Aspiration Breathing Research Articles

Locomotor rib kinematics in two species of lizards and a new hypothesis for the evolution of aspiration breathing in amniotes

Most lizards walk and run with a sprawling gait in which the limbs are partly advanced by lateral undulation of the axial skeleton. Ribs and vertebrae are integral to this locomotor mode, but 3D motion of the axial skeleton has not been reported for lizard locomotion. Here, we use XROMM to quantify the relative motions of the vertebrae and ribs during slow treadmill locomotion in three savannah monitor lizards (Varanus exanthematicus) and three Argentine black and white tegus (Salvator merianae). To isolate locomotion, we selected strides with no concurrent lung ventilation. Rib rotations can be decomposed into bucket-handle rotation around a dorsoventral axis, pump-handle rotation around a mediolateral axis, and caliper rotations around a craniocaudal axis. During locomotion, every rib measured in both species rotated substantially around its costovertebral joint (8–17 degrees, summed across bucket, pump and caliper rotations). In all individuals from both species, the middle ribs rotated cranially through bucket and pump-handle motion during the propulsive phase of the ipsilateral forelimb. Axial kinematics during swing phase of the ipsilateral forelimb were mirror images of the propulsive phase. Although further work is needed to establish what causes these rib motions, active contraction of the hypaxial musculature may be at least partly responsible. Unilateral locomotor rib movements are remarkably similar to the bilateral pattern used for lung ventilation, suggesting a new hypothesis that rib motion during locomotion may have been an exaptation for the evolution of costal aspiration breathing in stem amniotes.

Evolution and Functional Differentiation of the Diaphragm Muscle of Mammals.

Symmorphosis is a concept of economy of biological design, whereby structural properties are matched to functional demands. According to symmorphosis, biological structures are never over designed to exceed functional demands. Based on this concept, the evolution of the diaphragm muscle (DIAm) in mammals is a tale of two structures, a membrane that separates and partitions the primitive coelomic cavity into separate abdominal and thoracic cavities and a muscle that serves as a pump to generate intra-abdominal (Pab ) and intrathoracic (Pth ) pressures. The DIAm partition evolved in reptiles from folds of the pleural and peritoneal membranes that was driven by the biological advantage of separating organs in the larger coelomic cavity into separate thoracic and abdominal cavities, especially with the evolution of aspiration breathing. The DIAm pump evolved from the advantage afforded by more effective generation of both a negative Pth for ventilation of the lungs and a positive Pab for venous return of blood to the heart and expulsive behaviors such as airway clearance, defecation, micturition, and child birth. © 2019 American Physiological Society. Compr Physiol 9:715-766, 2019.

Function of Intracoelomic Septa in Lung Ventilation of Amniotes: Lessons from Lizards

Aspiration breathing is the dominant mechanism of lung inflation among extant amniotes. However, aspiration has two fundamental problems associated with it: paradoxical visceral translation and partial lung collapse. These can constrain the inspiratory tidal volume, reduce the effective lung ventilation, and ultimately curtail the aerobic capacity of an animal. Separation of the pleural and peritoneal cavities by an intracoelomic septum can restrict the cranial shift of abdominal viscera and provide structural support to the caudal lung surface. A muscular septum, such as the diaphragm of mammals or the diaphragmaticus of crocodilians, can exert active control over visceral translation and the degree of lung inflation. To a lesser degree, a nonmuscular septum can also function as a passive barrier when stretched taut by rib rotation. Studies of the posthepatic septum in teiid lizards and the postpulmonary septum in varanid lizards underscore the importance of nonmuscular septa in aspiration. These septa provide plausible functional models that help us infer the evolution of mammalian and avian lung ventilatory systems, respectively.

