The development and differentiation of the parabronchial unit in quail (Coturnix coturnix)

The present study has been inspired by the conflicting data in the relevant literature concerning the embryogenesis of cell types of the parabronchial epithelium and the formation, discharge and distribution of trilaminar substance and lamellar bodies. Lung tissue from embryonic, newly hatched, immature and mature quail was subjected to standard processing for light and transmission electron microscopy. The parabronchial rudiments form shallow primitive atria on embryonic day 13. The precursors of granular cells differentiate with lamellar bodies in their cytoplasm. The residual population of non-granular epithelial cells is the common source for the differentiation of primitive squamous atrial and respiratory cells, the potential producers of trilaminar substance. The primitive squamous atrial cells sprout as branching infundibular canaliculi into the mesenchyme on embryonic day 14. The infundibular epithelium differentiates into the squamous respiratory cells that constitute with blood capillaries the blood-air barrier. Not until the time of hatching could the trilaminar substance be visualized being produced by squamous atrial and respiratory cells. In the late prehatching and early posthatching period the granular cells intensely escalate the production and discharge of lamellar bodies. The lamellar bodies form, together with sheets of trilaminar substance, mixed multilayered masses in atria. They disappear fast in the successive posthatching period. The formation of trilaminar substance in squamous atrial and respiratory cells is governed by the agranular endoplasmic reticulum, the cisternae of which take part in the formation of trilaminar units. The gas exchange tissue is predominantly represented by infundibula in immature quail. The posthatching growth of the gas exchange tissue of immature to mature quail occurs via intense multiplication of air and blood capillaries.     

A systematic study of the development of the airway (bronchial) system of the avian lung from days 3 to 26 of embryogenesis: a transmission electron microscopic study on the domestic fowl, Gallus gallus variant domesticus

In the embryo of the domestic fowl, Gallus gallus variant domesticus, the lung buds become evident on day 3 of development. After fusing on the ventral midline, the single entity divides into left and right primordial lungs that elongate caudally while diverging and shifting towards the dorsolateral aspects of the coelomic cavity. On reaching their definitive topographical locations, the lungs rotate along a longitudinal axis, attach, and begin to slide into the ribs. First appearing as a solid cord of epithelial cells that runs in the proximal-distal axis of the developing lung, progressively, the intrapulmonary primary bronchus begins to canalize. In quick succession, secondary bronchi sprout from it in a craniocaudal sequence and radiate outwards. On reaching the periphery of the lung, parabronchi (tertiary bronchi) bud from the secondary bronchi and project into the surrounding mesenchymal cell mass. The parabronchi canalize, lengthen, increase in diameter, anastomose, and ultimately connect the secondary bronchi. The luminal aspect of the formative parabronchi is initially lined by a composite epithelium of which the peripheral cells attach onto the basement membrane while the apical ones project prominently into the lumen. The epithelium transforms to a simple columnar type in which the cells connect through arm-like extensions and prominently large intercellular spaces form. The atria are conspicuous on day 15, the infundibulae on day 16, and air capillaries on day 18. At hatching (day 21), the air and blood capillaries have anastomosed profusely and the blood-gas barrier become remarkably thin. The lung is well developed and potentially functionally competent at the end of the embryonic life. Thereafter, at least upto day 26, no further consequential structures form. The mechanisms by which the airways in the avian lung develop fundamentally differ from those that occur in the mammalian one. Compared with the blind-ended bronchial system that inaugurates in the mammalian lung, an elaborate, continuous system of air conduits develops in the avian one. Further studies are necessary to underpin the specific molecular factors and genetic processes that direct the morphogenesis of an exceptionally complex and efficient respiratory organ.     

Some recent advances on the study and understanding of the functional design of the avian lung: morphological and morphometric perspectives

The small highly aerobic avian species have morphometrically superior lungs while the large flightless ones have less well-refined lungs. Two parabronchial systems, i.e. the paleopulmo and neopulmo, occur in the lungs of relatively advanced birds. Although their evolution and development are not clear, understanding their presence is physiologically important particularly since the air- and blood flow patterns in them are different. Geometrically, the bulk air flow in the parabronchial lumen, i.e. in the longitudinal direction, and the flow of deoxygenated blood from the periphery, i.e. in a centripetal direction, are perpendicularly arranged to produce a cross-current relationship. Functionally, the blood capillaries in the avian lung constitute a multicapillary serial arterialization system. The amount of oxygen and carbon dioxide exchanged arises from many modest transactions that occur where air- and blood capillaries interface along the parabronchial lengths, an additive process that greatly enhances the respiratory efficiency. In some species of birds, an epithelial tumescence occurs at the terminal part of the extrapulmonary primary bronchi (EPPB). The swelling narrows the EPPB, conceivably allowing the shunting of inspired air across the openings of the medioventral secondary bronchi, i.e. inspiratory aerodynamic valving. The defence stratagems in the avian lung differ from those of mammals: fewer surface (free) macrophages (SMs) occur, the epithelial cells that line the atria and infundibula are phagocytic, a large population of subepithelial macrophages is present and pulmonary intravascular macrophages exist. This complex defence inventory may explain the paucity of SMs in the avian lung.     

