Structure and function of the avian respiratory system

Abstract

Among the extant air-breathing vertebrates, the avian respiratory system is the most efficient gas exchanger. Novel morphological and physiological adaptations and specializations largely explain its exceptional functional superiority. Anatomically, the avian respiratory system is separated into lungs that serve as gas exchangers and air sacs that operate as ventilators. Utterly rigid, the avian lungs are deeply fixed to the ribs and the vertebrae. A thin blood–gas barrier (BGB), vast respiratory surface area and large pulmonary capillary blood volume generate high total pulmonary morphometric diffusing capacity of O₂. The weak allometric scaling of the thickness of the BGB indicates optimization for gas exchange; the negative scaling and strong correlation between the surface density of the respiratory surface area and body mass show the extreme subdivision of the gas exchange tissue; and the respiratory surface area, the pulmonary capillary blood volume and the total pulmonary morphometric diffusing capacity of O₂ correlate strongly and positively with body mass. The arrangement of the structural components of the exchange tissue form crosscurrent-, countercurrent-like- and multicapillary serial arterialization gas exchange designs. By synchronized actions of the air sacs, the palaeopulmonic part of the of the avian lung is efficiently ventilated continuously and unidirectionally in a caudocranial direction.

This article is part of the theme issue ‘The biology of the avian respiratory system’.

1. Introduction

Comprising a constellation of sizes, shapes and colours (plumage), the distinctly morphologically homogenous feathered avian faunae [1] comprise ‘extraordinary creatures’ [2] that ‘are loved by everybody’ [3]. The so-called ‘Darwin’s finches’ of the Galápagos Islands decisively informed Charles Darwin [4] on the formulation of the theory of evolution by natural selection. In recognition of the adverse effects that global warming, in particular, and climate change, in general, are currently having on the life and the distribution of animal life [5], the natural science of birds has become considerably instructive [6] in understanding the impact of these challenges. For birds, aspects such as changes in migration times and routes followed, and distances covered are important signatures of environmental perturbations [7,8]. Because birds easily and quickly vacate injurious habitats, they are reliable bioindicators or sentinel animal species of the status of an ecological system [9]. In an environment, the specific diversity and numerical density of birds specify optimum living conditions [10].

After evolving flight during the Late Jurassic Epoch (ca 150 million years ago), birds dispersed widely geographically and underwent perceptible adaptive radiation and speciation within a short evolutionary time [11]. The number of extant species of birds is established to be more than 10 000 [11,12] but may surpass 20 000 [13]. Although all groups of birds arose from volant progenitors [14,15], approximately 60 species have lost the capacity of flight [16–18]. The evolutionary drivers of loss of flight include lack or scarcity of predators, inordinate increase in body mass and genetic, morphological and lifestyle changes [19,20]. Reduction of energy expenditure is, however, believed to be the primary reason for loss of volancy [17,18]. The rare Island rail (Atlantisia rogersi), which inhabits the isolated predator-scarce rocky island of the Tristan da Cunha Archipelago in the Central South Atlantic Ocean and weighs between 34 and 49 g, is the smallest extant flightless species of bird [16,20]. The heaviest living flying birds weigh ca 20 kg [21]. From their problematic take-off and landing, this body mass appears to mark a critical point at which flight is lost [22,23]: at that juncture, the flight muscles may not generate sufficient energy to lift the bird off the ground and keep it in the air [24]. Accomplishing a speed of 565 km hr^–1, the peregrine falcon (Falco peregrinus) is the fastest flying bird [25,26]. To access hospitable foraging locations, escape adverse environmental conditions, avoid seasonal predators and secure favourable surroundings for reproduction, ca 1800 species of birds migrate over long distances [27,28]. Travelling at an average speed of 146 km hr^–1, aca 285 g weight bar-tailed godwit (Limosa lapponica) flew nonstop over a distance of 28 000 km in 8 days [29,30]. Arctic terns (Sterna paradisea), weighing < 125 g, covered a remarkable distance of > 80 000 km in 207 days [31]. Species of birds such as the Ruppell’s griffon vultures (Gyps rueppellii), the bar-headed geese (Anser indicus) and the Andean geese (Chloephaga melanoptera) that fly to extreme altitudes have been dubbed ‘super birds’ [32]. A Ruppell’s griffon vulture struck a jet craft at an altitude of 11.3 km above sea level [33] and seasonally, bar-headed geese cross the Himalayan mountains at elevations of between 4000 and 8000 m above sea level [34–37].

