Review
Physiological Strategies of Oxygen Transport in High Altitude Bird Embryos

This paper was presented at the European Society of Comparative Physiology and Biochemistry Symposium on “Life in Extreme Environments” under the theme of “Hypoxia,” held in June 1995 at La Seyne-sur-Mer, France.
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Abstract

Because of the relative simplicity of factors governing gas exchange between the embryo and the environment, the avian embryo has been extensively studied at sea level as a model for describing the physical principles that govern the physiology of gaseous diffusion. Two patterns of response have been observed in the oxygen pressure (PO2) cascade of high altitude avian embryos: (1) At a fixed O2 conductance, a decrease in metabolic rate below levels typical of conspecific species at sea level results in a reduction of ΔPO2 between ambient air and air cell. The decrease in metabolic rate also affects each step in the gradient until the mitochondria is reached. This is illustrated by a Fick's-type equation: PO2 = V̇O2/GO2 (GO2 = oxygen conductance); (2) Maintenance of metabolic rate at roughly sea level values and a large GO2 will also keep the ΔPO2 unmodified or even reduced.

We have observed both patterns in mountain avian embryos in the Peruvian Andes. We measured V̇O2 and the ΔPO2 cascade of embryos of Peruvian coots (Fulica americana peruviana), which breed both at sea level and in the puna (Andean high altitude plateau), and those of Puna teal (Anas versicolor puna), a species that breeds solely in the puna, both at 4150 m.

These two different strategies result in similar arterial PO2 values in both values in both embryos. Because the a-v PO2 gradient remains protected, the PV̄O2 values are also similar in the embryos of both high altitude birds.

Introduction

In the process of growth and development of mammalian and avian embryos, aerobic production of ATP requires O2 and produces CO2 as a waste product. These gases are exchanged with the respective environments of the embryos by the process of diffusion, but here the similarities end. Mammalian fetuses exchange O2 and CO2 with the maternal circulation through the placenta. The rate of gas diffusion depends upon a complex set of relationships that involve gradients for each gas between the fetal and maternal circulation, the rate of flow of blood through the placenta, O2 carrying capacity of maternal blood and others [12]. In contrast, avian respiration between its respiratory organ, the chorioallantoic membrane, and the external environment is governed principally by the process of diffusion of gases through air-filled pores in the shell. Because of the relative simplicity of factors governing gas flux between the inside of the shell and the environment, gas exchange of the avian embryo has been extensively studied at sea level as a model for describing the physical principles that govern the physiology of gaseous diffusion 23, 28, 31, 32, 34.

The decrease in barometric pressure at high altitude and the concomitant decrease in PO2 pose challenges for both adults and embryos of birds and mammals 2, 18. In humans, maternal increases in ventilation maintain arterial PO2 at adequate levels, and modifications in maternal circulation and placental morphology increase the rate of delivery and the surface area for gas exchange with the fetus [18].

The purpose of this review is to present what is currently known about how selective forces acting on avian eggs and embryos at high altitudes have fostered the development of specializations that promote successful growth and development to hatching.

Section snippets

Basic principles of avian embryonic gas exchange

Gases diffusing between the avian embryo and the external environment travel through a number of different barriers. From the outside of a typical, 60-g chicken (Gallus domesticus) egg, O2 travels 300 μm through the shell via about 10,000 pores, through the outer shell membrane (60 μm thick) and an inner shell membrane (15 μm thick) and finally through the epithelium of the chorioallantoic membrane [28]. Each pore has an average diameter of 17 μm, resulting in a total functional pore area of

Adaptation of eggshell permeability to gases in high altitude birds

Rahn and Ar [25] were the first to point out that the inverse relation existing between barometric pressure and the diffusion coefficient for gases (D in Eq. (1)) should have implications for gaseous diffusion in avian eggs at altitude. If gas flux were measured in an egg at sea level and again at altitude and if all other factors in Eq. (1)remained equal, O2 would diffuse more rapidly into the egg, while CO2 and water vapor would diffuse out more rapidly 22, 23. Therefore, the G of an egg to

The PO2 Cascade

As altitude increases and PO2 in the ambient air decreases, the gradient for diffusion of O2 into tissues decreases. The decreased gradient should lower the rate of diffusion from ambient air through the shell into the air cell, then through the inner shell membrane and chorioallantoic membrane into the blood, from the blood into the cell, and finally into the mitochondria. Two patterns of O2 transport have been observed in high altitude animals:

  • 1.

    At a fixed O2 conductance, a decrease in

Conclusions

The first barrier to diffusion of O2 in the PO2 cascade is the shell and outer shell membrane. Of these, the shell constitutes almost all the resistance to O2 diffusion. When all the available data on G of eggs of birds laying at high altitude are considered, we see one of the few cases in biology in which an adaptation reverses direction over a physical gradient of the environment. This reversal is due to a shift in selective forces, from the importance of conservation of water and CO2 at

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