Search

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.

The blood capillaries (BC) and the air capillaries (ACs) are the terminal gas exchange units of the avian lung. The minuscule structures are astonishingly strong. It is only recently that the morphologies and the biomechanical properties of the BCs and the ACs were investigated. Regarding size and shape, the BCs and the ACs differ remarkably. While they were previously claimed to be tubular (cylindrical) in shape, the ACs are rather rotund structures which interconnect across short, narrow passageways. Atypical of those in other tissues, the BCs in the exchange tissue of the avian lung comprise of distinct segments which are about as long as they are wide and which are coupled in three-dimensions. The thin blood-gas barrier (BGB) which separates the ACs from the BCs is peculiarly strong. The causes of the strengths of the ACs and the BCs in general and the BGB in particular are varied and controversial. Here, the recent morphological and physiological findings on the structure, biomechanical properties, and the strengths of the respiratory units of the avian lung and the BGB have been critically examined. Also, in light of the new morphological findings of the ACs and the BCs, the functional model which is currently in use to assess the gas exchange efficiency of the avian lung should be revised and the inappropriateness of the terms 'blood capillary' and 'air capillary' for the gas exchange units of the avian lung is pointed out.

The anatomy of the domestic duck lung was studied macroscopically, by casting and by light, transmission, and scanning electron microscopy. The lung had four categories of secondary bronchi (SB), namely, the medioventral (MV, 4-5), laterodorsal (LD, 6–10), lateroventral (LV, 2–4), and posterior secondary bronchi (PO, 36–44). The neopulmonic parabronchi formed an intricate feltwork on the ventral third of the lung and inosculated those from the other SB. The lung parenchyma was organized into cylindrical parabronchi separated by thin septa containing blood vessels. Atria were shallow and well-fortified by epithelial ridges reinforced by smooth muscle bundles and gave rise to 2–6 elongate infundibulae. Air capillaries arose either directly from the atria or from infundibulae and were tubular or globular in shape with thin interconnecting branches. The newly described spatial disposition of the conducting air conduits closely resembles that of the chicken. This remarkable similarity between the categories, numbers, and 3D arrangement of the SB in the duck and chicken points to a convergence in function-oriented design. To illuminate airflow dynamics in the avian lung, precise directions of airflow in the various categories of SB and parabronchi need to be characterized.

The avian pulmonary circulation has many interesting features and much information can be gained by comparing the avian and mammalian systems. Two features are primarily responsible for the unique features of avian capillaries. First, the avian lung has separated the ventilation and gas exchange functions. Second, the avian lung uses a flow-through process for ventilation rather than the reciprocal pattern adopted by mammals. As a consequence, the environment of the pulmonary capillaries is very different in the avian compared with the mammalian lung. The avian capillaries are nested in a syncytium of air capillaries, whereas the capillaries of the mammalian lung are strung out along the alveolar walls. This means that the mechanical support of the categories is very different in birds compared with mammals. A consequence of this is that the walls of the capillaries are very different. In the avian lung, the blood–gas barrier is extremely thin and uniform throughout the capillaries. Contrast this with the mammalian lung where a type I collagen cable is required for the support of the capillaries, and as a result the blood–gas barrier is much thicker in places and the diffusion characteristics are therefore inferior. Another striking difference is that avian pulmonary capillaries are remarkably rigid unlike those in mammals, which undergo recruitment and distention when the cardiac output rises. The implications of this for pulmonary vascular resistance during intense exercise such as flying are still unclear.

Air flow in an avian lung was studied numerically to determine the effects of air sac compliance on flow in the parabronchi. In this preliminary study, the geometry of the avian respiratory system was simplified to capture the characteristics of respiratory flow. The pressure fluctuation within air sacs caused by inflation and deflation was expressed by a lumped parameter model. The results demonstrate that the flow direction in the parabronchi varied, depending upon the compliance of the air sacs. A unidirectional flow in the parabronchi was achieved for compliances where pressure fluctuations in all air sacs were in phase. Air sac compliance significantly affected the pressures in the anterior and posterior air sacs and thus the pressure difference over the parabronchi that drove the flow in the parabronchi. These results address the importance of air sac compliance in the avian respiratory system and suggest that the compliance of air sacs would be optimized to accomplish unidirectional flow in the parabronchi.

