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. 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).     

A gross and microscopic study of the respiratory anatomy of the Antarctic Weddell seal, Leptonychotes weddelli.

Four species of Phocidae, or true seals, inhabit the waters surrounding the Antarctic continent. These animals are thought to have different diving capabilities. The Weddell seal, Leptonychotes weddelli, is known to be capable of attaining depths up to 600 meters. The respiratiory system of the Weddell seal shows the usual adaptations to an aquatic environment characteristic of other marine. These include lungs that undergo compression acollapse at depths greater than 70 meters; hyaline cartilage in the tracheo-bronchial tree as far as the terminal bronchioles; and large amounts of smooth muscle surrounding the distal-most bronchioles. The collapsible lungs provide a mechanism by which air is forced from the alveoli adjacent to the pulmonary capillary beds thereby preventing the absorption of nitrogen gas into the bloodsteam. The presence of hyaline cartilage throughout most of the tracheo-bronchial tree increases the effective dead air space that accommodates most of the air forced from the collapsed lungs. The smooth muscle surrounding the respiratory bronchioles prevents their collapse while under the pressures of a deep dive. Collapse of the respiratory bronchioles not supported by cartilage would trap air in the lung alveoli during a dive. In addition, large- sac-like "diverticulae" are found in the submucosa throughout the tracheo-bronchial tree. These diverticulae, which open directly into the lumen of the tree, appear to be modified glands whose cells, in most cases, do not appear to be specialized for secretory function. They are most numerous in the more distal bronchi and terminal bronchioles where they are situated on both the luminal and adventitial sides of the hyaline cartilage supporting the walls of the air passages. Diverticulae are not found in the respiratory bronchioles or in the respiratory portion of the lungs.     

The functions and mechanisms of the protrusible upper jaws of some acanthopterygian fish

Photographs of Pterophyllum and Gasterosteus feeding indicate that they suck food into their mouths by expansion of the buccal and opercular cavities. The premaxillae are protruded as the mouth opens, and remain protruded as it closes. The mechanisms whereby these movements can be performed, by these and by more generalized acanthopterygians, are described. It is shown that the palatines of generalized acanthopterygians are so arranged as to prevent retraction of the premaxillae when the mouth is closed with the buccal cavity expanded.
It is estimated, from rough measurements on a few species, that a teleost cannot suck into its mouth food that is further from its mouth opening than about one-quarter of the length of its head. It is shown that protrusion of the premaxillae can be useful in getting the mouth opening close to food that is to be sucked in, expecially when it is to be taken from the bottom. The possible advantages of closing the mouth with the premaxillae protruded are discussed.
The origin of the acanthopterygian protrusile mechanism is discussed.     

On the mechanism of respiration in the bullfrog,Rana catesbeiana: A reassessment

The mechanism of respiration in the bullfrog has been analyzed by means of pressure recordings from the buccal cavity, the lungs and the abdominal cavity, by cinematography and cinefluorography, and by electromyography of buccal, laryngeal and abdominal muscles. Gas flow was investigated by putting frogs in atmospheres of changing argon and nitrogen content and monitoring the concentration of the nostril efflux. Three kinds of cyclical phenomena were found. (1) Oscillatory cycles consist of rhythmical raising and lowering of the floor of the mouth, with open nares. They have a definite respiratory function in introducing fresh air into the buccal cavity. (2) Ventilatory cycles involve opening and closing of the glottis and nares and renewal of a portion of the pulmonary gas. More muscles are involved and the pattern of muscular activity is more complex than in the oscillatory cycles. (3) Inflation cycles consist of a series of ventilation cycles, interrupted by an apneic pause. The intensity of the ventilatory cycles increases before this pause and decreases immediately thereafter. This results in a stepwise increase in pulmonary pressure, to a plateau (coincident with the pause) followed by a sudden or stepwise decrease. The respiratory mechanism depends on the activity of a buccal force pump, which determines pulmonary pressure whose level is always slightly less than the peak pressure values of the ventilation cycles. The elevated pulmonary pressure is responsible for the expulsion of pulmonary gas during the second phase of the next ventilation cycle. This pressure is maintained by the elastic fibers (and the smooth masculature) of the lungs.     

