An allometric study of pulmonary morphometric parameters in birds, with mammalian comparisons

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Abstract
Comprehensive pulmonary morphometric data from 42 species of birds representing ten orders were compared with those of other vertebrates, especially mammals, relating the comparisons to the varying biological needs of these avian taxa. The total lung volume was strongly correlated with body mass. The volume density of the exchange tissue was lowest in the charadriiform and anseriform species and highest in the piciform, cuculiform and passeriform species. The surface area of the blood-gas (tissue) barrier, the volume of the pulmonary capillary blood and the total morphometric pulmonary diffusing capacity were all strongly correlated with body mass. The harmonic mean thickness of both the blood—gas (tissue) barrier and the plasma layer were weakly correlated with body mass. The mass-specific surface area of the blood—gas (tissue) barrier (surface area per gram body mass) and the surface density of the blood—gas (tissue) barrier (i.e. its surface area per unit volume of exchange tissue) were inversely correlated (though weakly) with body mass. The passeriform species exhibited outstanding pulmonary morphometric adaptations leading to a high specific total diffusing capacity per gram body mass, consistent with the comparatively small size and energetic mode of life which typify passeriform birds. The relatively inactive, ground-dwelling domestic fowl ( Gallus gallus ) had the lowest pulmonary diffusing capacity per gram body mass. The specific total lung volume is about 27 % smaller in birds than in mammals but the specific surface area of the blood-gas (tissue) barrier is about 15% greater in birds. The ratio of the surface area of the tissue barrier to the volume of the exchange tissue was also much greater in the birds (170-305 %). The harmonic mean thickness of the tissue barrier was 56—67 % less in the birds, but that of the plasma layer was about 66% greater in the birds. The pulmonary capillary blood volume was also greater (22%) in the birds. Except for the thickness of the plasma layer, these morphometric parameters all favour the gas exchange capacity of birds. Consequently, the total specific mean morphometric pulmonary diffusing capacity for oxygen was estimated to be about 22% greater in birds than in mammals of similar body mass. This estimate was obtained by employing oxygen permeation constants for mammalian tissue, plasma and erythrocytes, as avian constants were not then available. Recalculations using recent values for the rate of oxygen uptake by avian whole blood indicate that the superiority of the avian pulmonary diffusing capacity for oxygen is even greater, the value for birds exceeding that of mammals by about 82%. However, because of the small numbers of some of the avian species investigated and the lack of representatives of many important groups of birds, our allometric computations should be regarded as essentially a preliminary basis for comparing the pulmonary morphometric characteristics of birds and mammals. It is suggested that the greater physiological efficiency of the avian pulmonary system compared with that of mammals can be attributed partly to the pulmonary morphometric differences between these two vertebrate classes. Other major factors are the cross-current relation of parabronchial gas and blood, the auxiliary countercurrent relation of air capillary gas and blood, and the bellows action of the air sacs.