Development, structure, and function of a novel respiratory organ, the lung-air sac system of birds: to go where no other vertebrate has gone

Among the air-breathing vertebrates, the avian respiratory apparatus, the lung-air sac system, is the most structurally complex and functionally efficient. After intricate morphogenesis, elaborate pulmonary vascular and airway (bronchial) architectures are formed. The crosscurrent, countercurrent, and multicapillary serial arterialization systems represent outstanding operational designs. The arrangement between the conduits of air and blood allows the respiratory media to be transported optimally in adequate measures and rates and to be exposed to each other over an extensive respiratory surface while separated by an extremely thin blood-gas barrier. As a consequence, the diffusing capacity (conductance) of the avian lung for oxygen is remarkably efficient. The foremost adaptive refinements are: (1) rigidity of the lung which allows intense subdivision of the exchange tissue (parenchyma) leading to formation of very small terminal respiratory units and consequently a vast respiratory surface; (2) a thin blood-gas barrier enabled by confinement of the pneumocytes (especially the type II cells) and the connective tissue elements to the atria and infundibulae, i.e. away from the respiratory surface of the air capillaries; (3) physical separation (uncoupling) of the lung (the gas exchanger) from the air sacs (the mechanical ventilators), permitting continuous and unidirectional ventilation of the lung. Among others, these features have created an incredibly efficient gas exchanger that supports the highly aerobic lifestyles and great metabolic capacities characteristic of birds. Interestingly, despite remarkable morphological heterogeneity in the gas exchangers of extant vertebrates at maturity, the processes involved in their formation and development are very similar. Transformation of one lung type to another is clearly conceivable, especially at lower levels of specialization. The crocodilian (reptilian) multicameral lung type represents a Bauplan from which the respiratory organs of nonavian theropod dinosaurs and the lung-air sac system of birds appear to have evolved. However, many fundamental aspects of the evolution, development, and even the structure and function of the avian respiratory system still remain uncertain.     

Lung growth of the turkey, Meleagris gallopavo: I. Morphologic and morphometric description

To describe lung growth qualitatively and quantitatively from prehatch to adulthood of an unselected line of turkey, a precocial avian species, 36 male turkeys, three in each age group, were killed at 22 and 25 days of incubation, on hatch day, and at 1, 4, 7, 10, 14, 21, 28, 112, and 420 days of age. Body weight and lung volume were measured. A three-level cascade sampling system was used to prepare lung tissue for morphologic and morphometric observation by light microscopy. Point and intersection counting were used to estimate volume and surface densities of lung compartments relative to lung volume. Absolute volumes and surfaces of lung compartments were calculated. Bilogarithmic regressions provided allometric equations to describe growth of the lung in three phases: Tissue proliferation--explosive growth of lung volume relative to body weight and of the gas-exchange compartment within the lung. At 22 days of incubation there were few air and blood capillaries and a great deal of tissue that looked like mesenchyme between the parabronchi. Within the 6 days prior to hatch, the surface area of air capillaries increased 11-fold and of blood capillaries 27-fold, whereas the volume of interparabronchial tissue decreased 58%. Equilibrated growth--from hatch day to 28 days of age, most lung compartments grew evenly with lung volume. Regulated growth--from 28 days of age to adult, all lung compartments, except large vessels and exchange compartment, grew more slowly than the entire lung. Interatrial septa lengthened and their epithelial covering thinned, infundibula became more apparent, and interparabronchial connective tissue reached a minimal volume density in the adult lung.     

A scanning and transmission electron microscopic study of the bat lung

The lungs of two adult species of bat Epomophorus wahlbergi and Miniopterus minor fixed with 2.3% glutaraldehyde were processed for SEM (scanning electron microscope) and TEM (transmission electron microscope) examination by the standard procedures. The bat lung comprised a blood and air conducting zone (consisting of bronchi, bronchioles and large blood vessels), the intermediate zone (made up of alveolar ducts), and the respiratory zone, which consisted of alveoli and blood capillaries. The interalveolar septa comprised basically granular pneumocytes (type II cells), squamous pneumocytes (type I cells), endothelial cells, and, in the interstitium, collagen and elastic fibres with occasional fibrocytes. Blood capillaries were interposed in the interalveolar septa, thus bulging into adjacent alveoli. It was noted that grossly, architecturally and structurally, the bat lung was similar to that of a terrestrial mammal. However, in previous morphometric and physiological studies it has been found that bats have a large lung, a thin pulmonary blood-gas barrier, a large pulmonary capillary blood volume, and high haematocrit and haemoglobin concentration. The bat lung, while retaining the basic mammalian pulmonary design, is well adapted to provide the large amount of oxygen demanded by flight. The avian pulmonary design (the lung-air sac system) is thus not a prerequisite to flight.     