To identify the forces that may exist in the parabronchus of the avian lung and that which may explain the reported strengths of the terminal respiratory units, the air capillaries and the blood capillaries, the arrangement of the parabronchial collagen fibers (CF) of the lung of the domestic fowl, Gallus gallus variant domesticus was investigated by discriminatory staining, selective alkali digestion, and vascular casting followed by alkali digestion. On the luminal circumference, the atrial and the infundibular CF are directly connected to the smooth muscle fibers and the elastic tissue fibers. The CF in this part of the parabronchus form the internal column (the axial scaffold), whereas the CF in the interparabronchial septa and those associated with the walls of the interparabronchial blood vessels form the external, i.e. the peripheral, parabronchial CF scaffold. Thin CF penetrate the exchange tissue directly from the interparabronchial septa and indirectly by accompanying the intraparabronchial blood vessels. Forming a dense network that supports the air and blood capillaries, the CF weave through the exchange tissue. The exchange tissue, specifically the air and blood capillaries, is effectively suspended between CF pillars by an intricate system of thin CF, elastic and smooth muscle fibers. The CF course through the basement membranes of the walls of the blood and air capillaries. Based on the architecture of the smooth muscle fibers, the CF, the elastic muscle fibers, and structures like the interparabronchial septa and their associated blood vessels, it is envisaged that dynamic tensional, resistive, and compressive forces exist in the parabronchus, forming a tensegrity (tension integrity) system that gives the lung rigidity while strengthening the air and blood capillaries.

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.

The gas exchanging region in the avian lung, although proportionally smaller than that of the mammalian lung, efficiently manages respiration to meet the high energetic requirements of flapping flight. Gas exchange in the bird lung is enhanced, in part, by an extremely thin blood-gas barrier (BGB). We measured the arithmetic mean thickness of the different components (endothelium, interstitium, and epithelium) of the BGB in the domestic chicken lung and compared the results with three mammals. Morphometric analysis showed that the total BGB of the chicken lung was significantly thinner than that of the rabbit, dog, and horse (54, 66, and 70% thinner, respectively) and that all layers of the BGB were significantly thinner in the chicken compared with the mammals. The interstitial layer was strikingly thin in the chicken lung (∼86% thinner than the dog and horse, and 75% thinner than rabbit) which is a paradox because the strength of the BGB is believed to come from the interstitium. In addition, the thickness of the interstitium was remarkably uniform, unlike the mammalian interstitium. The uniformity of the interstitial layer in the chicken is attributable to a lack of the supportive type I collagen cable that is found in mammalian alveolar lungs. We propose that the surrounding air capillaries provide additional structural support for the pulmonary capillaries in the bird lung, thus allowing the barrier to be both very thin and extremely uniform. The net result is to improve gas exchanging efficiency.

Mechanisms of unidirectional flow generation and gas transport enhancement in oscillatory flow of avian lungs were numerically studied with bifurcation models of avian trachea. Model systems of right-angled branched tubes with single and multi-bifurcating tubes were adopted for the numerical simulation. The effect of constriction near the bifurcation was also investigated. Main concern was placed on the effects of bifurcation structure on unidirectional flow generation and axial gas transport enhancement. Oscillatory flow fields as well as concentration fields were numerically analyzed with a developed code based on SIMPLE and CIP methods. Similar to the previous experiment by the authors, unidirectional net flow was observed from side-daughter tube to daughter tube. Strongly affecting on the oscillatory flow fields and flow distribution, the constriction and the multi-bifurcation structure were found to improve unidirectional net flow generation. In particular, multi-bifurcation structure was found not only to improve the unidirectional flow generation and gas transport but also to reduce the total pressure drop of the system.