From their morphological, physiological and behavioural exclusivity, birds have evolved a specialized respiratory system for obtaining O₂ from the air, particularly under the extreme environmental conditions of the high altitude, where temperatures are very low and the air hypoxic. Here, the unique structural and the functional features of the avian respiratory system are succinctly delineated.

2. Structure of the avian respiratory system

The avian respiratory system comprises lungs and air sacs [1,38–40] (figure 1a ). The lungs are small, wedge-shaped compact structures [40] (figure 1b ). Located on the dorsal part of the coelomic cavity [40], the lungs are deeply attached to the vertebrae and the ribs [38–41] (figure 1a–c ). The air sacs connect to the lungs at sites called ostia [1,38–40] (figure 1a,c,d ). A three-tiered airway system that comprises the intrapulmonary primary bronchus, the secondary bronchi and the parabronchi (tertiary bronchi) exists in the avian lungs (figure 1c,d ). As the intrapulmonary primary bronchus transits the lung, it originates four sets of secondary bronchi, namely the medioventral-, the mediodorsal-, the lateroventral- and the laterodorsal secondary bronchi (figure 1c,d ). The secondary bronchi are named according to the part of the lung they deliver air [38–41]. The terminal parts of the secondary bronchi give rise to the parabronchi that anastomose and interconnect the airways [1,38–41] (figure 1c,d ). A parabronchus comprises a gas exchange tissue mantle that surrounds a lumen (figure 1e ). The atria, which extend outwards from the parabronchial lumen (figure 1e ), generate infundibula that, in turn, give rise to the air capillaries (figure 1f,g ). The blood capillaries consist of spatially interconnected segments that are about as long as they are wide [42–45] (figure 1h ). The air and blood capillaries, which are the terminal respiratory (gas exchange) units of the avian lung, entwine very closely (figure 1i ): they are separated by a thin blood-gas (tissue) barrier that comprises a surfactant lining, an epithelial cell, a common basement membrane and an endothelial cell [46] (figure 1j ).

Figure 1.

(a) Lateral and dorsal (insert) views of a latex rubber cast preparation of the respiratory system (the lung–air sac system) of the domestic fowl (df) (Gallus gallus variant domesticus). i–v, air sacs; circles (○), ostia; arrows (↓), costal sulci; Tr, trachea. (b) Dorsal view of the wedge-shaped lungs of the ostrich (Struthio camelus). EPPB, extrapulmonary primary bronchus; Tr, trachea; arrows (↓), costal sulci. (c) Medial view of a latex rubber cast preparation of the lung of the domestic fowl showing the complexity of the airway system. PPP, palaeopulmonic parabronchi; MVSB, medioventral secondary bronchi; IPPB, intrapulmonary primary bronchus; LVSB, lateroventral secondary bronchus; NPP, neopulmonic parabronchi; arrows (↓), costal sulci; dashed white circle, ostium. (d) Lung of the domestic fowl drawn as if transparent to show the complexity of the airway system. PPP, palaeopulmonic parabronchi; NPP, neopulmonic parabronchi; MVSB, medioventral secondary bronchi; MDSB, mediodorsal secondary bronchi; LVSB, lateroventral secondary bronchus; EPPB, extrapulmonary primary bronchus; IPPB, intrapulmonary primary bronchus; dashed encircled areas (○), ostia. The laterodorsal secondary bronchi are excluded to simplify the diagram. (e) Transverse section of a parabronchus of the lung of the domestic fowl. PL, parabronchial lumen; ET, exchange tissue; asterisks (*), atria. (f) Exchange tissue of the lung of the house sparrow (Passer domesticus) showing cross-sectional profiles of air capillaries (AC) and the blood capillaries (BC) that entwine very closely. Arrows (↓), blood-gas barrier; Er, erythrocytes that are contained in the blood capillaries. (g) A latex rubber cast preparation of the lung of the domestic fowl showing AC that interconnect by very narrow passageways (circles (○)). (h) A latex rubber cast preparation of the lung of the domestic fowl showing blood capillaries (BC) and AC that entwine densely. (i) Three-dimensional serial section computer generated reconstruction showing the BC and the AC that entangle compactly. (j) The BGB of the lung of the df showing surface lining (surfactant), Arrows (↓); epithelial cell, diamonds (♦); basement membrane, asterisks (*); endothelial cell, dots (●); erythrocyte, Er; plasma layer, Pl.

