Respiratory anatomy and physiology in diving penguins

Abstract

The anatomy and function of the respiratory systems of penguins are reviewed in relation to gas exchange and minimization of the risks of pulmonary barotrauma, decompression sickness and nitrogen narcosis during dives. Topics include available lung morphology and morphometry, respiratory air volumes determined with different techniques, review of possible physiological and biomechanical mechanisms of baroprotection, calculations of baroprotection limits and review of air sac and arterial partial pressure of oxygen (P_O2) profiles in relation to movement of air during breathing and during dives. Limits for baroprotection to 200, 400 and 600 m in Adélie, king and emperor penguins, respectively, would require complete transfer of air sac air and reductions in the combined tracheobronchial tree-parabronchial volume of 24% in Adélie, 53% in king penguins and 76% in emperor penguins. Air sac and arterial P_O2 profiles at rest and during surface activity were consistent with unidirectional air flow through the lungs. During dives, P_O2 profiles were more complex, but were consistent with compression of air sac air into the parabronchi and air capillaries with or without additional air mixing induced by potential differential air sac pressures generated by wing movements.This article is part of the theme issue 'The biology of the avian respiratory system'.

Keywords: air sac; barotrauma; gas exchange; lung; oxygen store.

Figure 1.

The response of the respiratory system to increased hydrostatic pressure differs between mammals and birds. In penguins, the lungs and tracheobronchial tree are less compliant (compressible) than the air sacs. By contrast, in mammals, the tracheobronchial tree is less compliant than the lungs. Consequently, in penguins, compression of the air sacs at depth results in a decrease in air sac volume and a transfer of air into the lungs with preservation of lung volume and gas exchange (a and b). In marine mammals, such as the seal, the alveoli of the lung are compressed, resulting in decreased lung volume and gas exchange as well as a transfer of air into the tracheobronchial tree (c and d).

Figure 2.

The respiratory systems of Adélie, king and emperor penguins, reconstructed from whole body serial CT scans of living birds, and scaled to body size. Colour code: trachea—red, anterior air sacs—light blue, posterior air sacs—blue, lungs—yellow. From the data of Ponganis [21].

Figure 3.

Hypothesized air movement patterns within the respiratory system during dives of penguins. As hydrostatic pressure increases with depth during a dive, compression of air sacs results in transfer of air into the parabronchi and air capillaries of the lung. During ascent, decreased hydrostatic pressure results in expansion of the air sacs. In addition, movement of air through the parabronchi may occur secondary to differential air sac pressures induced by wing movements [74]. Unidirectional movement of air through the parabronchi could result from air routing from anterior air sacs through the primary bronchi into posterior air sacs and then into the lung with return to the anterior air sacs (a). Bidirectional movement of air through the parabronchi could result from to and fro movement between the anterior and posterior air sacs via secondary bronchi and lungs (b). Lastly, even without significant convective air transport, enhanced diffusion of oxygen into the parabronchi and air capillaries from the air sacs (via secondary bronchi) could result from differential air sac pressure oscillations as well as the increase in the partial pressure of oxygen within the air sacs and lungs (c). Modified from Williams et al. [71].

Figure 4.

Cervical and posterior thoracic air sac partial pressure of O₂ (P_O2) profiles with depth and stroke rate profiles during three shallow dives of an emperor penguin [71]. The merging and overlap of air sac P_O2 profiles could occur at different points in a dive but did not correlate with depth, time into dive or stroke rate. In addition, overlap did not occur in all dives. The shapes of air sac P_O2 profiles can be dependent on many factors, including start-of-dive respiratory air volumes, O₂ consumption during diving, changes in air sac P_O2 secondary to changes in depth, the rate of O₂ diffusion, the compression of air sac air into the lung on descent and re-expansion of that air into the air sacs on ascent, and possible differential air sac pressure oscillations due to wing movement [71,74,80]. See text and electronic supplementary materials. Modified from Williams et al. [71].