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. "
    Phylogeny, Anatomy and Physiology of Ancient Fishes, Edited by G. Zaccone, K. Dabrowski, M.S. Hedrick, J.M.O. Fernandes, J.M. Icardo, 01/2016: chapter 8: pages 179-200; CRC Press.
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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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    ABSTRACT: Studying vascular anatomy, especially in the context of relationships with hard tissues, is of great interest to biologists. Vascular studies have provided significant insight into physiology, function, phylogenetic relationships, and evolutionary patterns. Injection of resin or latex into the vascular system has been a standard technique for decades. There has been a recent surge in popularity of more modern methods, especially radiopaque latex vascular injection followed by CT scanning and digital "dissection." This technique best displays both blood vessels and bone, and allows injections to be performed on cadaveric specimens. Vascular injection is risky, however, because it is not a standardizable technique, as each specimen is variable with regard to injection pressure and timing. Moreover, it is not possible to view the perfusion of injection medium throughout the vascular system of interest. Both data and rare specimens can therefore be lost due to poor or excessive perfusion. Here, we use biplanar video fluoroscopy as a technique to guide craniovascular radiopaque latex injection. Cadaveric domestic pigs (Sus scrofa domestica) and white-tailed deer (Odocoileus virginianus) were injected with radiopaque latex under guidance of fluoroscopy. This method was found to enable adjustments, in real-time, to the rate, location, and pressure at which latex is injected in order to avoid data and specimen loss. In addition to visualizing the injection process, this technique can be used to determine flow patterns, and has facilitated the development of consistent markers for complete perfusion.
    PLoS ONE 05/2014; 9(5):e97940. DOI:10.1371/journal.pone.0097940 · 3.23 Impact Factor
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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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    ABSTRACT: The comparatively low compliance of the mammalian lung results in an evolutionary dilemma: the origin and evolution of this bronchoalveolar lung into a high-performance gas-exchange organ results in a high work of breathing that cannot be achieved without the coupled evolution of a muscular diaphragm. However, despite over 400 years of research into respiratory biology, the origin of this exclusively mammalian structure remains elusive. Here we examine the basic structure of the body wall muscles in vertebrates and discuss the mechanics of costal breathing and functional significance of accessory breathing muscles in non-mammalian amniotes. We then critically examine the mammalian diaphragm and compare hypotheses on its ontogenetic and phylogenetic origin. A closer look at the structure and function across various mammalian groups reveals the evolutionary significance of collateral functions of the diaphragm as a visceral organizer and its role in producing high intra-abdominal pressure.
    Respiratory Physiology & Neurobiology 04/2010; 171(1):1-16. DOI:10.1016/j.resp.2010.01.004 · 1.97 Impact Factor
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