At the parabronchial level of organization, the avian lungs display a notable morphological variety [40]. In the more phylogenetically advanced species of birds, generally, the lungs have palaeopulmonic (‘old’ lung) and neopulmonic (‘new’ lung) parts [39]: the palaeopulmo is the less-derived—that is, the basal or the conserved—morphological trait of the avian lung. Even where it is best developed, the neopulmo may constitute as much as 25% of the volume of the lung [39]. The neopulmo is largely found on the caudoventral part of the lung, where it is mainly intercalated between the lung and the caudal air sacs [38–41]. According to Duncker [39,47], the neopulmo serves as the site of gas exchange at rest, while the palaeopulmo is utilized during exercise. In the avian lungs, the existence of the neopulmo mainly explains the difference between the concentrations of CO₂ in the inspired air and that in the caudal air sacs [48–50]: the inspired air collects CO₂ as it flows through the exchange tissue of the neopulmo [51,52].

The air sacs are large, thin-walled structures [1]. In keeping with their locations in the coelomic cavity and particularly around the lungs, functionally, the air sacs comprise a cranial and a caudal group (figure 1a ).In some species of birds, the air sacs extend out of the coelomic cavity and come to lie subcutaneously [38,40,53–57] while others form lung/air sac diverticulae that pneumatized bones [38–40] or they enter or are interposed between certain body structures, for example, the intermuscular diverticula that are found in the subpectoral region [38,40,55,56,58]. Because the air sacs are normally avascular [1,49,59], the structures are not involved in gas exchange [60–62]. After isolating the lungs from the air sacs by ligating the ostial connections and injecting carbon monoxide (CO) into the air sacs, Soum [59] observed no signs of CO poisoning.

3. Function of the avian respiratory system

(a). Air flow dynamics

While on the whole the avian respiratory system is ventilated tidally—that is, in-and-out [1,40,49,63]—the flow of air in the lung and its connected air sacs is complicated [1,50,60,64–69]: many important aspects of the respiratory physiology of birds are still indeterminate [70]. Because of the overall morphological complexity of the avian respiratory system (figure 1a ) and particularly that of the airway system of the lung (figure 1c,d ), the path followed by the inspired air cannot be determined from mere visual examination of the geometry and the arrangement of the airways of the avian lung (figure 1c,d ). It takes two inspiratory and two expiratory cycles, that is, four respiratory phases, for the inspired air to transit the avian respiratory system [1,38,41,48–50,64–66,70–73] (figure 2). During the first inspiratory phase, the inspired air flows through the intrapulmonary primary bronchus to the caudal air sacs (figure 2a ); in the first expiratory phase, the air flows from the caudal air sacs into lung (figure 2b ); in the second inspiratory phase, the air travels from the lung to the cranial air (figure 2c ) and; during the second expiratory phase, the air flows from the cranial air sacs to the outside [48,64,69–71] (figure 2d ). With the lungs located between the cranial and the caudal groups of air sacs (figure 1a ), the exchange tissue of the palaeopulmonic parabronchi is ventilated (by the air sacs) continuously and unidirectionally in a caudocranial, that is, back-to-front, direction by synchronized actions of the air sacs [40,49,64,70,71]. Because the neopulmonic parabronchi are largely located on the caudoventral aspect of the lung, where they are mostly sited between the lung and the caudal air sacs, the airways are ventilated bidirectionally [38–41]. In the avian lung, the palaeopulmonic parabronchi and the intrapulmonary primary bronchus are in effect arranged in parallel [48,64,70–72] (figures 2a,b and figure 3): the arrangement permits the palaeopulmonic parabronchi (specifically their exchange tissue) to be ventilated unidirectionally. With vitiated (dead-space) air, that is, CO₂-loaded air, lacking in the exchange tissue of the avian lung, a high partial pressure gradient of O₂ (∆PO₂) is maintained across a thin blood-gas barrier (BGB) [48,50,64,66,73].

