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Three‐dimensional reconstruction for study of the functional design of the avian lung

Among the air‐breathing vertebrates, the avian respiratory system is anatomically the most complex and physiologically the most efficient. Considerably, these attributes explain how and why birds achieved powered flight, a highly energetically costly form of locomotion. The avian lung which is small and rigid and firmly attached to the vertebral column and the ribs is ventilated continuously and unidirectionally by synchronized activity of capacious air sacs. Although the respiratory system has been studied for nearly five centuries, i.e. since Coiter (1573), certain aspects of its functional design remained unclear. The size, the shape and the arrangement of the blood capillaries and the air capillaries, the minuscule terminal respiratory units, particularly remained uncertain. Various investigators considered the air capillaries to be ‘tiny tubules', ‘intercapillary air passages', ‘straight tubules', ‘terminal air canals' and ‘intercellular passages'. Furthermore, the air capillaries were deemed to terminate in blind expansions, the blood capillaries were not mirror images of the air capillaries and the air capillaries and the blood capillaries run parallel to and in contact with each other across the exchange tissue. Because of the intimate entwining between the air capillaries and the blood capillaries, the exchange tissue was reported to resemble ‘a sponge in structure’, ‘a sinusoidal three‐dimensional network’ and ‘a dexterously crafted blood capillary network that interfaces with the equally complex air capillary labyrinth’. The descriptive (imprecise) terms used on the morphologies of the air capillaries and the blood capillaries and their topographical relationships were based on personal perceptions of microscopic sectional profiles rather than on hard empirical data. Unfortunately, the imprecise details were used in the formulation of a functional model for gas exchange in the avian lung where the air‐ and the blood capillaries were tubular in shape, the air capillaries run outwards from the parabronchial lumen and contacted the blood capillaries which run inwards from the peripherally located interparabronchial arteries and each of the respiratory units terminated blindly. Taking advantage of the recent increase in computing power and availability of appropriate robust software, three‐dimensional reconstruction was performed on serial sections of the avian lung to elucidate the morphologies and the spatial assemblage of the air capillaries and the blood capillaries. Unlike the classical morphology of the blood capillaries, e.g., in skeletal muscle, where the capillaries are longer than they are wide, those of the avian lung comprise distinctive segments that are rather as long as they are wide and are connected in three‐dimensions. The air capillaries are rotund structures which are joined by very narrow passageways. Completely isolated air capillaries were identified: the functional role of such units remains unclear. The air capillaries and the blood capillaries are not mirror images and the structural interdependence between the air capillaries and the blood capillaries may explain the strength of the tiny respiratory units. Because in a exchange tissue the air diffuses outwards from the parabronchial lumen and the blood flows inwards from the peripherally located interparabronchial arteries, existence of an auxiliary countercurrent arrangement was confirmed between the air capillaries and the blood capillaries.