A scanning and transmission electron microscopic study of the lung of a caecilian Boulengerula taitanus

The lung of an apodan amphibian Bouiengerula taitanus has been investigated by scanning and transmission electron microscopy. This caecilian has only a single, long tubular lung that tapers towards the caudal end of the body. The lung has a central air duct which radially opens into a single stratum of alveoli lined by well developed septa that attach to two diametrically opposite trabeculae. The trabeculae carry the pulmonary artery and vein. The septa have blood capillaries on both surfaces and supportive and contractile elements like collagen, smooth muscle, elastic tissue and fibrocytes. The alveolar surface has only a single population of pneumocytes that combine the morphological features of the mammalian type 1 and 2 cells, i.e. they contain the osmiophilic, lamellated bodies and are squamous in form. Through subepithelial cytoplasmic invaginations, the pneumocytes, together with their basement lamina, were observed to be firmly attached to the septa1 tissue elements, presumably to avoid mechanical detachment during the rapid respiratory movements. The compartmentation of the whole lung in this species is viewed as a means of increasing the surface area available for gas exchange which, coupled with other already established cardiovascular adaptations in this species, may be of significance in its fossorial mode of life, an environment that is usually hypoxic and hypercarbic.     

Glycoconjugate sugar residues in the chick embryo developing lung: a lectin histochemical study

A lectin histochemical study was performed to investigate the distribution and changes of the oligosaccharidic component of the glycoconjugates in the lung of chick embryos, of 1-day-old chick, and of the adult animal. For this purpose, a battery of seven horseradish peroxidase-conjugated lectins (PNA, SBA, DBA, WGA, Con A, LTA, and UEA I) were employed. During the first phase of parabronchi and atria formation, D-galactose-(beta1-->3)-N-acetyl-D-galactosamine, beta-N-acetyl-D-galactosamine, D-glucosamine, alpha-D-mannose, and sialic acid, present at the level of the surface and of cytoplasmic granules of the lining epithelial cells, seem to play a role in regulating morphogenetic phenomena. In the subsequent phases, the parabronchial lumen and the atrial cavities were characterized by the presence of lectin-reactive material rich in terminal D-galactose-(beta1-->3)-N-acetyl-D-galactosamine, beta-N-acetyl-D-galactosamine, D-glucosamine and alpha-D-mannose. From day 18 onwards and immediately after hatching, the free border of the cells lining the air capillaries was characterized by the presence of beta-N-acetyl-D-galactosamine and alpha-D-mannose. The appearance of these sugar residues was concomitant with the beginning of respiratory activity.     

Pivotal debates and controversies on the structure and function of the avian respiratory system: setting the record straight

Among the extant air‐breathing vertebrates, the avian respiratory system is structurally the most complex and functionally the most efficient gas exchanger. Having been investigated for over four centuries, some aspects of its biology have been extremely challenging and highly contentious and others still remain unresolved. Here, while assessing the most recent findings, four notable aspects of the structure and function of the avian respiratory system are examined critically to highlight the questions, speculations, controversies and debates that have arisen from past research. The innovative techniques and experiments that were performed to answer particular research questions are emphasised. The features that are outlined here concern the arrangement of the airways, the path followed by the inspired air, structural features of the lung and the air and blood capillaries, and the level of cellular defence in the avian respiratory system. Hitherto, based on association with the proven efficiency of naturally evolved and human‐made counter‐current exchange systems rather than on definite experimental evidence, a counter‐current gas exchange system was suggested to exist in the avian respiratory system and was used to explain its exceptional efficiency. However, by means of an elegant experiment in which the direction of the air‐flow in the lung was reversed, a cross‐current system was shown to be in operation instead. Studies of the arrangement of the airways and the blood vessels corroborated the existence of a cross‐current system in the avian lung. While the avian respiratory system is ventilated tidally, like most other invaginated gas exchangers, the lung, specifically the paleopulmonic parabronchi, is ventilated unidirectionally and continuously in a caudocranial (back‐to‐front) direction by synchronized actions of the air sacs. The path followed by the inspired air in the lung–air sac system is now known to be controlled by a mechanism of aerodynamic valving and not by anatomical valves or sphincters, as was previously supposed. The structural strength of the air and blood capillaries is derived from: the interdependence between the air and blood capillaries; a tethering effect between the closely entwined respiratory units; the presence of epithelial–epithelial cell connections (retinacula or cross‐bridges) that join the blood capillaries while separating the air capillaries; the abundance and intricate arrangement of the connective tissue elements, i.e. collagen, elastin, and smooth muscle fibres; the presence of type‐IV collagen, especially in the basement membranes of the blood–gas barrier and the epithelial–epithelial cell connections; and a putative tensegrity state in the lung. Notwithstanding the paucity of free surface pulmonary macrophages, the respiratory surface of the avian lung is well protected from pathogens and particulates by an assortment of highly efficient phagocytic cells. In commercial poultry production, instead of weak pulmonary cellular defence, stressful husbandry practices such as overcrowding, force‐feeding, and intense genetic manipulation for rapid weight gain and egg production may account for the reported susceptibility of birds to aerosol‐transmitted diseases.     

