New perspectives on the evolution of lung ventilation mechanisms in vertebrates

Abstract

In the traditional view of vertebrate lung ventilation mechanisms, air-breathing fishes and amphibians breathe with a buccal pump, and amniotes breathe with an aspiration pump. According to this view, no extant animal exhibits a mechanism that is intermediate between buccal pumping and aspiration breathing; all lung ventilation is produced either by expansion and compression of the mouth cavity via the associated cranial and hyobranchial musculature (buccal pump), or by expansion of the thorax via axial musculature (aspiration pump). However, recent work has shown that amphibians exhibit an intermediate mechanism, in which axial muscles are used for exhalation and a buccal pump is used for inhalation. These findings indicate that aspiration breathing evolved in two steps: first, from pure buccal pumping to the use of axial musculature for exhalation and a buccal pump for inspiration; and second, to full aspiration breathing, in which axial muscles are used for both inhalation and exhalation. Furthermore, the traditional view also holds that buccal pump breathing was lost shortly after aspiration breathing evolved. This view is now being challenged by the discovery that several species of lizards use a buccal pump to augment costal aspiration during exercise. This result, combined with the observation that a behavior known as “buccal oscillation” is found in all amniotes except for mammals, suggests that a reappraisal of the role of buccal pumping in extant and extinct amniotes is in order.