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The terminal respiratory units of the gas exchange tissue of the avian lung, the air capillaries (ACs) and the blood capillaries (BCs), are small and rigid: the basis of this mechanical feature has been highly contentious. Because the strength of the blood-gas barrier (BGB) of the mammalian lung has been attributed to the presence of type-IV collagen (T-IVc), localization of T-IVc in the basement membranes (BM) of the BGB and the epithelial-epithelial cell connections (E-ECCs) of the exchange tissue of the lung of the avian (chicken) lung was performed in order to determine whether it may likewise contribute to the strength of the BGB. T-IVc was localized in both the BM and the E-ECCs. As part of an integrated fibroskeletal scaffold on the lung, T-IVc may directly contribute to the strengths of the ACs and the BCs.

Recent findings are reported about certain aspects of the structure and function of the mammalian and avian lungs that include (a) the architecture of the air capillaries (ACs) and the blood capillaries (BCs); (b) the pulmonary blood capillary circulatory dynamics; (c) the adaptive molecular, cellular, biochemical, compositional, and developmental characteristics of the surfactant system; (d) the mechanisms of the translocation of fine and ultrafine particles across the airway epithelial barrier; and (e) the particle-cell interactions in the pulmonary airways. In the lung of the Muscovy duck Cairina moschata, at least, the ACs are rotund structures that are interconnected by narrow cylindrical sections, while the BCs comprise segments that are almost as long as they are wide. In contrast to the mammalian pulmonary BCs, which are highly compliant, those of birds practically behave like rigid tubes. Diving pressure has been a very powerful directional selection force that has influenced phenotypic changes in surfactant composition and function in lungs of marine mammals. After nanosized particulates are deposited on the respiratory tract of healthy human subjects, some reach organs such as the brain with potentially serious health implications. Finally, in the mammalian lung, dendritic cells of the pulmonary airways are powerful agents in engulfing deposited particles, and in birds, macrophages and erythrocytes are ardent phagocytizing cellular agents. The morphology of the lung that allows it to perform different functions-including gas exchange, ventilation of the lung by being compliant, defense, and secretion of important pharmacological factors-is reflected in its "compromise design."

In the avian lung, inhaled air is shunted past the openings of the medioventral secondary bronchi (MVSB) by a mechanism termed 'inspiratory aerodynamic valving' (IAV). Sizes and orientations of the trachea (Tr), syrinx (Sx), extrapulmonary primary bronchus (EPPB), intrapulmonary primary bronchus (IPPB), MVSB, mediodorsal secondary bronchi (MDSB), lateroventral secondary bronchi (LVSB) and the ostium (Ot) were determined in the ostrich, Struthio camelus. Air flow was simulated through computationally generated models and its dynamics analysed. The 'truncated normal model' (TNM) consisted of the Tr, Sx, EPPB, IPPB, MVSB and the Ot. For the 'inclusive normal model' (INM), the MDSB and the LDSB were added. Variations of these models included the 'truncated MVSB1 rotated model' (T(MVSB1)RM), the 'truncated constriction fitted model' (TCFM) and the 'inclusive MVSB1 rotated model' (I(MVSB1)RM). In the TNM, the T(MVSB1)RM and the TCFM, the air flow exited through the MVSB while for the INM and the I(MVSB1)RM, very little of it did: IAV did not occur in the partial models. In the I(MVSB1)RM, rotating the MVSB1 clockwise did not affect IAV. The incomplete models may be faulty because the velocity/pressure profiles in different parts of the interconnected airways form an integrated functional continuum in which different parts of the system considerably impact on each other.

We have previously reconstructed the gas exchange tissue of the adult muscovy duck, Cairina moschata using a method of manually aligning sections and tracing the contours of the components of the gas exchange tissue. This reconstruction method demonstrated that the air capillaries are comprised of an expanded globular part interconnected by narrow air channels. The blood capillaries completely surround the air capillaries forming an anastomosing meshwork of short segments. However, the resulting reconstruction was limited in scope because of the laborious process of tracing the profiles of each component through the sequence of micrographs. We have now reconstructed a larger proportion of the exchange tissue by using a cross-correlation based alignment strategy and have demonstrated that the staining intensity of each of the exchange tissue components is sufficiently different to allow them to be identified by simple filtering and thresholding. The resulting reconstructions sample a much larger proportion of the exchange tissue and demonstrate the heterogeneity of structures from different locations in the parabronchus. We have shown that a sheet-flow-type arrangement of blood capillaries surrounds the infundibulum; this represents an unexpected functional convergence with the arrangement of blood capillaries surrounding the mammalian alveoli. It is feasible, using this reconstruction strategy, to analyse the exchange tissue of a large number of avian species in order to determine structural correlates of function. The resulting reconstructions could be analysed in order to determine the basis of the functional efficiency and rigidity of the avian lung.

