Lung ventilation in salamanders and the evolution of vertebrate air-breathing mechanisms

ArticleinBiological Journal of the Linnean Society 49(2):163 - 183 · June 1993with60 Reads
DOI: 10.1111/j.1095-8312.1993.tb00896.x
Functional analysis of lung ventilation in salamanders combined with historical analysis of respiratory pumps provides new perspectives on the evolution of breathing mechanisms in vertebrates. Lung ventilation in the aquatic salamander Necturus maculosus was examined by means of cineradiography, measurement of buccal and pleuroperitoneal cavity pressures, and electromyography of hypaxial musculature. In deoxygenated water Necturus periodically rises to the surface, opens its mouth, expands its buccal cavity to draw in fresh air, exhales air from the lungs, closes its mouth, and then compresses its buccal cavity and pumps air into the lungs. Thus Necturus produces only two buccal movements per breath: one expansion and one compression. Necturus shares the use of this two-stroke buccal pump with lungfishes, frogs and other salamanders. The ubiquitous use of this system by basal sarcopterygians is evidence that a two-stroke buccal pump is the primitive lung ventilation mechanism for sarcopterygian vertebrates. In contrast, basal actinopterygian fishes use a four-stroke buccal pump. In these fishes the buccal cavity expands to fill with expired air, compresses to expel the pulmonary air, expands to fill with fresh air, and then compresses for a second time to pump air into the lungs. Whether the sarcopterygian two-stroke buccal pump and the actinopterygian four-stroke buccal pump arose independently, whether both are derived from a single, primitive osteichthyian breathing mechanism, or whether one might be the primitive pattern and the other derived, cannot be determined. Although Necturus and lungfishes both use a two-stroke buccal pump, they differ in their expiration mechanics. Unlike a lungfish (Protopterus), Necturus exhales by contracting a portion of its hypaxial trunk musculature (the m. Iransversus abdominis) to increase pleuroperitoneal pressure. The occurrence of this same expiratory mechanism in amniotes is evidence that the use of hypaxial musculature for expiration, but not for inspiration, is a primitive tetrapod feature. From this observation we hypothesize that aspiration breathing may have evolved in two stages: initially, from pure buccal pumping to the use of trunk musculature for exhalation but not for inspiration (as in Necturus); and secondarily, to the use of trunk musculature for both exhalation and inhalation by costal aspiration (as in amniotes).
    • "This aspiratory mechanism is a unique mechanical feature of the ganoid scales and body wall and is not related to the aspiratory mechanism for lung ventilation in tetrapods. The buccal force pump lung ventilation mechanism has been described as a two-stroke buccal pump, characteristic of the sarcopterygian fi shes (and amphibians) or a four-stroke buccal pump mechanism, characteristic of the actinopterygian fi shes (Brainerd et al. 1993). The two-stroke mechanism, shared by the Dipnoi and Amphibia, is characterized by the buccal cavity making two-movements, one expansion and one compression, during the ventilatory cycle (Bishop and Foxon 1968; McMahon 1969; de Jongh and Gans 1969). "
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