Functional morphology and evolution of aspiration breathing in tetrapods

In the evolution of aspiration breathing, the responsibility for lung ventilation gradually shifted from the hyobranchial to the axial musculoskeletal system, with axial muscles taking over exhalation first, at the base of Tetrapoda, and then inhalation as well at the base of Amniota. This shift from hyobranchial to axial breathing freed the tongue and head to adapt to more diverse feeding styles, but generated a mechanical conflict between costal ventilation and high-speed locomotion. Some "lizards" (non-serpentine squamates) have been shown to circumvent this speed-dependent axial constraint with accessory gular pumping during locomotion, and here we present a new survey of gular pumping behavior in the tuatara and 40 lizard species. We observed gular pumping behavior in 32 of the 40 lizards and in the tuatara, indicating that the ability to inflate the lungs by gular pumping is a shared-derived character for Lepidosauria. Gular pump breathing in lepidosaurs may be homologous with buccal pumping in amphibians, but non-ventilatory buccal oscillation and gular flutter have persisted throughout amniote evolution and gular pumping may have evolved independently by modification of buccal oscillation. In addition to gular pumping in some lizards, three other innovations have evolved repeatedly in the major amniote clades to circumvent the speed-dependent axial constraint: accessory inspiratory muscles (mammals, crocodylians and turtles), changing locomotor posture (mammals and birds) and respiratory-locomotor phase coupling to reduce the mechanical conflict between aspiration breathing and locomotion (mammals and birds).

New perspectives on the evolution of lung ventilation mechanisms in vertebrates

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.

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

Abstract 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. transversus 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).

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

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. transversus 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).

Air Ventilation by Recoil Aspiration in Polypterid Fishes

High-speed x-ray cine films synchronized with intra-pleuroperitoneal pressure measurements show that polypterid fishes aspiration breathe by the deformation and recoil of their bony-scaled integument. Paleozoic amphibians arose from ancient air-breathing fishes and retained piscine bony scales in V-shaped rows along the belly. These scales resemble those of modern polypterid fishes and may have contributed to inhalation by elastic recoil. The discovery that polypterid fishes breathe by recoil aspiration is the first evidence for aspiration breathing in any lower vertebrate. The use of recoil aspiration by polypterids shows that elastic storage in a stiff body wall can contribute to inhalation in animals with limited capacity for active aspiration.

Air-breathing mechanics in two Amazonian teleosts, Arapaima gigas and Hoplerythrinus unitaeniatus

The mechanics of air breathing in pirarucu, Arapaima gigas, and jeju, Hoplerythrinus unitaeniatus, were studied by simultaneous monitoring of air bladder gas pressure and buccal pressure. Also the effect of alterations in air bladder gas tensions on air-breathing patterns was examined by a gas replacement technique. Pirarucu surface every 4.2 min to make a single ventilation of the air bladder, whilst jeju usually make two or three ventilations at an air breath every 3.0 min. Pirarucu exhale first, then inhale, but in jeju buccal filling occurred before lung emptying. Inhalation in pirarucu is a result of air bladder aspiration combined with the action of a buccal pump; however, lung filling in jeju is achieved by a buccal pump only. The significance of aspiration breathing in pirarucu is discussed. Both fish respond similarly to alterations in air bladder gas tensions. Hyperoxia prolongs the interval between air breaths and hypercapnia reduces this interval.

Is the aestivating lungfish the first vertebrate with suctional breathing?

THE current view is that ventilation of the lungs by aspiratory, negative-pressure inhalation probably occurred in the earliest, now extinct amphibians1. But no aspiration breathing has been demonstrated in extant air-breathing vertebrates below reptiles, which use freely movable ribs and specialised muscles for this purpose. We report experiments showing that the aestivating lungfish relies on suctional breathing.

Sound Production in the Salientia: Mechanism and Evolution of the Emitter

Frog sounds involve expulsion of air through the larynx. In mating, release, rain, and territorial calls, the air vibrates vocal cords and/or arytenoid cartilages. Sound is amplified and radiated by the distended buccal cavity and vocal sacs. Distress calls are emitted with open mouth, with minimum laryngeal modulation. The trunk is filled by inflation cycles, but air is driven out by synchronized contractions of the body wall musculature. The pressure levels are more than five times those during ventilation. In the release call of Bufo valliceps the dilatators and constrictors of the larynx fire simultaneously keeping the larynx closed. As the pulmonary pressure reaches a peak they cease firing. The arytenoids then separate and vibrate, as do the vocal cords. The dilatators terminate the sound pulse by pulling vibrators out of the air stream, hence the very sharp termination. Prolonged release call sequences include interpulse Teinflations that return air from buccal cavity to lung. Frogs apparently evolved from amphibians too small to use aspiration breathing. Vocalization represented a critical factor in their social organization and its importance locked these animals into reliance upon pulse-pumping rather than the more efficient aspiration breathing.