Among the air-breathing vertebrates, the respiratory system of birds, the lung-air sac system, is remarkably complex and singularly efficient. The most perplexing structural property of the avian lung pertains to its exceptional mechanical strength, especially that of the minuscule terminal respiratory units, the air- and the blood capillaries. In different species of birds, the air capillaries range in diameter from 3 to 20 micro m: the blood capillaries are in all cases relatively smaller. Over and above their capacity to withstand enormous surface tension forces at the air-tissue interface, the air capillaries resist mechanical compression (parabronchial distending pressure) as high as 20 cm H(2)O (2 kPa). The blood capillaries tolerate a pulmonary arterial vascular pressure of 24.1 mmHg (3.2 kPa) and vascular resistance of 22.5 mmHg (3 kPa) without distending. The design of the avian respiratory system fundamentally stems from the rigidity (strength) of the lung. The gas exchanger (the lung) is uncoupled from the ventilator (the air sacs), allowing the lung (the paleopulmonic parabronchi) to be ventilated continuously and unidirectionally by synchronized bellows like action of the air sacs. Since during the ventilation of the lung the air capillaries do not have to be distended (dilated), i.e., surface tension force does not have to be overcome (as would be the case if the lung was compliant), extremely intense subdivision of the exchange tissue was possible. Minuscule terminal respiratory units developed, producing a vast respiratory surface area in a limited lung volume. I make a case that a firm (rigid) rib cage, a lung tightly held by the ribs and the horizontal septum, a lung directly attached to the trunk, specially formed and compactly arranged parabronchi, intertwined atrial muscles, and tightly set air capillaries and blood capillaries form an integrated hierarchy of discrete network system of tension and compression, a tensegrity (tensional integrity) array, which absorbs, transmits, and dissipates stress, stabilizing (strengthening) the lung and its various structural components.

In the embryonic lung of the domestic fowl, Gallus gallus variant domesticus, hematogenetic and vasculogenetic cells become ultrastructurally clear from day 4 of development. In the former group of cells, filopodial extensions coalesce, cytoplasm thickens, and accumulating hemoglobin displaces the nucleus peripherally while in the latter, conspicuous filopodial extensions and large nuclei develop as the cells assume a rather stellate appearance. From day 5, erythrocytes and granular leukocytes begin forming from cytoarchitecturally cognate hematogenetic cells. The cells become distinguishable when hemoglobin starts to accumulate in the erythroblasts and electron dense bodies form in the leukoblasts. Vasculogenesis begins from day 7 in different areas of the developing lung: erthrocytes (but not granular leukocytes) appear to attract committed vasculogenetic cells (angioblasts) that form an endothelial lining and vessel wall. Arrangement of angioblasts around forming blood vessels sets the direction along which the vessels sprout (angiogenesis). In some areas of the developing lung, through what seems like an inductive erythropoietic process, arcades of erythrocytes organize. Once endothelial cells surround such continuities, discrete vascular units organize. By day 10, the major parts of the in-built (intrinsic) pulmonary vasculature are assembled. Complete pulmonary circulation (i.e., through the exchange tissue) is not established until after day 18 when the blood capillaries start to develop. Since the precursory erythrocytes do not have a respiratory role, it is imperative that de novo erythropoiesis is essential for vasculogenesis. Diffuse (fragmentary) development and subsequent piecemeal assembly of the pulmonary vascular system may explicate the fabrication of a complex circulatory architecture that grants cross-current, counter-current, and multicapillary serial arterialization designs in the exchange tissue of the avian lung. The exceptional respiratory efficiency of the avian lung is largely attributable to the geometries (physical interfacing) between the bronchial and vascular elements at different levels of morphological organization.

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.

In the avian lung, the bronchial system forms from epithelial (endodermal) cells. The intrapulmonary primary bronchus is the focal point of airway development. It originates secondary bronchi (SB) along its proximal-distal extent and parabronchi (tertiary bronchi) arise from and connect the SB. From as early as day 3.5, fibroblast growth factor-2 (FGF-2) is diffusely expressed in the epithelial and mesenchymal cells. Up-regulation of FGF-2 in discrete areas of the developing lung seem to set the growth rate, trajectories followed, areas appropriated, three-dimensional symmetry and coupling of the airways. Expressed early in development and persisting into the incubation period, FGF-2 may be involved in the formation of the avian lung. Morphogenetic differences between the avian and the mammalian lungs may explain the existing structural contrarieties.

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.

Over the evolutionary continuum, animals have faced similar fundamental challenges of acquiring molecular oxygen for aerobic metabolism. Under limitations and constraints imposed by factors such as phylogeny, behaviour, body size and environment, they have responded differently in founding optimal respiratory structures. A quintessence of the aphorism that 'necessity is the mother of invention', gas exchangers have been inaugurated through stiff cost-benefit analyses that have evoked transaction of trade-offs and compromises. Cogent structural-functional correlations occur in constructions of gas exchangers: within and between taxa, morphological complexity and respiratory efficiency increase with metabolic capacities and oxygen needs. Highly active, small endotherms have relatively better-refined gas exchangers compared with large, inactive ectotherms. Respiratory structures have developed from the plain cell membrane of the primeval prokaryotic unicells to complex multifunctional ones of the modern Metazoa. Regarding the respiratory medium used to extract oxygen from, animal life has had only two choices--water or air--within the biological range of temperature and pressure the only naturally occurring respirable fluids. In rarer cases, certain animals have adapted to using both media. Gills (evaginated gas exchangers) are the primordial respiratory organs: they are the archetypal water breathing organs. Lungs (invaginated gas exchangers) are the model air breathing organs. Bimodal (transitional) breathers occupy the water-air interface. Presentation and exposure of external (water/air) and internal (haemolymph/blood) respiratory media, features determined by geometric arrangement of the conduits, are important features for gas exchange efficiency: counter-current, cross-current, uniform pool and infinite pool designs have variably developed.

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.