Ultrastructural observations on the lung of the emperor penguin (Aptenodytes forsten)

Summary Of all avian species the emperor penguin is the best adapted bird to attain the greatest diving depths and diving durations. Therefore the lung of this bird was investigated with electron-microscopic, i.e., freeze-fracture and thin-section methods. The parabronchi are surrounded by bundles of smooth muscle cells innervated by varicosities of autonomic nerves. The parabronchial epithelium is flat, bears a few microvilli and does not show any conspicuous ultrastructural specializations; only individual cells contain secretory granules. The atrial epithelial cells bear apical microvilli and are interconnected by adhering and tight junctions (5–10 sealing strands), the latter presumably forming an effective barrier against paracellular fluid movements. The cells contain lamellar inclusions of two types: (i) round membrane-bounded granules, the lamellar content of which is fixation-labile, and (ii) large polymorphic compact deposits of well-preserved lamellae. In both types of inclusions the individual lamellae can be of trilaminar appearance, whereas their fracture faces are smooth. Lamellar material also covers the epithelium of atria, infundibula and air capillaries. In thin areas the diameter of the morphological blood-air barrier measures 220–330 nm. Usually the endothelium of the blood capillaries is thicker (40–180 nm) than the air capillary epithelium (25–150 nm). Both epithelium and endothelium are interconnected by tight junctions, which seem to be more extensive and presumably tighter in the epithelium than in the endothelium. Frequently the common basal lamina is the thickest individual component of the blood-air barrier, measuring between 170–230 nm. Often collagen fibrils occur in this area of the barrier. In comparison with that of other birds the entire blood-air barrier of the emperor penguin is relatively thick, probably owing to an adaptation of the lung tissue which must resist high hydrostatic pressure during diving excursions.     

Ultrastructural characterization of the pulmonary cellular defences in the lung of a bird,the rock dove,Columba livia

Free (surface) avian respiratory macrophages (FARMs) were harvested by lavage of the lung/air-sac system of the rock dove, Columba livia. The presence of FARMs in the atria and infundibula was confirmed by scanning electron microscopy. The respiratory system has developed several cellular defence lines that include surface macrophages, epithelial, subepithelial and interstitial phagocytes, and pulmonary intravascular macrophages (PIMs). Hence, C. livia appears to have a multiple pulmonary cellular protective armoury. Ultrastructurally, the FARMs and the PIMs were similar to the corresponding cells of mammals. The purported high susceptibility of birds to respiratory diseases, a state that has largely been deduced from morbidities and mortalities of commercial birds, and which has chiefly been attributed to paucity of the FARMs, is not supported by the present observations.     

The ultrastructure of the lung of two newborn marsupial species,the northern native cat,Dasyurus hallucatus,and the brushtail possum,Trichosurus vulpecula

Summary The lungs of newborn northern native cats, Dasyurus hallucatus and newborn brushtail possums, Trichosurus vulpecula were examined by both light and electron microscopy. The native cat has a birth weight of 18 mg after a gestation of about 21 days, whereas the brushtail possum weights 200 mg at birth and has a gestation period of 17.5 days. The lungs of the native cat are two large respiratory sacs, with a respiratory lining of squamous cells and surfactant-secreting cells. The capillaries are located within the connective tissue just below this respiratory epithelium. The visceral covering of the lung is formed by squamous cells. The lungs of the possum are composed of numerous large respiratory sacs which are separated by connective tissue septa in which the capillaries are located. The sacs, as in other species, are lined with squamous cells and surfactant secreting cells. It is proposed that the structure of the lung of the newborn marsupial is related more to the size of the newborn rather than to the length of the gestation period.     

Morphogenesis of the laminated, tripartite cytoarchitectural design of the blood-gas barrier of the avian lung: a systematic electron microscopic study on the domestic fowl, Gallus gallus variant domesticus

Formation of a thin blood-gas barrier in the respiratory (gas exchange) tissue of the lung of the domestic fowl, Gallus gallus variant domesticus commences on day 18 of embryogenesis. Developing from infundibulae, air capillaries radiate outwards into the surrounding mesenchymal (periparabronchial) tissue, progressively separating and interdigitating with the blood capillaries. Thinning of the blood-gas barrier occurs by growth and extension of the air capillaries and by extensive disintegration of mesenchymal cells that constitute transient septa that divide the lengthening and anastomosing air capillaries. After they contact, the epithelial and endothelial cells deposit intercellular matrix that cements them back-to-back. At hatching (day 21), with a thin blood-gas barrier and a large respiratory surface area, the lung is well prepared for gas exchange. In sites where air capillaries lie adjacent to each other, epithelial cells contact directly: intercellular matrix is lacking.     