The initiation of diving apnoea in the frog, Rana pipiens.

1. Diving apnoea in Rana pipiens was initiated by submerging the external nares. As the water level was raised above the frog, both buccal and lung pressure increased by an amount corresponding to the water head. During submergence the external nares remained closed, although the apnoeic period was punctuated by ventilation movements which moved gas between the lungs and buccal cavity. 2. Bilateral section of the ophthalmic nerves did not alter the normal pattern of ventilation in air, although it often resulted in the intake of water into the buccal cavity on submergence. Introduction of water into the buccal cavity, either naturally as in denervates or by injection through a catheter in intact frogs, triggered sustained electromyographical activity in some respiratory muscles. 3. Electroneurograms recorded from the cut peripheral end of an ophthalmic nerve showed that receptors in the external narial region were stimulated by movement of a water meniscus across them. Activity could also be recorded in the ophthalmic nerve in response to water flow past the submerged nares. Punctate stimulation of the narial region confirmed that these receptors were mechanosensitive. 4. Bilateral electrical stimulation of the central ends of cut ophthalmic nerves in lightly anaesthetized frogs caused apnoea with a latency of less than 200 ms. The external nares remained closed throughout the period of stimulation although buccal pressure events, resembling underwater ventilation movements, occurred when stimulation was prolonged.     

The Evolution of Lung-Gill Bimodal Breathing and the Homology of Vertebrate Respiratory Pumps

SYNOPSIS. A comparative analysis of actinopterygian and sarcopterygianaerial buccal pumps indicates that the primitive pattern ofair transfer differs fundamentally between these two clades.Actinopterygian fishes ventilate their lungs with a four-strokebuccal pump: the buccal cavity expands and fills with expiredair, compresses to expel expired air, expands again to takein fresh air, and then compresses again to pump fresh air intothe lungs. Lungfishes, caudates, and anurans expand and compressthe buccal cavity only once per expiratory-inspiratory cycle,and thus use a two-stroke pump. Both of these bidirectional,aerial buccal pumps evolved from unidirectional, aquatic buccalpumps. The two-stroke aerial pump and the primitive aquaticpump used for gill irrigation share slow movements and may bothbe triggered by the same central rhythm generator. These similaritiessuggest that the two-stroke buccal pump evolved from the gillirrigation pump. Similarly, the four-stroke pump shares rapidmovement and afferent triggering with aquatic suction feedingand coughing, suggesting that the four-stroke pump may haveevolved from a combination of two suction feeding or coughingmovements. Thus the differences between the actinopterygianand sarcopterygian aerial buccal pumps may be due to their independentevolution from different aquatic buccal pumps, rather than dueto divergence from a single aerial buccal pump.     

Suckermouth armored catfish resolve the paradox of simultaneous respiration and suction attachment: a kinematic study of Pterygoplichthys disjunctivus

Suckermouth armored catfishes (Loricariidae) use their suckermouth for inspiration, feeding, and attachment to substrates. The sucker consists of a pre-valvular cavity, formed by a modified lip disc, and is separated from the larger post-valvular buccal cavity by a muscular oral valve. The combination of respiration and suction attachment seems paradoxal, as a properly functioning suction device would need a sucker without leakage (yet inspiration must occur via the sucker), and continuous subambient pressure in the sucker cavity (even during expiratory mouth floor elevation). In the loricariid Pterygoplichthys disjunctivus, the anatomy of the suckermouth structures was examined, and a kinematic analysis was performed to acquire insights into how respiration and attachment are combined. High-speed external and X-ray recordings show that suckermouth attachment influences respiratory parameters such as decreasing excursion amplitudes of mouth floor elements, and the way water enters the mouth via furrows in the lip disc. Respiration, however, continues during attachment and is not blocked. Our data show that the muscular oral valve actively separates the post-valvular buccal cavity from the pre-valvular sucker cavity. Volume changes of this pre-valvular cavity are opposite to those of the post-valvular cavity and assure sucker function even during expiration. These volume changes are caused by movements of the lower lip, the lower jaws, and the oral valve. The lateral inflow furrow openings, controlled by the maxillary barbels, can occur unilaterally. Morphological and kinematic data also show that the opercle is anatomically and functionally decoupled from the gill opening.     