Figure 2.

Simplified schematic illustration of the air flow through the avian respiratory system (the lung–air sac system). It takes two inspiratory and two expiratory cycles for a volume of inspired air to enter and exit the respiratory system. (a) During the first inspiratory cycle, the inspired air (shown in blue) flows from outside down the trachea and the primary bronchus to enter the caudal air sacs. (b) In the first expiratory cycle, the air moves from the abdominal air sacs into the palaeopulmonic parabronchi via the mediodorsal secondary bronchi. The dashed square shows the location of the neopulmonic parabronchi where air flows bidirectionally. (c) During the second inspiratory cycle, the air (in the lung) moves into the cranial air sacs. (d) In the second expiratory cycle, the air in the cranial air sacs moves to the outside via the extrapulmonary primary bronchus and the trachea. The question marks (?) on (a) and (b), respectively, show sites where IAV and EAV occur. The insert in (d) gives a view of a delicate semitransparent developing air sac of the domestic fowl (Gallus, gallus variant domesticus).

Figure 3.

Flow of air through the lung–air sac system of birds where palaeopulmo and neopulmo exist. The rather parallel arrangement between the intrapulmonary primary bronchus (IPPB) and the palaeopulmonic parabronchi (PPP) permits flows of inspired air in the passageways to occur in opposite directions and allows the exchange tissue of the palaeopulmo to be ventilated in a caudocranial direction (red dashed arrows): the palaeopulmonic parabronchi connect the mediodorsal secondary bronchi (MDSB) to the medioventral secondary bronchi (MVSB). Black solid arrows, inspired air flowing through the trachea (Tr) and the intrapulmonary primary bronchus (IPPB) to the caudal air sacs (d, e); dashed cyan arrows, expired air flowing from the caudal air sacs through the neopulmo; dashed black arrows, inspired air flowing from the neopulmo into the MDSB; red arrowheads, air flowing out of the lung through the MVSB, the primary bronchus and the Tr. The flow of air in the neopulmo is bidirectional (tidal) (solid black arrows and white dashed arrows). The air sacs comprise a cranial group, that is, the cervical (a), the clavicular (b) and the craniothoracic (c) air sacs and a caudal group that consists of the caudothoracic (d) and the abdominal (e) air sacs. The air sacs connect to the lung at sites called ostia (circles, (o)). Inserts (i,ii): Three-dimensional serial section computer reconstruction (i), histological preparation (ii) and scanning electron micrograph (iii) of a transverse section of lung of the domestic fowl (Gallus gallus variant domesticus) showing the rather parallel topographical arrangement between the PPP and the IPPB. NPP, neopulmonic parabronchi; asterisks (*), medioventral secondary bronchi; SB, secondary bronchi.