Over its life, an organism's survival and success are determined by the inventory of vital adaptations that its progenitors have creatively appropriated, devised and harnessed along the evolutionary pathway. Such conserved attributes provide the armamentarium necessary for withstanding the adverse effects of natural selection. Refinements of the designs of the respiratory organs have been critical for survival and phylogenetic advancement of animal life. Gas exchangers have changed in direct response to the respiratory needs of whole organisms in different environmental states and conditions. Nowhere else is the dictum that in biology 'there are no rules but only necessities' more manifest than in the evolutionary biology of the gas exchangers. The constructions have been continually fashioned and refined to meet specific needs. Solutions to common respiratory needs have been typified by profound structural convergence. Over the evolutionary continuum, as shifts in environmental situations occurred, infinitely many designs should theoretically have emerged. Moreover, without specific selective pressures and preference for certain designs, considering that there are only two naturally occurring respirable fluid media (air and water), air-lungs, water-lungs, air-gills and water-gills would have formed to similar extents. Factors such as body size, phylogenetic level of development, respiratory medium utilized and habitats occupied have permutatively prescribed the design of the gas exchangers. The construction of the modern gas exchangers has eventuated through painstaking cost-benefit analysis. Trade-offs and compromises have decreed only a limited number of structurally feasible and functionally competent outcomes. The morphological congruity (analogy) of the gas exchangers indicates that similar selective pressures have compelled the designs. Solutions to metabolic demands for molecular O2 have only differed in details. Passive physical diffusion, for example, is the ubiquitous method of transfer of O2 across biological tissues. Gills, evaginated gas exchangers, were the primordial respiratory organs that evolved for water breathing, whereas lungs (invaginated gas exchangers) developed for terrestrial (air) breathing. Transitional (= bimodal = amphibious) breathing has evolved in animals with specialized organs that extract O2 from both water and air. Lungs are tidally (= bidirectionally) ventilated, while gills are unidirectionally ventilated, a feature that allows the highly efficient counter-current disposition between blood and water. Since animals occupy inconstant environmental milieus and their metabolic states vary, gas exchangers are designed to operate optimally across a spectrum of conditions that range from resting to exercise and even under hypoxia. Inbuilt structural and functional flexibility provides the requisite safety factors that allow adjustments to modest pressures. The fundamental structural features that determine the respiratory function of a gas exchanger are respiratory surface area, thickness of the blood-water/gas (tissue) barrier and volume of the pulmonary capillary blood. The diffusing capacity of a gas exchanger correlates directly with the surface area and inversely with the thickness of the blood-water/gas (tissue) barrier. An extensive surface area is generated in gills by extensive stratification of the gas exchanger and in lungs by profuse internal subdivision. Compartmentalization yields small terminal gas exchange compartments that compel greater commitment of energy to ventilate. The surfactant, a phospholipid lining, reduces the forces of surface tension at the air-water interface. This attenuates the propensity of physical collapse of the minute gas exchange units and minimizes the cost of ventilation. The surfactant characterizes all the gas exchangers derived from the piscine air bladder. In the lower air-breathing vertebrates, such as the lungfishes (Dipnoi), amphibians and certain reptiles, the pneumocytes are not differentiated into type I and II cells, as is the case in the lungs of the higher vertebrates-birds and mammals. It is envisaged that in endotherms, the overall numerical density of the pneumocytes and hence the O2 consumption of the gas exchangers may be reduced and a thin blood-gas (tissue) barrier generated, factors that enhance respiratory efficiency. The thin blood-gas (tissue) barriers, for example, those of the mammalian (in the respiratory sections of the interalveolar septum) and avian lungs, consist of an epithelial cell and an endothelial cell with a common basement membrane. An interstitial space occurs in the blood-air/water (tissue) barriers of the gas exchangers of fish gills and lungs of lungfishes, amphibians, reptiles and in the supportive parts of the interalveolar septum of the mammalian lung. Collagen, elastic tissue, nerves, lymphatic vessels and smooth muscle elements are found in the interstitial space. The thickness of the blood-air/water (tissue) barrier allometrically changes very little. This suggests that the thicknesses of the blood-water/air (tissue) barriers have been optimized. The presentation and exposure to the gas exchange media (water/air to blood), features dictated by the geometry and arrangements of the structural components of the gas exchangers, contribute greatly to respiratory efficiency. The countercurrent presentation between water and blood in fish gills is the most efficient design in the evolved gas exchangers: It was imperative for survival in water, a medium that contains relatively less O2 and is more expensive to breathe. In the evolved vertebrate gas exchangers, the exposure of blood to air is best manifested in the diffuse design of the avian lung, where the capillary blood is literally suspended in a three-dimensional air space, the blood being exposed to air virtually across the entire blood-gas (tissue) barrier. A double capillary design occurs in the lungs of amphibians and generally those of reptiles, whereas a single capillary design commonly occurs in those of adult mammals. The capillary loading (the ratio of the volume of the capillary blood to the surface area across which blood is exposed to air) in lungs with a double capillary arrangement is high and manifests a poor design. On the other hand, the low capillary loading that characterizes the single capillary system indicates better exposure of blood to air and greater respiratory capacity. Fractal geometry features in the construction of the gas exchangers. The highly versatile design allows the gas exchangers to function optimally under different conditions and circumstances and to maintain congruent morphologies over a wide range of body size, shape and metabolic capacities. At the gas exchange level, sheet-flow design preponderates in the evolved gas exchangers; blood is efficiently exposed to the external respiratory medium. The respiratory capacity of a gas exchanger is comprehensively granted by refinements of structural features and functional processes. Modelling, mathematical integration of structural and functional parameters, provides a holistic view of the essence of the design of a gas exchanger.