The functions and mechanisms of the protrusible upper jaws of two species of cyprinid fish

Photographs have been taken of Idus and Gobio feeding. Idus , a primitive cyprinid, protrudes its premaxillae very little when it opens its mouth to take in food, but closes the mouth by further protrusion of the premaxillae. This enables it to close its mouth while keeping its buccal cavity fully expanded. Gobio , a more advanced cyprinid, protrudes its premaxillae strongly as it opens its mouth and is thereby able to apply the mouth closely to a surface from which it is taking food. The mechanisms of the movements are described.     

On the mechanism of air ventilaton in anabantoids (Pisces: Teleostei)

Summary Air ventilation in most Anabantoid species is diphasic, consisting of exhalation and inhalation. Exhalation is the release of air from the accessory breathing organs (suprabranchial chambers) through the mouth either into the water near the surface (e.g.,Ctenopoma) or directly into the atmosphere (e.g.,Osphronemus goramy). Inhalation, i.e., taking in fresh air through the mouth at the surface, immediately follows exhalation. X-ray films show (Figs. 5 and 6) that evacuation of the suprabranchial chambers during exhalation is total or nearly total. This, together with the fact that these chambers can contract at most to a very small extent, led to the conclusion that gas is replaced by water entering the chambers during exhalation and that this water is replaced by fresh air during inhalation. Further analysis of films, including conventional films showing the behavior of the opercular apparatus during air ventilation (Fig. 7), leads to a theory of a double-pumping mechanism responsible for air ventilation. This mechanism consists of the buccal apparatus and the opercular apparatus. It is suggested that both of these structures are able to act as both suction and pressure pumps, and thus air ventilation may be explained as the result of alternating activity of these two pumps.In the monophasic air ventilation characteristic of (adult)Anabas testudineus, there is no exhalation phase comparable to that of other Anabantoids. Therefore, no water enters the suprabranchial chambers, which remain filled with gas during the whole ventilation process (Fig. 10). Ventilation is limited to one phase comparable to inhalation in other Anabantoids.The structure of the accessory breathing organs (Fig. 1) and its progressive complication with growth (Fig. 4) were studied inOsphronemus goramy. The arrangement of the labyrinthine plates is in accordance with the requirements of transport of water and gas through the suprabranchial chambers. One plate (the inner plate, Fig. 1) separates these chambers into atrium, ventro-caudal, and dorso-caudal compartments, each with its own opening (valve). This organization seems essential for the transport of gas and water through the suprabranchial chambers and ensures that during exhalation, water flows into the chambers from above, so that while water is filling these chambers displaced gas can be sucked through the deep-lying pharyngeal openings into the expanding buccal cavity.Supported by the Deutsche Forschungsgemeinschaft     

Structures and movements of the buccal and pharyngeal jaws in relation to feeding in Diplodus sargus

