the environment or controlled by the incubating parents. The eggshell provides the egg with an external “skeletal” support that utilizes the dome principle to obtain strength with economy in building material and without need for internal supporting posts. It must satisfy conflicting demands: On the one hand, it must be strong enough to support the incubating bird’ s mass plus the egg’ s own mass and to protect and prevent it from being crushed during incubation. On the other hand, it must not be too strong for the hatchling to break its way out, a problem that may become crucial in bigger eggs where shell thickness increases and the specific metabolic rate of the embryo decreases (Paganelli et al. 1974, Rahn et al. 1974). The ratio of total shell pore area to shell thickness is largely evolved to meet the forthcoming metabolic demands of the growing embryo, which in turn, are a function of mass (Ar et al. 1974). Adding to this the belief that any saving in building material should benefit the laying bird, we hypothesize that eggshell strength should be related to egg mass. Eggshells have been subjected to numerous strength tests in the past. They have been crushed, cracked, pierced, snapped, compressed, bent and deformed in various ways. Force has been applied inwards and outwards, on whole eggs and on pieces of shells. Various methods and instrumentations have been used (Brooks 1960, Tyler and Geake 1963, 1964, Tyler and Coundon 1965, Tyler and Thomas 1966, Carter 1971, Scott et al. 1971). However, most of these studies were designed to establish practical “quality” criteria as they are understood by the poultry industry (Petersen 1965). As a result, most of the research has been concentrated on domestic hen (Gallus domesticus) eggs and little has been published on other species (Romanoff and Romanoff 1949, Brooks 1960, Tyler 1969a, Radcliffe 1970, Peakall et al. 1973). Strength has been correlated with factors such as calcium diet, diet in general, insecticides, shell microstructure, specific gravity, incubation period and shape index (e.g., Sluka et al. 1967, Wells 1967a, b, Vanderstoep and Richards 1969, Connor and Arnold 1972, King and Robinson 1972, Cooke 1973, Carter 1976). However, Tyler (196913) clearly demonstrated that the main factor affecting strength in hen eggs is shell thickness, where strength is a function of shell thickness squared. It is our purpose here to describe how egg strength scales with mass. We do not try to explain the relationship, but rather attempt to define the common principles that emerge from this relationship.

Regulation of Incubation Water Loss in Eggs of Seven Species of Terns

Water loss during incubation in the eggs of seven species of terns are reported. The nesting sites ranged from a relatively cold region, southern Alaska, to a tropical climate in the equatorial Pacific Ocean. In addition, measurements of various physical parameters of the eggs and eggshells were made, including the water-vapor conductance of the fresh egg, which allows one to calculate the total effective pore area of the shell. The rate of water loss during incubation was proportional to egg weight (9-39 g) but inversely proportional to incubation period (21-36 days); the eggs of all species lost about the same fractional amount of water, namely, 14% of their initial weight. The rate of water loss is determined by a species-specific water-vapor conductance or pore geometry of the shell, provided that a water-vapor pressure difference of about 27 torr is maintained between the egg and the microenvironment of the nest. Since water-vapor pressure in the incubating egg is determined by egg temperature and is about 47 torr, the microclimate of the nest must be maintained at a vapor pressure of about 20 torr. Therefore, the bird must achieve a nest ventilation which is a function of the water loss of the egg and brood patch and the difference between the water-vapor content of the ambient air and that in the microclimate of the nest.

The Avian Egg: In vivo Conductances to Oxygen, Carbon Dioxide, and Water Vapor in Late Development

In vivo measurements of both O2 and water vapor conductances(\({\text{G}}_{{\text{O}}_{\text{2}} }\) and \({\text{G}}_{{\text{H}}_{\text{2}} {\text{O}}} \)) were made at 38°C on the same hen’s eggs between days 12 and 18 of incubation. Neither \({\text{G}}_{{\text{O}}_{\text{2}} }\) or \({\text{G}}_{{\text{H}}_{\text{2}} {\text{O}}}\) changed systematically during this phase of incubation. Average \({\text{G}}_{{\text{O}}_{\text{2}} }\) (cm3/day/torr) was 12.60 ± 0.30 (S.D.); average \({\text{G}}_{{\text{H}}_{\text{2}} {\text{O}}}\), 15.26 ± 0.51; \({\text{G}}_{{\text{O}}_{\text{2}} } \)/\({\text{G}}_{{\text{H}}_{\text{2}} {\text{O}}} \)= 0.83. In vivo determination of \( {\text{G}}_{{\text{CO}}_{\text{2}} } \) and \({\text{G}}_{{\text{H}}_{\text{2}} {\text{O}}} \) in a second group of eggs gave values of 9.22 ± 1.54 and 14.60 ± 0.65, respectively; \({\text{G}}_{{\text{CO}}_{\text{2}} }\)/\({\text{G}}_{{\text{H}}_{\text{2}} {\text{O}}}\)= 0.64. The conductance ratios agree closely with the binary diffusivity ratios (in air or N2) of the gases in question. We conclude that O2, CO2, and water vapor diffuse between environment and air cell of the chicken egg via the same diffusion path, whose chief resistance lies in the shell itself. The outer shell membrane offers little resistance in vivo to passage of gas molecules.

HUMIDITY IN THE AVIAN NEST AND EGG WATER LOSS DURING INCUBATION

An egg diffusion hygrometer is described for measurement of absolute humidity in the nest air immediately surrounding bird eggs during natural incubation. The empty eggshell of the species under study is filled with a drying agent and calibrated by observing its weight change in time upon exposure to known water vapor tensions. Such an egg is then placed in the nest for several days and its rate of gain in weight recorded, from which the mean vapor pressure during exposure can be calculated. The vapor pressure in the nest microclimate of eight species varied from 18 to 26 torr. An indirect method for predicting nest air vapor pressure without the use of a hygrometer is also presented, and for 10 other species yields values similar to those of the diffusion hygrometer. The vapor pressure of nest air is always greater than that of ambient air; from the difference and the known rate of water loss of the egg, nest ventilation can be calculated.

Oxygen Consumption, Gas Exchange, and Growth of Embryonic Wedge-Tailed Shearwaters (Puffinus pacificus chlororhynchus)

The mass of the wedge-tailed shearwater (Puffinus pacificus chlororhychus) egg is approximately the same as that of the chicken (≃60 g), but the incubation period is more than twice as long (52 days vs. 21 days) and the water vapor conductance,