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.

Airflow in an avian respiratory system was simulated to study why birds affected with airsacculitis have respiratory distress. The airflow in the avian lung was modeled with a 1D electrical circuit and simulated for investigating what effect an increase in wall thickness of air sacs caused by airsacculitis has on flow in lung. The results demonstrated that thickening of the air sac wall caused anti-synchronization between an elastic recoiling force of the air sac walls and an intra-pleural pressure, bringing difficulties in expansion of air sacs to draw in airs during an inspiration period and thereby decreasing air to be pumped out during an expiration period. This was reflected in a decrease in air flow volume in parabronchi where gas exchange takes place. Therefore, it was concluded that airsacculitis causes imbalance in air flow dynamics in the avian lung and thus impairs breathing ability of birds.

It is known that alterations in respiratory gases in birds can cause a nonhomogenous redistribution of pulmonary blood flow between the 2 separate gas-exchanging regions of the avian lung, the paleopulmo (PALEO) and neopulmo (NEO); however, the effect of alterations in respired gas content on the distribution of pulmonary blood flow in birds, such as the chicken, that possess a highly developed NEO is not known. This study used a colorimetric microsphere method to determine the effects of hypoxia and hypercapnia on the relative distribution of pulmonary blood flow in anesthetized chickens (Gallus domesticus) during control (normoxic) and experimental (hypoxic or hypercapnic) conditions, where the relative regional distribution of blood flow in the lung is expressed as the ratio NEO/PALEO. Administration of a hypoxic gas mixture (16.0% O2) produced a 13.4% increase in NEO/PALEO, and, administration of a hypercapnic gas mixture (5.0% CO2) resulted in a 27.8% increase in NEO/PALEO. Our results are consistent with a mechanism in which the regional redistribution of pulmonary blood flow is mediated by local intrapulmonary factors.

The mechanism of avian respiration is still controversial. It is fundamentally different from respiration in mammals. Although during in-and expiration a continuous caudocranial airflow is present within the tertiary bronchi and the air capillaries of the avian lung, the air flow within the entire respiratory system is still equivocal. Several patterns explaining the air flow during in-and expiration have been proposed during the past century. Moreover, various anatomical structures and aerodynamic mechanisms have recently been described in an attempt to explain the proposed mechanisms of respiration. This manuscript gives an overview of the anatomy of the avian respiratory system and the hypotheses concerning the physiology of avian respiration.

1. 1. Birds present remarkably variable pulmonary morphometric characteristics which closely correspond with factors such as phylogeny, body size, mode of life and habitat. These factors determine the oxygen demands, energetics and exercise capacities of the various species. 2. 2. Genetics, domestication and longstanding intense selection for production traits such as weight gain and egg production appear to have played a role in the deterioration of the morphometric parameters of the galliform species. Captive non galliform birds, however, appear to retain pulmonary structural adaptations and hence the potential for efficient gas exchange probably for occasional instances which may require explosive energy production. 3. 3. The morphometric pulmonary parameters such as lung volume, volume of the pulmonary capillary blood and surface area of the blood-gas (tissue) barrier scale linearly with body weight while the harmonic mean thickness of the blood-gas (tissue) barrier does so very weakly. This suggests that barrier thickness has been optimized in birds and is thus probably the least adaptable parameter in the lung. The weight specific surface area of the blood-gas (tissue) barrier scales negatively with body weight indicating that the small birds which generally are more energetic and have a higher O2 consumption, have adaptively superior lungs than the larger ones. 4. 4. Bats have better pulmonary morphometric parameters than birds. This may be a compensation for having retained their functionally inferior mammalian lungs. Refinement of the structural components of the bat lung does not appear to have sufficed in effecting the exchange of the large amounts of oxygen required for flight and has called for adaptation and subsequently co-option of extrapulmonary components such as the heart and blood into the respiratory processes. 5. 5. In comparative pulmonary morphometry, regressional and statistical analysis enables the magnitudes of various parameters in different groups of animals to be assessed and wide ranging conclusions to be drawn. Pulmonary modelling which entails integration of pulmonary parameters to formulate factors which best define the global structural capacity of a gas exchanger has been attempted on respiratory organs of a number of animals. The major limiting factors which have been the course of the current methodological variations, have been the interpretation and correlation of measurements made on tissue preparations with the functional (in life) state and the lack of the essential morphophysiological data on pulmonary tissues of many animals. There is need to harmonize the various approaches.