The present paper studies the possibly different feeding strategies of Diplodus sargus to crustaceans, molluscs, worms, and small fish. The buccal jaws are built strongly and bound together by numerous ligaments. The dentition is heterodont: incisors in front and molars in the middle and hind parts. The principal originality of the musculature of this species is the forward insertion of the adductores mandibulae. These are very thick and insert on both the upper and lower jaws, so that contraction of any individual muscle acts on the buccal pieces as a whole, which thus constitute a remarkable crushing device. The pharyngeal jaws are frail as in primitive perciforms: the lower ones are well separated, being bound only anteriorly, while the upper ones consist of the second and third pharyngobranchials and a posterior toothed plate. When feeding on crabs, Diplodus sargus always sucks in the prey and seizes it with the buccal jaws. Mouth opening is accompanied by extensive protrusion of the mouth, with or without neurocranial elevation. Mouth sucking and seizing movements vary little. Once seized, the prey is usually moved to the molars and crushed. The crushing movements may be fast and ample or slow. In the latter case, deformation of the prey is observable. Crushing usually results in the crab being broken into pieces. The pharyngeal jaws grip one part of the prey and shift it to the oesophagus, then seize the second part. Diplodus sargus adapts its feeding behaviour to the type of prey. A snail, for instance, is crushed by the buccal or pharyngeal teeth, the pieces of shell are ejected, and the soft parts conveyed with difficulty to the oesophagus by the pharyngeal jaws. A fish on the other hand, is sucked tail first into the mouth cavity and quickly shifted to the digestive tract by the pharyngeal bones. Behaviour toward different prey differs by the presence or absence of parts of the sequence of feeding movements (for example crushing) or by the fact that certain movements or parts of the sequence are repeated. The variability of any movement in the sequence is the same whatever the sort of prey. Crushing occurs between the buccal incisors and molars and was observed twice between the pharyngeal teeth. Usually, it seems, the latter are involved in transport only. In transport, the left and right pharyngeal jaws may perform different functions: their movements, unlike the symmetrical movements of the buccal jaws, sometimes differ.     

Suctorial feeding in a deep-sea octopus as a means of niche partitioning (Cephalopoda: Octopodidae)

Molecular phylogenetic analyses indicate that two clades of deep-sea octopuses evolved at opposite ends of the earth to become globally sympatric. Coexistence of these overtly similar, but phylogenetically distinct octopuses requires some means of niche partitioning. To investigate details of feeding, the buccal complexes of specimens of each clade, Muusoctopus and Graneledone, were sectioned at 90° to the radular ribbon. The buccal complex of Muusoctopus is the same as reported in Octopus; the radula and its bolsters extend the length of the buccal complex. In Graneledone, however, the radula and its bolsters are restricted to anterior half of the buccal complex. Posterior to the radular sac, a vertically oriented muscle, named here the buccal abductor, extends from the floor of the mouth to the base of the buccal complex. In Muusoctopus, the bolsters extend the radula to bring food into the mouth; the palps propel it to the esophagus. In Graneledone, although the bolsters extend the radula, contraction of the buccal abductor to expand the posterior mouth may be the primary food mover. The negative pressure differential created draws food into the mouth and to the entry to the esophagus. The buccal abductor may permit the ingestion of larger pieces of prey, as gut contents show. Its evolution may represent a key innovation that heightens deep-sea octopus diversity.     

The influence of geomagnetic variations on the formation of nitric oxide in exhaled air in human

The content of nitric oxide in exhaled air in healthy persons has been studied. It was shown that nitric oxide in exhaled air is formed from saliva nitrite due to the nitrite reductase activity of mouth cavity microflora. A relationship between the nitric oxide level and age, arterial pressure, and geomagnetic field indices was established. It was shown that the level of nitric oxide diminishes with age. A negative correlation between the nitric oxide content in exhaled air and arterial pressure (systolic and diastolic) was found. It was assumed that nitric oxide from the mouth can penetrate into the lungs and then to the blood where it can influence the vessel tonus. It was shown that the negative relationship took place between nitric oxide level in the air and Ki-indices of geomagnetic field on the day of measurement or the day preceding the measurement. The data obtained suggest that nitric oxide is involved in processes causing infarcts and insults in periods of magnetic storms.     