The fine structure of the parabronchi and the gas exchange area of the Adelie penguin lung

The parabronchi of the Adelie penguin are endowed with wide atria forming pockets between a loose meshwork of bundles of smooth muscle cells lining the parabronchial lumen. The atrial epithelium is of variable thickness and bears numerous microvilli, which are overlain by/or embedded in sheets or whorls of lamellar material ("trilaminar substance", diameter of one lamella 8 ..10 nm) forming layers of very variable thickness. The cells contain either stacks or whorls of this material or roundish lamellated bodies, and are interconnected by desmosomal contacts as well as what presumably represent tight junctions. Underneath the epithelium and within the bundles of muscle cells regularly nerve fibres have been found. The diameter of the morphological air/blood barrier is about 165...210 nm in thin areas, excluding a 12...20 nm thick layer covering the luminal plasma membrane of the air capillary epithelium. The blood capillary endothelium ordinarily is markedly thicker (40...250 nm) than the air capillary epithelium (17...25 nm). The basal lamina between endo- and epithelium is a uniform structure measuring about 95...105 nm. The endothelial cells are interconnected by desmosomal and probably tight junctions.     

Ultrastructural and morphometric study of the lung of the European salamander,Salamandra salamandra L.

Ultrastructural and morphometric investigations were performed on the lung of the European salamander, Salamandra salamandra L. Folds of first and second order are covered with a ciliated epithelium containing goblet cells. The respiratory surface of the lung is lined by a single type of cell which, in amphibians, combines features of type I and type II alveolar cells of the mammalian lung. In the salamander the respiratory and ciliated epithelial cells as well as goblet cells possess electron dense and lucent vesicles in their cytoplasm as well as lamellar bodies. A small amount of surfactant, composed most probably of phospholipids and mucopolysaccharides, was observed covering the entire inner surface of the lung. Morphometric methods were used to determine the dimensions of the perinuclear region of pneumocytes, the thickness of the air-blood barrier and lung wall, and also the diameter of capillaries. The thickness of the respiratory air-blood barrier was found to be considerably higher than that of the corresponding barrier in mammals.     

Histology of the trachea and lung of Siphonops annulatus (Amphibia, Gymnophiona)

The structure of the trachea and lung of Siphonops annulatus was studied in ten specimens of routinely fed animals. The trachea is constituted mainly by incomplete cartilage rings lined by a respiratory epithelium (ciliated and mucous cells) with variable morphology according to the region observed. A rich vascularization of this organ suggests its participation in blood-air gas exchange. The right lung in this species is developed and the left one is atrophied. This organ is constituted mainly by longitudinal septa formed by connective tissue, smooth muscle cells and blood capillaries. These structures are covered by pneumocytes of one type only, which present cytoplasmic particles that have been related with surfactant activity described in the lung of Gymnophiona.     

Der Atemapparat der V?gel und ihre lokomotorische und metabolische Leistungsf?higkeit

Zusammenfassung Zum Verständnis der besonderen Struktur- und Funktionsprinzipien des Atemapparates der Vögel werden die spezielle Bauweise des Vogelrumpfes und die bei den Vögeln hochdifferenzierte Septierung ihrer Leibeshöhle dargestellt. Sodann werden der Bau der Lungen und ihres Bronchialsystems beschrieben sowie die Lage und Verbindungen der Luftsäcke und ihrer Divertikel. Die Schilderung der Atembewegungen des Vogelrumpfes ergibt die Grundlage für die Diskussion der Ventilation der Vogellunge. Auf die Darstellung des Aufbaus der Parabronchien, der funktionellen Baueinheit für den Gasaustausch in der Vogellunge, sowie ihres Gefäßsystems folgen die Daten über den quantitativen Aufbau des Lungen-Luftsacksystems von Kolibris bis zu Schwänen und ihrer morphometrisch bestimmten Austauschkapazitäten. Anschließend werden die physiologischen Daten über den Gasaustausch in der Vogellunge und den Transport der Atemgase durch das Blut diskutiert und die Kenntnisse über die sensorische und neuronale Steuerung von Atmung und Gasaustausch aufgeführt. Sodann werden die vorhandenen Daten über den qualitativen und quantitativen Aufbau der Flugmuskulatur und des Herz-Kreislaufsystems zusammengestellt und ihre körpergrößenabhängigen Beziehungen und deren funktionelle Konsequenzen diskutiert. Abschließend wird die Evolution der Vögel als hochentwickelter Warmblüter diskutiert, die mit ihren zu Dauerleistung befähigten Schlagfliegern wie vielen Zugvögeln extrem gesteigerte metabolische und lokomotorische Leistungen vollbringen, von denen sich die als Bodenvögel spezialisierten größeren Hühnervögel mit ihrer sehr beschränkten physiologischen Leistungsfähigkeit aber deutlich unterscheiden.