To elucidate the shape, size, and spatial arrangement and association of the terminal respiratory units of the avian lung, a three-dimensional (3D) computer-aided voxel reconstruction was generated from serial plastic sections of the lung of the adult muscovy duck, Cairina moschata. The air capillaries (ACs) are rather rotund structures that interconnect via short, narrow passageways, and the blood capillaries (BCs) comprise proliferative segments of rather uniform dimensions. The ACs and BCs anastomose profusely and closely intertwine with each other, forming a complex network. The two sets of respiratory units are, however, absolutely not mirror images of each other, as has been claimed by some investigators. Historically, the terms 'air capillaries' and 'blood capillaries' were derived from observations that the exchange tissue of the avian lung mainly consisted of a network of minuscule air- and vascular units. The entrenched notion that the ACs are straight (non-branching), blind-ending tubules that project outwards from the parabronchial lumen and that the BCs are direct tubules that run inwards parallel to and in contact with the ACs is overly simplistic, misleading and incorrect. The exact architectural properties of the respiratory units of the avian lung need to be documented and applied in formulating reliable physiological models. A few ostensibly isolated ACs were identified. The mechanism through which such units form and their functional significance, if any, are currently unclear.

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.

Scanning electron microscopy (SEM) was utilized to examine the interparabronchial septum as a potential site of lymphatic drainage in the lungs of anesthetized chickens (Gallus domesticus). Birds were subjected to extracellular fluid volume expansion in order to produce hydrostatic pulmonary edema via increased pulmonary capillary fluid flux into the interstitial spaces of the lung. Micrographs obtained from freeze-dried lungs of volume-loaded birds were compared with similarly prepared lungs from normal control chickens, which were not volume loaded. The adjacent parabronchi of the control lungs were closely opposed by a minimal septal space, whereas the interparabronchial septal space of the volume-loaded birds was measurably thickened and appeared to be engorged as a result of hydrostatic pulmonary edema. The results of this study are consistent with observations of the lungs of mammals subjected to hydrostatic pulmonary edema and suggest that the interparabronchial septum may be a potential route of lymphatic drainage in the avian lung.

Scanning electron microscopy was used to examine the interparabronchial septa of chickens as a potential site of lymphatic drainage in the avian lung. Anaesthetized chickens were subjected to extracellular fluid volume expansion to produce pulmonary oedema as a result of increased capillary fluid flux into the interstitial spaces of the lung. In normal (control) chickens, the adjacent parabronchi were separated by a minimal septal space. In the "volume-loaded" birds, however, the interparabronchial septal spaces were measurably thickened and engorged as a result of hydrostatic pulmonary oedema. These results, which were consistent with reports of the effect of hydrostatic pulmonary oedema in mammals, suggest that the interparabronchial septum is a potential route of lymphatic drainage in the avian lung.