In the avian lung, by a mechanism termed ‘inspiratory aerodynamic valving’ (IAV) [74–76], inspired air is shunted past the orifices of the medioventral secondary bronchi (figures 2a and 4a ), while by that designated ‘expiratory aerodynamic valving’ (EAV), air leaving the caudal air sacs is directed away from the intrapulmonary primary bronchus (the way it came in) into the mediodorsal secondary bronchi [68,77] (figures 2b and 3). Using state-of-the-art techniques such as computational fluid dynamics (CFD) and mathematical modelling [74–76], the early on speculation that sphincters (valves) controlled air flow in the avian lungs has been disproved. Compared with IAV [74,77–83], little is known about the mechanism of EAV [68].

Figure 4.

(a) Illustration showing the mechanism of inspiratory aerodynamic valving. Narrowing of the lumen at the terminal part of the extrapulmonary primary bronchus (EPPB) accelerates the inspired air, thrusting it past the orifices of the medioventral secondary bronchi (MVSB) (asteriscs, *). SA, segmentum accelerans;IPPB, intrapulmonary primary bronchus. Inserts: (i) Latex rubber cast preparation of the lung of the domestic fowl (Gallus gallus variant domesticus) of the part of the lung illustrated showing the angulation of the medioventral secondary bronchi and the orifices opening into them (asteriscs, *). (ii) The SA is intensely vascularized. Dots (●), blood vessels. (b) The lung of the domestic fowl, showing the aerofoil-shaped SA that is located at the distal end of the lumen of the EPPB. IPPB, intrapulmonary primary bronchus. Insert: Location of the segmentum accerelans (arrow, ↓) at the distal part of the EPPB.

Interestingly, a well-vascularized, aerofoil-shaped structure—that is, one with a streamlined cross-sectional profile—that protruded into the lumen at the terminal part of the extrapulmonary primary bronchus (EPPB) was reported in the lung of the domestic fowl (Gallus gallus variant domesticus) by Maina and Africa [82] (figure 4b ). From its location and presumed function, the structure was termed ‘segmentum accerelans’. Earlier, after noting a narrowing of the EPPB at the same location after experimentally observing the flow of a radio-opaque gas in the lung of a goose (Anser anser), Wang et al. [78] had reported that a narrowing, that they designated segmentum accerelans, existed. Maina and Africa [82] supposed that the segmentum accerelans worked like the erectile or carvenous tissue, for example, that in organs such as the human pennis: inflow and outflow of blood should regulate the diameter of the lumen of the EPPB. In a computational fluid dynamics study of the lung of the ostrich (Struthio camelus), Maina et al. [73] determined that a segmentum accerelans introduced in the model accelerated the flow of inspired air, thrusting it past the orifices of the mediodorsal secondary bronchi. Overall, for the avian lung, the process ofIAV directs the inspired air to the rear (‘back’) of the lung, that is, to the caudal air sacs (figures 2a and 3), while that of EAV directs the air that leaves the caudal air sacs away from the intrapulmonary primary bronchus (IPPB) into the mediodorsal secondary bronchi of the lung [73–81] (figures 2b and 3): on the whole, the mechanisms permit the avian lung to be ventilated craniocaudally.

(b). Crosscurrent gas exchange system

In the avian lungs, most of the gas exchange tissue is found in the parabronchi (figures 1e and 5a–d ). As the air flows through the parabronchial lumen, it travels outwards, that is, centrifugally, into the exchange tissue (figures 1e and 5a–d ). At the same time, deoxygenated (venous) blood flows inwards, that is, centripetally, from the periphery of the parabronchus into the exchange tissue (figure 5a–f ). The rather perpendicular (orthogonal) disposition between the directions of air flow in the parabronchial lumen and that of venous blood into the exchange tissue forms the crosscurrent gas exchange system. In the lungs of the domestic duck (Anas platyrhynchos domesticus), Scheid and Piiper [71] showed experimentally the existence of a crosscurrent gas exchange system: under steady state breathing, reversing the direction of air flow in the lung did not produce an effect on the partial pressure of O₂ (PO₂) in air as well as that in the arterial and mixed venous blood. Such a gas exchange profile could not be explained by the existence of a functional countercurrent gas exchange system but only by a crosscurrent one. Indeed, if a functional countercurrent gas exchange system existed in the avian lungs, the experimental manipulation [71] would have created a cocurrent one, where air and blood flowed in the same direction. Under such an assemblage, the PO₂ between air and blood would have precipitously dropped.