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The respiratory apparatus of birds and their locomotory and metabolic efficiency

Summary The structural and functional principles of the avian respiratory apparatus and the differences with respect to the respiratory apparatus of mammals have been well understood from published investigations since 1970 (for review articles see Duncker 1971, 1978a, 1979, 1983, Fedde 1986, Seller 1987, King & McLelland 1989). The various and great structural and functional differences between birds and mammals are often ignored or have only rarely found adequate treatment. In the face of the fundamental structural uniformity of birds, the large differences which exist in the functional efficiency of their respiratory and cardiovascular apparatus are not generally realized. This applies to an even greater extent to their interaction and cooperation with the locomotory apparatus, especially when comparing the well-known domestic fowl with the more rarely examined wild and migratory birds. Migratory birds are vertebrates whose respiratory, cardiovascular und locomotory apparatus are capable of the highest sustainable effort. In contrast, the physiology of larger fowl-like birds is not designed for the purpose of hard and sustained exercise, but in accordance with their anaerobically performed short escape flight, the capacity of their cardiovascular and respiratory systems is greatly reduced. Fowl-like birds are therefore suitable only to a very limited extent to afford a functional understanding of avian construction. With this in mind the present article reviews the structure of the respiratory apparatus of birds with its important qualitative and quantitative structural and functional characteristics and the functionally important and correlated aspects of the cardiovascular and locomotory systems. Against this background these avian systems are compared with the functional characteristics of the corresponding mammalian systems.The lung air sac system of birds is related to the special construction of the avian trunk and the highly differentiated septation of the body cavity of birds (Fig. 1; Duncker 1971, 1979). The construction of the trunk wall and the septation of the body cavity are responsible for the volume constancy of the pleural cavity during all respiratory movements, thus establishing the necessary structural conditions for the development of the rigid parabronchial lung. Only under these conditions can the parabronchial air capillaries remain extended and air-filled. The ventilation of this rigid avian lung is achieved by the volume changes of the air sacs, whereby the air flow through the parabronchi is directed aerodynamically. The relative rigidity of the avian trunk with its highly specialized articulations between the spinal column, which is more or less immobile, and the ribs and the sternum enables large excursions for the breathing movements so that ventilation of the air sacs can occur with a large amplitude and at minimum pressure differences. By virtue of the large volume elasticity (compliance) of the air sacs the respiratory apparatus of birds works as a low-pressure system. In addition, owing to the special construction of the shoulder girdle of birds as well as to the arrangement of the large flight muscles and the air sac diverticula between the cranial shoulder girdle and the frontal thorax, complete dissociation of respiratory and flight movements can result, which allows birds to fly and to breath with different, even changing frequencies, which are related specifically to body size (Fig. 5; Berger & Hart 1974).In contrast to this avian construction, the mammalian trunk, especially in small to mediumsized mammals, possesses a strongly elastic thorax and a highly pliant lumbar vertebral column, which result in a coupling between locomotory and respiratory movements. The thoracic cage and the cervical and thoracic vertebral column represent the crucial origins for the musculature of the shoulder girdle including its highly mobile scapula. The extensive movements of the lumbar vertebral column are substantial for the locomotory movements of the hind limb. Owing to its small volume elasticity (compliance) and powerful retractile forces, the broncho-alveolar mammalian lung requires larger pressure gradients for full inspiration. Thus, the thorax musculature and a muscularized diaphragm are well developed. In addition to the performance of its inspiratory movements, the diaphragm must also counteract the high intraabdominal pressures, which are an inevitable consequence of the extensive movements of the lumbar vertebral column and the active abdominal muscles, especially during rapid locomotion. Thus, the body cavities of mammals including the pleural cavity are high-pressure systems, which have multiple, not yet investigated effects on the structure and function of different organ systems.Just as the structure and function of the lung air sac apparatus of birds differ fundamentally from the lungs of mammals, the ontogenetic development of the respiratory apparatuses of these two classes are also basically different. In viviparous mammals the lung develops similarly to all lungs of amniotes secreting pulmonary fluid, which fills the lumina of the developing bronchial tree including its respiratory portion. With the onset of respiratory movements in the late embryological/fetal development, this pulmonary fluid comes into partial exchange with the amniotic fluid. During parturition, a portion of the pulmonary fluid is squeezed out by the compression of the fetus. The remaining pulmonary fluid, which is sucked into the terminal ends of the respiratory bronchial tree by the first breath, will be resorbed in the first few hours of life by active transport of the alveolar epithelium and the endothelium of the alveolar