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Elephants have had to adapt to gravitational stresses imposed on their very large respiratory structures. We describe some unusual features of the elephant's respiratory system and speculate on their functional significance. A distensible network of collagen fibers fills the pleural space, loosely connects lung to chest wall but appears not to constrain lung-chest wall movements. Myriad spaces within the network and its rich supply of capillaries suggest effective local sources and sinks for pleural fluid that may replace the gravity-dependent flows of smaller mammals. The lung is partitioned into approximately equal to 1 cm3 parenchymal units by a system of thick, elastic septa that ramify throughout the lung from origins on the lung's elastic external capsule. Parenchymal units suspended upon the elastic septal system protect dependent alveoli from compression, thereby reducing the usual gravitational gradient of lung expansion. Intra-pulmonary airways are devoid of cartilage, instead they appear to derive resistance to collapse from tethering forces of the attached septa.

The pectoral muscles in birds comprise up to a third of the body weight and provide the principal drive to the wing. Their attachment to the sternum suggests that they could compress the thorax and assist ventilation during flight. Most, but not all, birds have an integer ratio relationship between wingbeat and breathing frequency, but no measurements of the respiratory flow associated with the act of wingbeat are available. We recorded respiratory flow and wing timing in three starlings that flew at 22 knots (11 m.s-1) for up to 5 min in a wind tunnel. Triggering on wingbeat, we ensemble averaged flow records for many wingbeats in each flight. Because wingbeats occurred throughout the respiratory cycle, breathing flow tended to average to zero, and a small flow event related to wingbeat emerged. The volume change associated with wingbeat ranged from 3 to 11% of tidal volume, and this is probably an overestimate. We conclude that wingbeat and breathing in starlings are essentially mechanically independent, despite the direct attachment of the locomotor muscles to the thorax.

Inspiratory airflow in the avian lung completely bypasses the most cranial secondary bronchi (the ventrobronchi), and instead enters bronchi arising more caudally (the dorsobronchi). Dotterweich (1936) proposed that 'aerodynamic valves' prevented entry into the ventrobronchi. We have recently provided evidence that inspiratory aerodynamic valving in avian lungs depends on convective inertia in the primary bronchus (Banzett et al., 1987). Theoretical and physical models (Butler et al., 1988; Wang et al., 1988) showed that convective inertia could effect valving, but the effectiveness of valving at resting flows was less than that observed in the bird. This leads us to hypothesize that a segment of the primary bronchus is constricted, accelerating the gas and enhancing the convective inertia. To test this hypothesis in the present work we measured pressures throughout the airways and air sacs in anesthetized, pump-ventilated geese at different flow rates and gas densities. Our data show: (1) there is a large pressure drop in the primary bronchus close to the ventrobronchial junction, indicating the presence of a constriction; (2) this pressure drop increases with gas density and flow; (3) the convective inertia at this site is more than 10 times downstream opposing pressures. We conclude that the primary bronchus just cranial to the first ventrobronchus forms a constriction which accelerates inspired air. Furthermore, we conclude that the convective inertia of gas leaving this segment is sufficient to achieve inspiratory valving.

The non-reversing gas flow pattern in the avian lung has been attributed to 'aerodynamic valves'. A fundamental property of all aerodynamic valves is their dependence on inertial forces in the gas stream: sufficient reduction of inertial forces will cause aerodynamic valves to fail. If valving in the avian lung is aerodynamic, it should fail when gas stream momentum is reduced. We tested the dependence of the inspiratory valves in the goose lung on gas density and gas flow velocity. A bolus of tracer gas was placed in the tracheal cannula during an end-expiratory pause. Tracer gas appearance in a cranial air sac during the following inspiration and pause was used to deduce failure of the 'inspiratory valve' in cyclically ventilated geese. Little or no tracer entered the sac under control conditions, which approximated resting breathing, indicating highly effective valving. Lower flow rate or lower gas density caused increased tracer appearance, indicating valve failure. These results demonstrate the importance of gas inertial forces to normal valve function, and are direct evidence for the aerodynamic nature of the avian inspiratory valve.

The presence of unidirectional flow in the avian lung is thought to be effected by aerodynamic 'valves'. First we review the history of this hypothesis and summarize existing evidence. Second, we present a semiquantitative treatment of the various fluid dynamic factors that may be involved in directing fluid flow. The resulting calculations show in some detail how the inspiratory valve may work, and upon what mechanisms it may depend. Our calculations suggest that gas convective inertial forces are sufficient to effect inspiratory valving. Finally, we give some heuristic arguments regarding the mechanisms of expiratory valving.

We assessed various aerodynamic factors which might influence inspiratory valve function in the avian lung. During inspiration, no flow enters the proximal segments of the ventrobronchi connecting the primary bronchus to cranial sacs. Instead, all flow in the primary bronchus continues through the mesobronchus. This pattern of flow past the ventrobronchi into the mesobronchus is called inspiratory aerodynamic valving. Introducing steady inspiratory flows into simplified plastic models of a bifurcation, we altered geometry, downstream resistance, flow rate and gas density while we measured the resulting flow partitioning between downstream branches. We found that these models did reproduce the inspiratory valving phenomenon. Gas flow rate, gas density and geometry upstream of the bifurcation played important roles in flow partitioning, but the geometry and branching angles of the ventrobronchi did not. These findings are consistent with the idea that convective inertia of the inspiratory gas stream promotes preferential axial flow (Butler et al., 1988) and may be the principal mechanism accounting for inspiratory aerodynamic valving in the avian lung.