Figure 5.

(a), (b), (d) and (g) are schematic illustrations; (c) is a histological section; and (e) and (f) are scanning electron micrographs of a double latex rubber cast preparation of the lung of the domestic fowl (Gallus gallus variant domesticus). They show the gas exchange designs that exist in the exchange tissue (ET) of a parabronchus of the lung. (a) Longitudinal view of a parabronchus and the blood vessels that deliver and drain blood to and from the ET. Large cyan-coloured arrows, air flowing through the parabronchial lumen; large purple arrows, deoxygenated (venous) blood flowing in the interparabronchial artery; thin purple arrows, blood flowing into the exchange tissue via the intraparabronchial arteries; thin red arrows, blood draining from the exchange tissue via the intraparabronchial veins; large red arrows, blood draining from a parabronchus through an interparabronchial vein. The crosscurrent gas exchange system (CrCGES) comprises the rather perpendicular disposition between the flow of air in the parabronchial lumen and the inwards (centripetal) one of the venous blood in the exchange tissue; the countercurrent-like gas exchange system (CoClGES) is constituted by the inwards flow of venous blood in the exchange tissue and the outwards (centrifugal) one of air in the exchange tissue; and the multicapillary serial arterialization gas exchange system (MCSAGES) consists of the sequential arrangement of the considerably many air capillaries and blood capillaries in the exchange tissue, where gas exchange occurs. (b) View of a transverse section of a parabronchus where the exchange tissue surrounds the parabronchial lumen. The CrCGES, the CoClGES and the MCSAGES are shown using the sizes and colours of arrows defined above. Thin arrows (↓), atria; asterisks (*), interparabronchial arteries; arrowheads, intraparabronchial arteries. (c) A histological transverse section of a parabronchus of the lung of the house sparrow (Passer domesticus). The CrCGES and the CoClGES are shown and explained using the sizes and colours of arrows explained above. (d) Schematic illustration of a parabronchus and the blood vessels associated with it. The CrCGES, the CoClGES and the MCSAGES are shown using the colours and sizes of arrows defined above. (e, f) Double latex rubber cast preparation of the lung of the domestic fowl (G. g. var. domesticus) showing the CrCGES and the MCSAGES (defined and shown above). Dashed yellow lines, locations of parabronchi; circles, interparabronchial arteries; thin purple arrows, intraparabronchial arteries. Dots (●) in (f), atria. (g) Sequential arrangement and interaction of the air capillaries and the blood capillaries in the exchange tissue of a parabronchus, forming the MCSAGES (explained above).

(c). Countercurrent-like gas exchange system

Regarding physical processes such as heat and gas transfer, human-engineered and naturally evolved countercurrent exchange systems are profoundly superior [84–88]. This is primarily because the exchanging media flow in opposite directions and therefore the corporeal driving force/pressure exists until an equilibration point is reached. For the avian lung, venous (deoxygenated) blood flows ‘inwards’ into the exchange tissue—that is, from the periphery of a parabronchus—while air travels ‘outwards’ from the parabronchial lumen (figure 5a–f ). Over a long period of time, it was claimed that a countercurrent gas exchange system existed in the avian lung [87–89]. In fact, from mere speculation rather than from empirical evidence, early in the investigation of the avian respiratory system physiology [90] up to as recently as five decades ago [87], it was claimed that a countercurrent gas exchange system explained the exceptional respiratory efficiency of the avian lung. This once intuitively appealing suggestion is, however, no longer acceptable [48,72,91]. Reviewing the literature, Scheid [48] dismissed the assumed countercurrent gas exchange system as an auxiliary mechanism superposed on, and independent of the basic crosscurrent arrangement [48, p. 171]. For a conventional countercurrent gas exchange system to exist in the exchange tissue of the avian lung, two features would have to exist: (i) air and blood capillaries would have to interface over critical distances and (ii) air and blood would have to flow in opposite directions. However, such circumstances do not exist in the avian lung [1,41]. Notwithstanding, the air and the blood capillaries are separated by only microscopic distances [1,43–45] and because the structures intimately entwine three-dimensionally, counter flow of air cannot be maintained (figure 1f–i ). To de-emphasize its functional utility, in the exchange tissue of the parabronchus of the avian lung, the ‘outward’ flow of air from the parabronchial lumen and the ‘inward’ one of venous the blood should be properly termed as a ‘countercurrent-like gas exchange system’.