Microvideography of gas bladder inflation in larval walleye

High-resolution microvideograph observations supported the hypothesis that first filling of the gas bladder of larval walleye Stizostedion vitreum is accomplished by the fish penetrating the air-water interface to gulp air, then transmitting a swallowed air bubble through the gut and the pneumatic duct to the gas bladder. The snout of the larva penetrated the water surface with extension of most of the mouth into the air for only 1.5 s. An air bubble ( c. 100 μm) in the foregut was broken up into progressively smaller bubbles (10–15 μm), presumably by the combined effect of surfactant derived from the gall bladder and mechanical (peristaltic) action of the gut. These smaller bubbles seemed to be aligned in the pneumatic duct before being forced to the gas bladder by pressures generated from peristalsis.     

Aspects of masticatory form and function in common tree shrews,Tupaia glis

Tree shrews have relatively primitive tribosphenic molars that are apparently similar to those of basal eutherians; thus, these animals have been used as a model to describe mastication in early mammals. In this study the gross morphology of the bony skull, joints, dentition, and muscles of mastication are related to potential jaw movements and cuspal relationships. Potential for complex mandibular movements is indicated by a mobile mandibular symphysis, shallow mandibular fossa that is large compared to its resident condyle, and relatively loose temporomandibular joint ligaments. Abrasive tooth wear is noticeable, and is most marked at the first molars and buccal aspects of the upper cheek teeth distal to P². Muscle morphology is basically similar to that previously described for Tupaia minor and Ptilocercus lowii. However, in T. glis, an intraorbital part of deep temporalis has the potential for inducing lingual translation of its dentary, and the large medial pterygoid has extended its origin anteriorly to the floor of the orbit, which would enhance protrusion. The importance of the tongue and hyoid muscles during mastication is suggested by broadly expanded anterior bellies of digastrics, which may assist mylohyoids in tensing the floor of the mouth during forceful tongue actions, and by preliminary electromyography, which suggests that masticatory muscles alone cannot fully account for jaw movements in this species.     

Form and Function of Lungs: The Evolution of Air Breathing Mechanisms

SYNOPSIS. Structural evolution of the vertebrate lung illustratesthe principle that the emergence of seemingly new structuressuch as the mammalian lung is due to intensification of oneof the functions of the original piscine lung. The configurationof the mechanical support of the lung in which elastic and collagenfibers form a continuous framework is well matched with thefunctional demands. The design of the mammalian gas exchangecells is an ingenious solution to meet the functional demandsof optimizing maintenance pathways from nucleus to the cytoplasmwhile simultaneously providing minimal barrier thickness. Surfactantis found in the most primitive lungs providing a protectivecontinuous film of fluid over the delicate epithelium. As thelung became profusely partitioned, surfactant became a functionallynew surface-tension reduction device to prevent the collapseof the super-thin foam-like respiratory surface. Experimentalanalyses have established that in lower vertebrates lungs areventilated with a buccal pulse pump, which is driven by identicalsets of muscles acting in identical patterns in fishes and frogs.In the aquatic habitats suction is the dominant mode of feedinggenerating buccal pressure changes far exceeding those recordedduring air ventilation. From the perspective of air ventilationthe buccal pulse pump is overdesigned. However in terrestrialhabitats vertebrates must operate with higher metabolic demandsand the lung became subdivided into long narrow airways andprogressively smaller air spaces, rendering the pulse pump inefficient.With the placement of the lungs inside a pump, the aspirationpump was established. In mammals, the muscular diaphragm representsa key evolutionary innovation since it led to an energeticallymost efficient aspiration pump. Apparently the potential energycreated by contraction of the diaphragm during inhalation isstored in the elastic tissues of the thoracic unit and lung.This energy is released when lung and thorax recoil to bringabout exhalation. It is further determined experimentally thatrespiratory and locomotory patterns are coupled, further maximizingthe efficiency of mammalian respiration. Symmorphosis is exhibitedin the avian breathing apparatus, which is endowed with a keyevolutionary innovation by having the highly specialized lungcontinuously ventilated by multiple air sacs that function asbellows. Functional morphologists directly deal with these kindsof functional and structural complexities that provide an enormouspotential upon simple changes in underlying mechanisms.     