The form, geometry and epithelial morphology of the extrapulmonary primary bronchi (EPPB) of the domestic fowl (Gallus gallus var. domesticus) and the rock dove (Columba livia) were studied microscopically and by three-dimensional computer reconstruction to determine the structural features that may be involved in the rectification of the inspired air past the openings of the medioventral secondary bronchi (MVSB), i.e. the inspiratory aerodynamic valving (IAV). In both species, the EPPB were intercalated between the clavicular and the cranial thoracic air-sacs. A notable difference between the morphology of the EPPB in G. g. domesticus and C. livia was that, in the former, the EPPB were constricted at the origin of the MVSB, while a dilatation occurred at the same site in the latter. In both species, a highly vascularized, dorsally located hemispherical epithelial swelling was observed cranial to the origin of the MVSB. The MVSB were narrow at their origin and variably angled relative to the longitudinal axis of the EPPB. Conspicuous epithelial tracts and folds were observed on the luminal aspect of the EPPB in both C. livia and G. g. domesticus. From their marked development and their orientation relative to the angled MVSB, these properties may influence the flow of the air in the EPPB. It was concluded that features such as syringeal constriction, an intimate topographic relationship between the EPPB and the cranial air-sacs, prominent epithelial tracts and folds, an epithelial swelling ahead of the origin of the first MVSB (corresponding to the ‘segmentun accelerans’), and narrowing and angulation of the MVSB at their origin, may together contribute to IAV to a variable extent. In as much as the mechanism of pulmonary ventilation and mode of airflow in the parabronchial lung are basically similar in all birds, the morphological differences observed between G. g. domesticus and C. livia suggest that either the mechanism of production of IAV or its functional efficiency may be different, at least in these two species of birds.

The unidirectional gas-flow pattern through the avian lung is thought to result from ‘aerodynamic valves’; support for this hypothesis lies mainly in the failure to find any evidence for anatomical valves. During expiration, air flows from the caudal air sacs through the major exchange area of the lung, the paleopulmonic parabronchi, instead of bypassing the lungs via the intrapulmonary bronchus. We tested whether the effectiveness of this expiratory flow control mechanism depends on aerodynamic factors, especially convective inertial forces that depend on gas density and flow velocity. In pump-ventilated, anaesthetized geese, a bolus of tracer gas was introduced into both the right and left caudal thoracic air sacs during an end-inspiratory pause. During the first expiration, the rise of tracer levels within the caudal trachea was measured. Valve efficacy was positively correlated with the AO rate of expiratory gas flow, (range 8–200 ml s-1). At flows assumed to occur during exercise in geese , the expiratory valve efficacy was approximately 95 %; it was less effective at lower flows. Surprisingly, the density (ρ) of the background gas (ρ of He/O2=0.43 g l-1, Ar/O2=1.72 g l-1 or SF6/O2=5.50 g l-1) had no effect on expiratory valving. We suggest two possible mechanisms that might explain this unusual combination of flow dependence without density dependence. (1) If airway geometry changes occurred between experiments with different gases, flow in the vicinity of the expiratory valve may have varied independently from flow measured at the airway opening. (2) Alternatively, valving may depend on dynamic compression of the intrapulmonary bronchus, which could depend mainly on viscous resistance and thus on flow velocity but not gas density.

We recorded discharge frequencies of 32 intrapulmonary chemoreceptors (IPC) during caudocranial and craniocaudal ventilation in the perfused duck lung. Blood gases, ventilatory gas flow, inspired P CO 2 and P O 2 , and expired P CO 2 measured simultaneously were used to predict regional CO 2 and O 2 gradients within the lung. Gas exchange was modelled in 7 log normal ventilation-perfusion compartments using mass balance differentials with an adjustable step size. CO 2 and O 2 interactions during exchange were modelled using the Bohr effect. P 50 , blood acid-base status and the CO 2 dissociation relationship. Close agreement (± 1.0 Torr) between simulated arterial and expired P CO 2 and observed values was achieved after forcing simulated Pa O 2 to converge on observed Pa O 2 by an iterative adjustment of the perfusive shunt or the log standard deviation of the ventilation-perfusion distribution. Using the IPC static CO 2 sensitivity measured in the non-perfused lung and the CO 2 gradients generated by the model, we have found evidence for a distributed multi-ending receptor system in the duck lung.