(d). Multicapillary serial arterialization gas exchange system

In the parabronchus of the avian lung, venous blood is delivered to all parts of the exchange tissue at about the same time by the intraparabronchial arteries (figure 5a–f ): the respiratory gas concentrations of the blood in the blood capillaries equilibrate with air in the air capillaries as the latter's composition varies during breathing. At the entrance of a palaeopulmonic parabronchus (the part that connects to a mediodorsal secondary bronchus), venous blood is exposed to air with high partial pressure of oxygen (PO₂) and low partial pressure of carbon dioxide (PCO₂), while at the opposite end (the part that joins the medioventral secondary bronchus), gas tensions are reversed, that is, PO₂ is lower and PCO₂ greater. The multicapillary serial arterialization gas exchange system comprises the numerous places (in the exchange tissue of a parabronchus) where the air and the blood capillaries are in contact and O₂ and CO₂ are exchanged (figure 5a,b,d–g ). From the multicapillary serial arterialization gas exchange system, the quantity of O₂ in the oxygenated (arterial) blood that returns to the heart via the pulmonary vein derives from an additive, that is, cumulative, process where O₂ is collected at the considerably many points where air and blood capillaries contact (figures 1f–i and 5a,b,d,e–g ). The multicapillary serial arterialization gas exchange system extends the time during which air is exposed to pulmonary capillary blood across the BGB (figure 1j ). For the lung of the domestic fowl, the total length of the parabronchi (if they were connected end-to-end) is reportedly approximately 30 m [92]. The property increases the volume of the parabronchial gas exchange tissue which in turn increases the respiratory surface area.

The existence of crosscurrent and the multicapillary serial arterialization gas exchange systems have been morphologically corroborated in the gas exchange tissue of the parabronchi of the avian lung [1,41–45,93]. Functionally, the designs are not autonomous entities. They are greatly integrated assemblages that work as a single unit. While the countercurrent-like gas exchange system does not appear to play a gas exchange role, its presence is vital to the configuration of the crosscurrent gas exchange- and the multicapillary serial arterialization systems.