Buccal oscillation and lung ventilation in a semi-aquatic turtle, Platysternon megacephalum

Movements of the hyobranchial apparatus in reptiles and amphibians contribute to many behaviors including feeding, lung ventilation, buccopharyngeal respiration, thermoregulation, olfaction, defense and display. In a semi-aquatic turtle, Platysternon megacephalum, x-ray video and airflow measurements from blowhole pneumotachography show no evidence that above water hyobranchial movements contribute to lung inflation, as in the buccal or gular pump of amphibians and some lizards. Instead, hyobranchial movements produce symmetrical oscillations of air into and out of the buccal cavity. The mean tidal volume of these buccal oscillations is 7.8 times smaller than the mean tidal volume of lung ventilation (combined mean for four individuals). Airflow associated with buccal oscillation occurs in the sequence of inhalation followed by exhalation, distinguishing it from lung ventilation which occurs as exhalation followed by inhalation. No fixed temporal relationship between buccal oscillation and lung ventilation was observed. Periods of ventilation often occur without buccal oscillation and buccal oscillation sometimes occurs without lung ventilation. When the two behaviors occur together, the onset of lung ventilation often interrupts buccal oscillation. The initiation of lung ventilation was found to occur in all phases of the buccal oscillation cycle, suggesting that the neural control mechanisms of the two behaviors are not coupled. The pattern of occurrence of both buccal oscillation and lung ventilation was found to vary over time with no obvious effect of activity levels.     

The structure and function of the labrum in the lobster Homarus gammarus (L.).

The labrum of decapod crustaceans is a soft lobe overhanging the mouth. The labral skeleton, musculature and innervation of Homarus gammarus are described. There are three bilateral groups of sensory neurons innervating the floor, lobe and lateral walls of the labrum. These are probably responsible for the phasic afferent activity that can be recorded from the inner labral nerve on mechanical deformation of the labrum. The labrum undergoes rhythmical retraction-protraction movements during ingestion and is shown to be active during both mandibular activity and oesophageal peristalsis. Studies were made on the duration and frequency of labral "swallowing" activity. The role of the labrum in feeding is discussed.     

New buccinator myomucosal island flap: anatomic study and clinical application

The authors studied the vascular anatomy of the buccinator muscle by dissecting fresh cadavers. The anatomy of the buccal branches of the facial artery consistently confirmed the existence of a posterior buccal branch, a few inferior buccal branches, and anterior buccal branches to the posterior, inferior, and anterior portions of the buccinator. The buccal artery and posterior buccal branch anastomose to each other and ramify over the muscle. Several veins originate from the lateral aspect of the muscle, converge into the buccal venous plexus, and drain into the facial vein (from two to four tributaries) or into the pterygoid plexus and the internal maxillary vein (from the buccal vein). These vessels and nerves enter the posterior half of the buccinator posterolaterally. The facial artery and vein are located at variable distances from each other around the oral commissure and the nasal base. Two patterns of buccinator musculomucosal island flaps supplied by these buccal arterial branches are proposed in this article. The buccal musculomucosal neurovascular island flap (posteriorly based), supplied by the buccal artery, its posterior buccal branch, and the long buccal nerve, can be passed through a tunnel under the pterygomandibular ligament for closure of mucosal defects in the palate, pharyngeal sites, the alveolus, and the floor of the mouth. The buccal musculomucosal reversed-flow arterial island flap (superiorly based), supplied by the distal portion of the facial artery through the anterior buccal branches, can be used to close mucosal defects in the anterior hard palate, alveolus, maxillary antrum, nasal floor and septum, lip, and orbit. The authors have used the flaps in 12 patients. There has been no flap necrosis, and results have been satisfactory, both aesthetically and functionally.