The bronchial system (BS), the pulmonary artery (PA) and the pulmonary vein (PV) of the lung of the domestic pig, Sus scrofa were simultaneously cast with silicone rubber and studied. Asymmetrical dichotomous bifurcation preponderated in the tree-like arrangement of the three conducting systems. Lengths and diameters of the various generations were measured. At the extremities of the BS and the PA, alveoli and blood capillaries related very closely. In the cranial and middle lobes of the right and left lungs, topographically, the PA and the PV closely followed the BS, but in the accessory and the caudal (diaphragmatic) lobes, only the PA accompanied the BS: the PV run intersegmentally. Certain similarities and differences were observed between the diameters and lengths of the various generations of the three conducting systems. The strong correlations between some of the structural parameters indicated a high level of structural optimization. While morphometric variations suggest that the air and the blood flow dynamics may somewhat differ between the three conducting systems, they may also register structural features unique to the lung of the domestic pig, an animal that has been highly genetically exploited for fast growth and now leads an indolent lifestyle in captivity.

The ostrich lung, with its lack of interparabronchial septa, the presence of very shallow atria and exceptional morphometric refinement, structurally resembles those of small, energetic flying birds, whereas it also displays features characteristic of the flightless ratites in which the neopulmo is relatively poorly developed and a segmentum accelerans may be generally lacking. The large size of the bronchial system of the ostrich may help explain the unique shifts in the airflow pathways that must occur from resting to panting breathing, explaining its insensitivity to acid-base imbalance of the blood during sustained panting under thermal stress. The mass-specific volume of the lung is 39.1 cm(3)kg(-1) and the volume density of the exchange tissue is remarkably high (78.31%). The blood-gas (tissue) barrier is relatively thick (0.56 microm) but the plasma layer is very thin (0.14 microm). In this flightless ratite bird, the mass-specific surface area of the tissue barrier (30.1 cm(2)g(-1)), the mass-specific anatomical diffusing capacity of the tissue barrier for oxygen (0.00 22 ml O(2) s(-1) Pa(-1) kg(-1)), the mass-specific volume of pulmonary capillary blood (6.25 cm(3)kg(-1)) and the mass-specific total anatomical diffusing capacity for oxygen (0.00073 ml O(2) s(-1) Pa(-1) kg(-1)) are equivalent to or exceed those of much smaller highly aerobic volant birds. The distinctive morphological and morphometric features that seem to occur in the ostrich lung may explain how it achieves and maintains high aerobic capacities and endures long thermal panting without experiencing respiratory alkalosis.

Along the evolutionary continuum, a kaleidoscope of gas exchangers has evolved from the simple cell membrane of the primeval unicells. The most momentous events in this process were: the intensification of molecular oxygen in the biosphere and its appropriation into aerobic metabolism, the rise of multicellular organisms, the development of a circulatory system and carrier pigments in blood, the advocacy of air breathing, adoption of suctional breathing, and the shift to endothermy. To satisfy species-specific needs for oxygen, some constraints were overcome through transactions that obliged certain compromises and trade-offs. Optimal designs of the gas exchangers for particular phylogenetic levels of development, habitat, and lifestyle have developed only so far as to satisfy prescribed needs. The efficiency of the human lung, for example, falls well below those of certain taxa that are considered to be relatively "less advanced." Utilizing different resources and strategies, in fascinating processes of conformity, different groups of animals have developed similar respiratory structures. In most cases, the analogy reflects evolutionary convergence in response to corresponding selective pressures rather than common ancestry. Anat Rec (New Anat) 261:25-44, 2000., (Copyright 2000 Wiley-Liss, Inc.)

1. The lungs of four species of bats, Phyllostomus hastatus (PH, mean body mass, 98 g), Pteropus lylei (PL, 456 g), Pteropus alecto (PA, 667 g), and Pteropus poliocephalus (PP, 928 g) were analysed by morphometric methods. These data increase fivefold the range of body masses for which bat lung data are available, and allow more representative allometric equations to be formulated for bats. 2. Lung volume ranged from 4.9 cm3 for PH to 39 cm3 for PP. The volume density of the lung parenchyma (i.e. the volume proportion of the parenchyma in the lung) ranged from 94% in PP to 89% in PH. Of the components of the parenchyma, the alveoli composed 89% and the blood capillaries about 5%. 3. The surface area of the alveoli exceeded that of the blood-gas (tissue) barrier and that of the capillary endothelium whereas the surface area of the red blood cells as well as that of the capillary endothelium was greater than that of the tissue barrier. PH had the thinnest tissue barrier (0.1204 microns) and PP had the thickest (0.3033 microns). 4. The body mass specific volume of the lung, that of the volume of pulmonary capillary blood, the surface area of the blood-gas (tissue) barrier, the diffusing capacity of the tissue barrier, and the total morphometric pulmonary diffusing capacity in PH all substantially exceeded the corresponding values of the pteropid species (i.e. PL, PA and PP). This conforms with the smaller body mass and hence higher unit mass oxygen consumption of PH, a feature reflected in the functionally superior gas exchange performance of its lungs. 5. Morphometrically, the lungs of different species of bats exhibit remarkable differences which cannot always be correlated with body mass, mode of flight and phylogeny. Conclusive explanations of these pulmonary structural disparities in different species of bats must await additional physiological and flight biomechanical studies. 6. While the slope, the scaling factor (b), of the allometric equation fitted to bat lung volume data (b = 0.82) exceeds the value for flight VO2max (b = 0.70), those for the surface area of the blood-gas (tissue) barrier (b = 0.74), the pulmonary capillary blood volume (b = 0.74), and the total morphometric lung diffusing capacity for oxygen (b = 0.69) all correspond closely to the VO2max value. 7. Allometric comparisons of the morphometric pulmonary parameters of bats, birds and non-flying mammals reveal that superiority of the bat lung over that of the non-flying mammal.(ABSTRACT TRUNCATED AT 400 WORDS)