4. Morphometrics of the avian lung

In the vertebrate gas exchangers, the volume of the lung, the respiratory surface area (that is, the surface area of the BGB), the pulmonary capillary blood volume and the thickness of the BGB are the most important morphometric parameters that determine gas exchange efficiency [1,41,93–99]. In birds, the volume of the lung comprises as much as 34% of the volume of the body [98]. For animals of equivalent body mass, the volume of the avian lung is approximately 27% smaller than that of a nonvolant mammal [41,94–97,100,101]. In birds, the volume of the lung correlates strongly (r = 0.9970) and scales positively (b = 1.5467) with body mass [1,41,95,99] (figure 6a ). With respective values of 42.8 and 42.9 cm³ kg^–1, among the species of birds that have been investigated, the Andean goose [100] and the violet-eared hummingbird (Colibri coruscans) [101] have the greatest mass-specific volume of the lung. From the extreme compartmentalization (subdivision) of the exchange tissue of the avian lung (figure 1e–h,i ), the surface density of the BGB per unit volume of the exchange tissue correlates strongly (0.7679) and scales negatively (−0.1031) with body mass (figure 6b ). In the avian lungs, the high surface density of the BGB explains how and why, for birds, the lung has a respiratory surface area that is ca 15% greater than that of a nonflying mammal of comparable body mass [1,41,95,100,101]. Strong positive correlation (r = 0.9952) and scaling (b = 0.8674) exist between the respiratory surface area of the avian lung and body mass [41,100,101] (figure 6c ). Among the species of birds that have been investigated, the respective body mass-specific respiratory surface areas of the lungs of the Andean goose and the violet-eared hummingbird, that is, 96.5 and 87.1 cm² g^–1 [100,101], are the greatest. The harmonic mean thickness of the BGB of the avian lung is ca 2.5 [102] and ca 56–67% [41,95,99] times thinner than those of the lungs of nonvolant mammals of equivalent body mass. The violet-eared hummingbird [101] and the African rock martin (Hirundo fuligula) [41,95,99] have the thinnest BGBs of harmonic mean thicknesses respectively of 0.099 and 0.090 µm, respectively. The lungs of the ostrich [103], the Humboldt penguin (Spheniscus humboldti) [104] and the Chilean tinamou (Notoprocta perdicaria) [105], with respective harmonic mean thicknesses of 0.56, 0.53 and 0.47 µm, are—among the bird lungs that have been studied—the thickest. In birds, weak correlation (r = 0.4512) and low scaling (b = 0.0687) exist between the harmonic mean thicknesses of the BGB and body mass [41,96,100] (figure 6d ). In the avian lung, the volume of blood comprises as much as 36% of that of the organ: 58–80% of it located in the blood capillaries [1,41,95,100,105]. The pulmonary capillary blood volume correlates (r = 0.9899) and scales (b = 0.9594) strongly with body mass [1,41,95,100] (figure 6e ). The total pulmonary morphometric diffusing capacity of O₂ , a parameter that conveys the conductance of O₂ by the avian lung [95–98], correlates (r = 0.9863) and scales (b = 0.9198) strongly with body mass [1,41,95,100] (figure 6f ).

Figure 6.

Allometric relationships of some pulmonary morphometric parameters of the bird lungs. (a) Relationship between the volume of the lung (VL) and body mass: strong positive correlation exists between the parameters. (b) Relationship between the surface density of the BGB (S_V) and body mass: strong negative correlation exists between the parameters. (c) Relationship between the respiratory surface area (SA), that is, the surface area of the BGB, and body mass: strong positive correlation exists between the parameters. (d) Relationship between the harmonic mean thickness of the BGB and body mass: weak positive correlation exists between the parameters. (e) Relationship between the pulmonary capillary blood volume and body mass: strong and positive correlation exists between the parameters. (f) Relationship between the total morphometric pulmonary diffusing capacity and body mass: strong and positive correlation exists between the two parameters.

5. Conclusions

The unique structural and functional properties of the avian respiratory system mainly explain its notable respiratory efficiency. Among others, the foremost features are the crosscurrent and multicapillary serial arterialization gas exchange systems, the unidirectional continuous ventilation of the lung and novel morphometric specializations. As usually stated with regard to elegant states, events and processes, among the evolved vertebrate gas exchangers, the avian respiratory system is the ‘epitome of cool’.

Ethics

This work did not require ethical approval from a human subject or animal welfare committee.

Data accessibility

This article has no additional data.

Declaration of AI use

I have not used AI-assisted technologies in creating this article.

Authors’ contributions

J.N.M.: conceptualization.

Conflict of interest declaration

I declare I have no competing interests.

Funding

I am most grateful to the National Research Foundation (NRF) of South Africa for supporting the preparation of this work and funding my past research activities. I greatly appreciate the contributions which many of my students and collaborators have made as we have undertaken a long exciting journey of exploration.