capillaries. Thus, the mammalian lung, which has developed a thin exchange surface in the sacculi or alveoli of the respiratory bronchial tree, can aerate most of the exchange surface with the first breath at birth so that it can instantly take over the function of gas exchange from the placenta (Duncker 1990).The avian lung and its principal air sacs develop in the embryo, which is emersed in the amniotic fluid of the egg. Similarly, the lumina of the growing bronchial system are filled with pulmonary fluid. Towards the end of the incubation period the air capillaries start to sprout from the tubuli of the fluid-filled anlagen of the parabronchi between the surrounding blood capillaries. One to three days before hatching, after having swallowed the remaining amniotic fluid, and initiated regular breathing movements, the chick perforates the membrane into the air chamber of the egg (Duncker 1978b, Piiper 1978). Thus, not only the primary and secondary bronchi of the lung and the large air sacs are ventilated, but also the lumina of the parabronchi. The parabronchial air capillaries, which continue growing and sprouting, are filled with pulmonary fluid, which is now absorbed by the epithelium of the air capillaries and the endothelium of the blood capillaries. Depending upon the size of the egg and the duration of the incubation, the air capillaries are completely air-filled after one to two days. With this ventilation and the increasing filling of the air capillaries with air, they progressively assume the gas exchange function, which up to this time has been carried out by the chorioallantoic membrane. The latter is closely attached to the inside of the shell membrane. At the end of this process the embryo hatches. As early as in the embryological development the pleural cavities maintain volume constancy during all respiratory and body movements. The rigid lungs, which grow together with the pleural cavity walls during their embryological development, attain their gas exchange ability after ventilation of the bronchial system only through the resorption of the pulmonary fluid by the epithelium of the air capillaries. The avian lung therefore can only attain its functional capacity for gas exchange by a temporal overlapping of gas exchange by the chorioallantoic membrane with the respiration of air by the lung, which is only possible in a hard-shelled egg. Thus, the highly differentiated, non-inflatable lung structure in birds is inevitably bound to development in a hard-shelled egg (Duncker 1978b).All birds possess a respiratory apparatus that in principle is comparably constructed. They differ vastly, however, in the extent to which the diffusion capacity of their lungs is developed and thus in their metabolic and locomotory efficiency. Those capable of sustained, efficient flight, e.g. hummingbirds to large migratory birds, possess lungs with an exchange capacity that is higher than that of comparably large mammals by a factor of 6 to 8 (Fig. 27). The relative weight of the heart of birds and their cardio-vascular transport capacity are correspondingly larger than in comparable mammals and they have a somewhat larger relative blood volume (Duncker & Güntert 1985). By virtue of this construction, sustainably flying birds can supply their flight musculature, which consists to a large extent or completely of aerobic muscle fibers, which are sufficient for a continuous flapping type flight activity. However, a crucial body-size relationship arises within these functional interdependencies, since the hearts of larger animals can only pump a relatively smaller blood volume per time unit owing to the size-dependent maximum pulse rate. Accordingly, large ducks, geese and swans adapt to these scale problems by a reduction in their relative flight muscle mass, which entailes them using a longer time for take-off with violent flapping of their wings (Fig. 28). Large water birds can perform such a long take-off only on water, out of reach of preying terrestrial hunters.Large land birds, like the large fowl-like birds, owe their survival to the fact that they can save themselves from stalking hunters by a direct lifting flight, in order to escape into a tree or by sweeping off to a safe distance. For a direct lifting flight, however, a flight muscle mass of at least 20% of their total body weight is necessary. Larger sustainably flying birds had to reduce their aerobic, red flight musculature to 13–12% of their total body mass in accordance with the described body-size dependent cardio-vascular blood transport capacity. Based on these scaling interdependencies, the medium- to large-sized fowl-like birds could not differentiate aerobic fibers in their flight musculature. Because of the requirement that flight musculature must amount to 20% of body weight for lifting stroke flight, they were able to differentiate their flight muscles only as anaerobic, white fibers and thus they can fly strongly but fatigue very quickly (Fig. 28). Accordingly, the heart and circulatory system has also differentiated to the physiological needs of the flight musculature. Thus, the size of the heart and the cardio-vascular transport capacity of larger fowl-like birds are reduced to half of or less than the heart size and transport capacity of comparably large sustainably flying birds, and they possess an even more greatly reduced diffusion capacity of their lungs. Medium-sized and large fowl-like birds passed up the development of the ability for sustainable higher metabolic permormance during their very special evolution towards a more terrestrially based, running bird with short escape flight. The fowl-like birds, adapted very well to their specific habitat, therefore are not an appropiate example of a typical bird with the ability for long-term, flapping flight and high metabolic achievement.