The lung of the lesser bushbaby (Galago senegalensis) has been investigated morphologically and morphometrically using the transmission and scanning electron microscopes. Grossly and microscopically, the bushbaby lung was found to be essentially similar to that of the other primates and the mammals in general. Subtle morphometric differences were, however, observed, with the bushbaby lung being generally structurally less sophisticated than that of the other primates on which comparable data are available, except for man. The weight-specific surface area of the blood-gas (tissue) barrier in G. senegalensis was 25 cm2 g-1. The thickness of the blood-gas barrier was 0.355 micron and the weight specific total anatomical pulmonary diffusing capacity 0.045 mlO2 sec-1 mbar1 kg-1. The morphological similarity of the galago lung to that of man gives sufficient grounds to justify its possible use in human pulmonary studies but caution has been called for in the general utilisation of primate tissues without first establishing their morphological characteristics, just because the primates are taken to be evolutionally close to man. The dearth of morphological studies on the various organ systems of the prosimians is pointed out.

Qualitative and quantitative characteristics suggest that the lung of the emu is poorly adapted for gas exchange when compared with that of other birds. The granular epithelial cells extend over the air capillaries, and the squamous epithelial cells have microvilli indicating a poor differentiation of the epithelium of the exchange tissue. The surface area of the blood-gas tissue barrier per unit body mass was only 5.4 cm2/g, the volume of the pulmonary capillary blood per unit body mass was only 0.93 cm3/kg, and the tissue barrier was unusually thick (0.232 micron). These parameters produce a relatively small total morphometric pulmonary diffusing capacity for oxygen of 0.014 ml O2/sec/mbar/kg. The findings conform to the evolution of a very large flightless bird in a warm environment lacking effective predators.

The lungs of 46 adult, wild passerine birds belonging to 8 species have been analysed morphometrically, both by light and electron microscope. Volumes were estimated by point counting, surface areas by intersection counting, and thicknesses by intercept length measurements. The mean values obtained for these passerine species appertaining to both lungs together were: volume of the lung per kilogram body weight 25 cm3/kg, volume density of the exchange tissue 52%, surface area of the blood-gas (tissue) barrier per gram body weight 47.48 cm2/g, surface density of the blood-gas (tissue) barrier 323.8 mm2/mm3, capillary loading 1.15 cm3/m2, harmonic mean thickness of the blood-gas (tissue) barrier 0.127 micron, arithmetic mean thickness 0.745 micron and the total morphometric pulmonary diffusion capacity 7.08 ml O2/min/mm Hg/kg. These values indicate that the passerine lung is specially well adapted for gas exchange, mainly by having a thin and extensive blood-gas (tissue) barrier, in response to the high oxygen demand by this group of bird.

The lungs of four adult specimens of the vervet monkey (Cercopithecus aethiops) have been examined by transmission and scanning electron microscopy. A morphometric evaluation of the structural components directly involved in gas exchange has been carried out and the data have been modelled to estimate the anatomical diffusing capacity of the lung. The upper air-conducting airways of the lung were lined by an epithelium characterized by ciliated cells among which were dispersed goblet cells. The alveolar surface was lined by squamous type I pneumocytes and cuboidal type II granular pneumocytes. The blood-gas (tissue) barrier consisted of an epithelial cell, a common basal lamina, and an endothelial cell in the thin parts of the interalveolar septum. In the thicker parts of the septum, an interstitial space interposed between the basal laminae of the epithelial and endothelial cells contained supportive elements such as collagen, elastic tissue, and fibrocytes. The alveoli, the blood capillaries, and septal tissue composed 73%, 16%, and 11%, respectively, of the parenchyma. The harmonic and arithmetic mean thicknesses of the blood-gas (tissue) barrier were 0.311 micron and 1.048 microns; the surface area of the blood-gas (tissue) barrier per unit body weight was 50 cm2g-1, and the surface density was 117 mm2.mm3-1. The weight-specific total morphometric diffusing capacity was 0.11 mlO2 (sec.mbar.kg)-1. In comparison, the pulmonary morphometric characteristics of vervet monkey lung were superior to those of the other primates (Macaca irus, M. mulatta, and Homo sapiens) for which equivalent data are available. The gas-exchange potential of the lungs of the nonhuman primates as revealed by morphometric studies surpasses that of man, a feature that can be attributed to the relatively less energetic human lifestyle.

Comprehensive pulmonary morphometric data from 42 species of birds representing ten orders were compared with those of other vertebrates, especially mammals, relating the comparisons to the varying biological needs of these avian taxa. The total lung volume was strongly correlated with body mass. The volume density of the exchange tissue was lowest in the charadriiform and anseriform species and highest in the piciform, cuculiform and passeriform species. The surface area of the blood-gas (tissue) barrier, the volume of the pulmonary capillary blood and the total morphometric pulmonary diffusing capacity were all strongly correlated with body mass. The harmonic mean thickness of both the blood-gas (tissue) barrier and the plasma layer were weakly correlated with body mass. The mass-specific surface area of the blood-gas (tissue) barrier (surface area per gram body mass) and the surface density of the blood-gas (tissue) barrier (i.e. its surface area per unit volume of exchange tissue) were inversely correlated (though weakly) with body mass. The passeriform species exhibited outstanding pulmonary morphometric adaptations leading to a high specific total diffusing capacity per gram body mass, consistent with the comparatively small size and energetic mode of life which typify passeriform birds. The relatively inactive, ground-dwelling domestic fowl (Gallus gallus) had the lowest pulmonary diffusing capacity per gram body mass. The specific total lung volume is about 27% smaller in birds than in mammals but the specific surface area of the blood-gas (tissue) barrier is about 15% greater in birds. The ratio of the surface area of the tissue barrier to the volume of the exchange tissue was also much greater in the birds (170-305%). The harmonic mean thickness of the tissue barrier was 56-67% less in the birds, but that of the plasma layer was about 66% greater in the birds. The pulmonary capillary blood volume was also greater (22%) in the birds. Except for the thickness of the plasma layer, these morphometric parameters all favour the gas exchange capacity of birds. Consequently, the total specific mean morphometric pulmonary diffusing capacity for oxygen was estimated to be about 22% greater in birds than in mammals of similar body mass. This estimate was obtained by employing oxygen permeation constants for mammalian tissue, plasma and erythrocytes, as avian constants were not then available.(ABSTRACT TRUNCATED AT 400 WORDS)

