Lung ventilation in salamanders and the evolution of vertebrate air-breathing mechanisms. Biological Journal of the Linnean Society

Biological Journal of the Linnean Society (Impact Factor: 2.26). 05/1993; 49(2):163 - 183. 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).

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    • "The type I breath therefore consists of an exhalation followed by inhalation during one breath cycle (i.e., a four-stroke mechanism), whereas the type II breath consists of an inhalation only, with no associated exhalation (Hedrick and Jones 1993). It is unknown whether any of the other primitive actinopterygians use a two-stroke mechanism like the one described for Amia, but some teleostean air-breathers use a two-stroke mechanism (Hoplerythrinus and Gymnotus, Graham 1997); likewise, not all amphibians use a two-stroke lung ventilation pattern (Amphiuma, Brainerd and Ditelberg 1993 and Xenopus, Brett and Shelton 1979). Thus, the two-stroke, four-stroke distinction may have little usefulness as a character state for determining evolutionary relationships but, rather, may refl ect the plasticity and variation of centrally-generated motor patterns among the Osteichthyes. "

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    • "In addition to guiding injections, we found that fluoroscopy enables observation of flow patterns for radiopaque fluids pumped through the common carotid artery. Beyond cranial vascular studies, video fluoroscopy has been a useful technique for observation of fluid flow through many anatomical systems [38], [39]. Furthermore, this study has yielded consistent markers for complete perfusion of cranial arteries. "
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    • "The transverse muscle group has a dorso-ventral orientation, lies internal to the ribs and is usually not attached to them (Maurer, 1896). In all animals that possess it, the transversus serves to increase intraperitoneal pressure during expiration (Brainerd et al., 1993). Tetrapods also possess a sub-vertebral muscle group that plays an important role in neck movement. "
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