     

The respiratory system of the genusCallithrix,the South American monkey

It has been described the cytology of the following parts of the respiratory system of some South American primates:Callithrix jacchus andCallithrix argentata melanura. The nasal cavities are divided into three parts: a vestibule, covered with a stratified nonkeratinized squamous epithelium; the respiratory portion, consisting of a pseudostratified columnar ciliated epithelium with goblet cells and the olfactory portion which is also covered with a high respiratory epithelium without goblet cells. The trachea is lined with a mucous membrane, whose epithelium is pseudostratified columnar ciliated with scarce goblet cells in the proximal portion unlike to the distal one. In the dorsal portion of the trachea, at the level of the gap between the two ends of incomplete cartilaginous rings, the epithelial lining is of transitional type. The incomplete hyaline cartilaginous rings present centers of calcification. The right and left lungs consist of two and three lobes respectively characteristic for these species, but they are not divided into lobules by connective tissue as in other ones. The bronchi, bronchioles and the respiratory portion, respiratory bronchioles, alveolar ducts, alveolar sacs, and alveoli present the typical respiratory structure with exception of their cartilaginous configuration; the cartilage continues as far as the respiratory bronchioles and alveolar ducts. These last structures are formed by a thin squamous epithelium, in which we observed two types of alveolar lining cells. This work was supported by grants from the Consejo Nacional de Investigaciones Cientificas y Técnicas (CONICET) and EHIGE program. Postgraduated fellow from CONICET. established Investigator and Director of EHIGE (Estudio Histológico comparado del Sistema de Glándulas Endócrinas) from CONICET.     

Lungs of the gecko Rhacodactylus leachianus (Reptilia: Gekkonidae): a correlative gross anatomical and light and electron microscopic study

The lungs of the New Caldeonian gecko Rhacodactylus leachianus were examined by means of gross dissection and light and electron microscopy. This tropical species, which is the largest living gecko, possesses two simple, single-chambered lungs. Right and left lungs are of similar size and shape. The lung volume (27.2 ml.100 g-1) is similar to that of the tokay (Gekko gecko) but differs in that the gas exchange tissue is approximately homogeneously distributed, and the parenchymal units (ediculae) are very large, approximately 2 mm in diameter. The parenchymal depth varies according to the location in the lung, being deepest near the middle of the lung and shallowest caudally. Scanning and transmission electron microscopy reveal an unusual distribution of ciliated cells in patches on the edicular walls as well as on the trabeculae. Secretory cells are very numerous, particularly in the bronchial epithelium, where they greatly outnumber the ciliated cells. The secretory cells form a morphological continuum characterized by small secretory droplets apically and large vacuoles basally. This continuum includes cells resembling type II pneumocytes but which are devoid of lamellar bodies. Type I pneumocytes similar to those of other reptiles cover the respiratory capillaries, where they form a thin, air-blood barrier together with the capillary endothelial cells and the fused basement laminae. The innervation, musculature, and vascular distribution in R. leachianus are also characterized. Apparent simplification of the lungs in this taxon may be related to features of its sluggish habits, whereas peculiarities of cell and tissue composition may reflect demands of its mesic habitat.     

Gross and fine anatomy of the respiratory vasculature of the mudskipper,Periophthalmodon schlosseri (Gobiidae: Oxudercinae)

To illustrate vascular modification accompanying transition from aquatic to amphibious life in gobies, we investigated the respiratory vasculatures of the gills and the bucco‐opercular cavities in one of the most terrestrially‐adapted mudskippers, Periophthalmodon schlosseri, using the corrosion casting technique. The vascular system of Pn. schlosseri retains the typical fish configuration with a serial connection of the gills and the systemic circuits, suggesting a lack of separation of O₂‐poor systemic venous blood and O₂‐rich effluent blood from the air‐breathing surfaces. The gills appear to play a limited role in gas exchange, as evidenced from the sparsely‐spaced short filaments and the modification of secondary lamellar vasculature into five to eight parallel channels that are larger than red blood cell size, unlike the extensive sinusoidal system seen in purely water‐breathing fishes. In contrast, the epithelia of the bucco‐opercular chamber, branchial arches, and leading edge of the filaments are extensively laden with capillaries having a short (<10 μm) diffusion distance, which strongly demonstrate the principal respiratory function of these surfaces. These capillaries form spiral coils of three to five turns as they approach the epithelial surface. The respiratory capillaries of the bucco‐opercular chamber are supplied by efferent blood from the gills and drained by the systemic venous pathway. We also compared the degree of capillarization in the bucco‐opercular epithelia of Pn. schlosseri with that of the three related intertidal‐burrowing gobies (aquatic, non‐air‐breathing Acanthogobius hasta; aquatic, facultative air‐breathing Odontamblyopus lacepedii; amphibious air‐breathing Periophthalmus modestus) through histological analysis. The comparison revealed a clear trend of wider distribution of denser capillary networks in these epithelia with increasing reliance on air breathing, consistent with the highest aerial respiratory capacity of Pn. schlosseri among the four species. J. Morphol. 2011. © 2011 Wiley‐Liss, Inc.