Air and blood capillaries of the lung of the domestic fowl constitute the functional gas exchange units. They anastomose profusely and interlace with each other in 3 dimensions. Air capillaries are not blind-ending tubules as has occasionally been suggested.

The lungs of the domestic fowl were prepared for scanning electron microscopy after vascular and airway latex rubber casting to demonstrate the spatial organization of the various structural components that are involved in the gas exchange that takes place in the parabronchial tissue mantle. The bulk of the intrapulmonary air flows through the parabronchial lumen and then centrifugally diffuses into the exchange tissue through the atria, the infundibula, and the air capillaries. The blood flows centripetally from the interparabronchial arteries, then into the intraparabronchial arterioles, and finally into the blood capillaries, which together with the air capillaries constitute the functional terminal gas exchange units. The relationship between the air flow in the parabronchial lumen and the incoming blood (into the exchange tissue) has been shown to be crosscurrent, where the directions of the flow of these two gas exchange media are essentially perpendicularly disposed to each other; whereas the relationship between the blood capillaries and the air capillaries is countercurrent, the blood flowing towards the parabronchial lumen and the air in the opposite direction, i.e., towards its periphery. Both these spatial structural relationships between the air and blood are significant factors that contribute to the remarkable efficiency of the avian lung in gas exchange.(ABSTRACT TRUNCATED AT 250 WORDS)

The lungs of five species of bat Pipistrellus pipistrellus, Miniopterus minor (Peters), Tadarida mops (De Blainville), Cynopterus brachyotis (Muller) and Cheiromeles torquatus (Horstield) have been analysed by morphometric techniques. The mean body weight (W) ranged from 5 g in Pipistrellus pipistrellus to 173 g in Cheiromeles torquatus; the lung volume (VL) ranged from 0.3 cm3 in Pipistrellus to 10 cm3 in Cheiromeles. The volume densities or the main components of the bat lung, namely the parenchyma [VV(p,L)] (the gas exchange region) and the non-parenchyma [VV(np,L)], were closely similar, the VV(p,L) constituting a mean value of 84.2% and the VV(np,L) 15.8% in the five species. The VL, the surface area of the blood--gas (tissue) barrier (St), the pulmonary capillary blood volume (Vc), and the total morphometric pulmonary diffusing capacity (DLO2) were all strongly correlated with body weight. The harmonic mean thickness of the blood--gas (tissue) barrier (tau ht) and the surface density of the blood--gas (tissue) barrier [SV(t,p)] were poorly correlated with W. The bats had a remarkably higher VL than either birds or terrestrial mammals. The Vc in the bat lung was similar to that in the bird lung but higher than that of the terrestrial mammals. The bats had a more extensive St than either the birds or the terrestrial mammals. In the bats the tau ht was thicker than in the birds but thinner than that of the terrestrial mammals. These pulmonary structural adaptations culminated in a higher DLO2 in the bat than either in the birds or in the terrestrial mammals. The superior morphometric properties of the bat lung coupled with the established physiological adaptations may help to explain how the bat lung is capable of providing the immense amount of oxygen demanded by flight.

The lung of a snake, the black mamba (Dendroaspis polylepis), has been investigated by scanning and transmission electron microscopy. This species has only one lung, the right, which is long and occupies most of the pleuro-peritoneal cavity. Grossly, the lung could be divided into two discrete anatomical regions: an anterior respiratory area made up of a honeycomb network of capillary-bearing partitions, and a posterior membranous saccular region. The exchange region consisted of a central air duct, the bronchus, which was delineated both dorsally and laterally by morphologically and spatially distinct hierarchically arranged septa. The primary septa gave rise to the secondary septa from which the much deeper peripherally situated tertiary septa that formed the immediate openings to the faveoli arose. The faveoli were rather parallel elongated pockets separated by partitions, the interfaveolar septa, and terminated peripherally on the pleura. A double capillary disposition of the blood capillaries was observed on the relatively thick primary and secondary septa. These septa were lined by a heterogenous epithelium made up of ciliated cells, secretory cells, and smooth squamous cells. This epithelium was continued from the trachea and the bronchus. At the faveolar level the blood capillaries exhibited a single system where they formed a matrix on both sides of the partitions. The surface of the faveoli was covered by two types of cells: Type I cells were squamous and their remarkably attenuated cytoplasmic arborisations were notably extensive while the Type II cells were rather cuboidal, bore stubby microvilli and contained the characteristic osmiophilic lamellated bodies. On the basis of the clearly evident complete differentiation of the pneumocytes and the presence of both the double and single capillary systems, it was observed that this lung, and apparently the reptilian lung in general, manifests a transitional developmental and structural stage in the evolution of the lungs of the air-breathing vertebrates from lower through to higher vertebrates. The gross and ultrastructural heterogeneity of the organisation of the ophidian lung is illustrated and the dearth of pulmonary morphological data in this taxon is pointed out.

The morphology of the lungs of two reptilian species, Varanus exanthematicus and Malacochersus tornieri, have been studied on gross preparations, latex casts, and critical-point-dried tissues. The shape of these lungs was observed to conform with that of the body, the lung of the monitor lizard (Varanus) being long and ovoid while that of the pancake tortoise (Malacochersus) was rounded and laterally indented. With respect to the size distribution of the gas exchange compartments, the lungs were observed to be notably heterogenous. In both species these units were generally smaller in diameter in the cranial region of the lung while those in the caudal region were larger. The gas exchange compartments in the tortoise were more profusely compartmented with the primary, secondary, and tertiary septa being well developed while in the lizard only the primary and secondary septa were observed. The tertiary septa in the tortoise lung and the secondary septa in that of the monitor lizard defined the terminal gas exchange units, the faveoli. The cast impressions closely resembled the actual lung tissue and convincingly revealed the hierarchical design of the gas exchange compartments as they radiate from the air chambers and ducts, terminally giving rise to the faveoli. This stratification clearly increases the surface area available for gas exchange in these lungs. Disparate refinements of the basic reptilian lung design, as noted here, may lead to differing anatomic pulmonary diffusing capacities for oxygen to which characteristics like energetics and mode of respiration in this taxon may be attributed.

The lungs of five charadriiform species of bird, two of which are good divers and three predominantly flyers (soarers and gliders) have been analysed by morphometric techniques. Largely the morphometric structural values in the divers significantly exceeded those of the flyers (gulls). The average weight specific surface area of the blood-gas (tissue) barrier in the divers (28.45 +/- 2.05 cm2 X g-1 SD) surpassed that of the flyers (23.5 +/- 3.61 cm2 X g-1 SD). The divers had a higher volume of the pulmonary capillary blood per unit body weight (4.42 +/- 0.11 cm3 X kg-1 SD) than the flyers (2.84 +/- 0.58 cm3 X kg-1 SD). The weight specific volume of the lung in the divers (34.90 +/- 3.11 cm3 X kg-1 SD) exceeded that of the flyers (26.94 +/- 3.15 cm3 X kg-1 SD). The total morphometric pulmonary diffusing capacity per unit body weight in the divers (4.73 +/- 0.05 ml O2 X (min X mm Hg X kg)-1 SD) was higher than that of the flyers (3.09 +/- 0.47 ml O2 X (min X mm Hg X kg)-1 SD). The divers, however, had a notably thicker blood-gas (tissue) barrier with a harmonic mean thickness of 0.212 +/- 0.03 micron SD compared to that of the flyers (0.138 +/- 0.02 micron SD). The data acquired here commensurate the modes of life exhibited by these two groups of bird. The divers, which are relatively energetic birds, expend a lot of energy to move and stay underwater, concomitantly undergoing prolonged asphyxia during submergence and may hence need to extract as much of the oxygen in the pulmonary air as possible to prolong a dive. These birds appear in general to have structurally better adapted lungs than those of the gulls, birds which to a large extent exhibit relatively less energetic soaring and gliding flights.

The lungs of five adult Epauleted Fruit-bats (Epomophorus wahlbergi) of mean body weight 96 g were analysed morphometrically. The lung volume per unit body weight was 0.043 cm3/g, the surface area of the tissue barrier (i.e., the effective alveolar surface area) component of the blood-gas pathway per unit body weight was 138 cm2/g, and the surface density of the tissue barrier (surface area of the tissue barrier per unit volume of parenchyma) was 121 mm2/mm3. The harmonic mean thickness of the tissue barrier was between 0.267 and 0.349 micron. The morphometric pulmonary diffusing capacity per unit body weight (DLO2/W) was 0.02 ml O2 per min per mm Hg per g. These values are compared with those of shrews and birds. It is suggested that in bats enlargement of the lungs, small subdivisions of the air spaces, and a thin blood-gas barrier, could be linked with previously reported circulatory adaptations to account for the high oxygen consumption during flight.

The lungs of 5 domestic fowls have been analysed electron microscopically by standard morphometric methods. The anatomical diffusing capacity has been calculated from the relevant parameters. The blood-gas barrier consisted essentially of endothelium, basal lamina, and a very thin squamous epithelial cell. Granular cells are absent and interstitial tissue is minimal. The following measurements are mean values applying to both lungs together, in the fixed state: lung volume, 25.0 cm3; total intrapulmonary blood volume, 6.9 cm3; volume of the exchange tissue, 11.6 cm3; pulmonary capillary blood volume, 3.51 cm3; pulmonary capillary haematocrit, 62.7%; total intrapulmonary air volume, 16.61 cm3; air capillary volume, 6.68 cm3; surface area of the blood-gas barrier, 2.08 m2; surface area of the barrier per unit volume of exchange tissue, 179.5 mm2/mm3; arithmetic mean thickness of the tissue barrier, 1.20 micrometers; harmonic mean thickness of the tissue barrier, 0.314 micrometers; harmonic mean thickness of the plasma layer, 0.342 micrometers. The values of the maximum and minimum morphometric diffusing capacities for the lung (DL02 m) were respectively 3.55 and 1.50 ml O2/min/mm Hg; those for the membrane (Dmo2 m) were 13.61 and 12.01 ml O2/min/mm Hg.

The lungs of 107 birds of 19 different species from seven orders were fixed in situ. The mean volumes of both fixed lungs together ranged from 0.15 to 95.31 cm3. Histological sections of one lung from each bird were analyzed by point counting with a Zeiss integrating eyepiece to determine the volume densities and thence the absolute volumes of the main functional components of the lung. The mean volume density of the exchange tissue was highest in the 11 passeriform species (53.5%) and lowest in the 2 charadriiform species (34.6%); that for all of the 8 non-passeriform species was 42.6%. The possible significance of these variations in relation to the differing oxygen requirements of these groups of birds is discussed. The parabronchi showed minor variations in the degree of development of the interparabronchial septa, atria, interatrial septa, and atrial muscles. The diameter of the parabronchi (including the mantle of exchange tissue) ranged from about 0.34 mm in the passeriform species to about 0.63 mm in Anser anser; the lumen of the parabronchus accounted for about half of this diameter. Body weight an lung volume were strongly correlated (0.995); the allometric function relating lung volume to body weight was 29.5 w0.988.

The lungs of 5 wild mallard ducks (Anas platyrhynchos) and 5 feral graylag geese (Anser anser) of mean body weight 1.04 and 3.84 kg, respectively, were fixed in situ by intratracheal infusion of 2.3% glutaraldehyde, pH 7.4 and total osmolarity 350 mOsm, at a pressure head of 25 cm, and analysed by standard morphometric techniques. The following data apply to both lungs together, in the fixed state, the first value relating to Anas and the second to Anser in each case: lung volume, 30.4 and 95.3 cm3; volume of exchange tissue, 12.32 and 38.50 cm3; volume of capillary blood, 4.06 and 12.49 cm3; surface area of blood-gas (tissue) barrier per unit body weight, 28.56 and 23.10 cm2/g; surface area of the blood-gas (tissue) barrier per unit volume of lung, 977 and 932 cm2/cm3; surface area of blood-gas (tissue) barrier per unit volume of exchange tissue, 241 and 230 mm2/mm3; harmonic mean thickness of tissue barrier, 0.133 and 0.118 microns; arithmetic mean thickness of tissue barrier, 0.903 and 0.887 microns; harmonic mean thickness of plasma layer, 0.369 and 0.322 microns; mean total morphometric pulmonary diffusing capacity per unit body weight, 3.85 and 3.59 ml O2/min/mm Hg/kg. These morphometric parameters of Anas and Anser are compared with those reported in the literature for the domestic fowl (Gallus gallus), the budgerigar (Melopsittacus undulatus), the house sparrow (Passer domesticus), and the violet-eared hummingbird (Colibri coruscans). The lungs of these six avian species show progressively advancing adaptations, from Gallus, through Anser, Anas, Melopsittacus and Passer, to Colibri, which appear to be consistent with the energetic characteristics of these birds.

The gross, histological and ultrastructural organisation of the baboon lung was found to be similar to that of the human lung. It is suggested that, in general, the lungs of the non-human primates would serve as ideal models for the study of the human lung. The baboon lung comprises the parenchyma, the gas exchange part of the lung which consists of alveoli, blood capillaries and the tissue of the interalveolar septum, and the non-parenchyma made up of the air conducting passages like bronchi, bronchioles, larger blood vessels, connective tissue and pleura. On morphometric analysis, the parenchyma was found to constitute 87% of the lung, the rest being made up of the elements of the non-parenchyma. The alveoli, blood capillaries and the interalveolar tissue respectively constituted 76, 8 and 16% of the parenchyma. The harmonic mean thickness of the blood-gas (tissue) barrier was 0.475 micron and the arithmetic mean 1.12 micron, the ratio being 1:2.3. The weight specific surface area of the blood-gas (tissue) barrier was 37 cm2/g and the surface density of the tissue barrier in the parenchyma 92 mm2/mm3. The total morphometric pulmonary diffusion per unit body weight was 4 ml O2/min/mmHg/kg and the volume of the pulmonary capillary blood per unit surface area of the tissue barrier 0.84 cm3/m2. Morphometrically the baboon lung was thus observed to be better adapted for gas exchange than that of man but less specialised than that of the smaller monkeys such as Macaca mulatta.

In mammals, surface macrophages (SMs) play a foremost role in protecting the respiratory system by engulfing and destroying inhaled pathogens and harmful particulates. However, in birds, the direct defense role(s) that SMs perform remains ambiguous. Paucity and even lack of SMs have been reported in the avian respiratory system. It has been speculated that the pulmonary defenses in birds are inadequate and that birds are exceptionally susceptible to pulmonary diseases. In an endeavour to resolve the existing controversy, the phagocytic capacities of the respiratory SMs of the domestic fowl and the rat were compared under similar experimental conditions by exposure to polystyrene particles. In cells of equivalent diameters (8.5 µm in the chicken and 9.0 µm in the rat) and hence volumes, with the volume density of the engulfed polystyrene particles, i.e. the volume of the particles per unit volume of the cell (SM) of 23% in the chicken and 5% in the rat cells, the avian cells engulfed substantially more particles. Furthermore, the avian SMs phagocytized the particles more efficiently, i.e. at a faster rate. The chicken erythrocytes and the epithelial cells of the airways showed noteworthy phagocytic activity. In contrast to the rat cells that did not, 22% of the chicken erythrocytes phagocytized one to six particles. In birds, the phagocytic efficiencies of the SMs, erythrocytes, and epithelial cells may consolidate pulmonary defense. The assorted cellular defenses may explain how and why scarcity of SMs may not directly lead to a weak pulmonary defense. The perceived susceptibility of birds to respiratory diseases may stem from the human interventions that have included extreme genetic manipulation and intensive management for maximum productivity. The stress involved and the structural–functional disequilibria that have occurred from a ‘directed evolutionary process’, rather than weak immunological and cellular immunity, may explain the alleged vulnerability of the avian gas exchanger to diseases. [ABSTRACT FROM AUTHOR]