THE ANATOMICAL RECORD (NEW ANAT.) 261:25– 44, 2000
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Comparative Respiratory Morphology: Themes and Principles in the Design and Construction of the Gas Exchangers JOHN N. MAINA*
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. © 2000 Wiley-Liss, Inc. KEY WORDS: respiration; lungs; gills; oxygen; adaptation; evolution; comparative anatomy
“The Lord God formed man from the dust of the ground and breathed into his nostrils the breath of life, and man became a living being.” (Genesis 2:7) Few processes are as vital for life as respiration. The metabolic scope of an animal is set by the capacity of the gas exchanger to deliver oxygen to the tis-
Dr. Maina received his B.V.M. at the University of Nairobi and his Ph.D. and D.V.Sc. degrees at the University of Liverpool. He is Professor and Chair of the Department of Anatomical Sciences at the University of the Witwatersrand in Johannesburg, South Africa. Dr. Maina’s research focuses on the structural-functional correlation of respiratory morphology in many organisms. His most recent investigations involve the comparative ultrastructural morphology of birds, small mammals, crustaceans, and fish. *Correspondence to: J.N. Maina, Department of Anatomical Sciences, The Medical School, University of the Witwatersrand, 7 York Road, Park Town, Johannesburg, 2193, South Africa. Fax: 27-11-647-2422. E-mail:
[email protected]
© 2000 Wiley-Liss, Inc.
sues. In antiquity, before the discovery of oxygen by Joseph Priestley in 1771, and again 3 years later, the determination of the composition of air by Antoine Lavoisier, it was well recognized that breathing, a process experienced, observed, and felt in many animals, was essential for life. Until recently, failure or lack of breathing was taken to be a sign of death and the common method of killing was by strangulation. The popular phrases “breath of life” and “kiss of life” are used to express the importance of breathing in sustaining life. Fundamentally, animals face similar challenges for survival, including those for acquisition of oxygen, the subject of this review. While similar challenges may not necessarily compel corresponding adaptive solutions, certain respiratory designs have remained unchanged under the very different adaptive pressures that different animal lineages have endured during their evolutionary histories. Wagner (1998) called such conserved features “the frozen core” (the Bau-
plan). The strongly defended states and developments must be of considerable importance for life and should be of great interest to functional morphologists. To present a holistic picture of the transactions that were central to the evolution of the different designs of gas exchangers, a comparative morphological approach is heuristically useful. This account focuses on the resemblances while looking at the differences.
RESPIRATION: FUNDAMENTAL CONCEPTS Oxygen: Vital but Paradoxical Molecule Acquisition of oxygen from the atmosphere is the primary purpose of respiration. Oxygen is the most important molecule contracted from the external environment. It is an important factor for aerobic metabolism and a necessary resource for growth and development. Animals will generally live for weeks without food, days without water, but only minutes with-
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Figure 1. Oxygen diffusion pathway in the gills. Thickness and surface area determine the diffusing capacity of a gas exchanger. The serial resistance barriers only differ in detail in the lungs.
out oxygen. Activities such as feeding, locomotion, and reproduction can be altered, delayed, or even totally abandoned. Energy is decisive in all biological events from molecular, biochemical, ecological, and evolutionary levels. In biology, energy is what money is to economics: it is the currency by which living things procure essential commodities and services. Like money, to serve a useful purpose, within certain limits, energy is interchangeable. The respiratory rate of an animal bespeaks of its pace of life. It determines the rate at which an animal utilizes its resources to meet the demands placed on it by the environment and lifestyle. Animals that maintain a high oxygen to carbon dioxide exchange ratio relative to their body sizes are the most successful. Under a partial pressure gradient, oxygen diffuses from the atmosphere through a composite tissue barrier (Fig. 1) at a rate of 2.3 ⫻ 10⫺5 cm2.s⫺1, a process completed in about 250 to 500 milliseconds. Since its incorporation in aerobic metabolism some 2 billion years ago (e.g., Schopf et al., 1993), no other molecule has been as consequential in shaping life and as paradoxical in its operation as oxygen. A 70 kg adult human uses 14.5 L of oxygen.h⫺1 or about 1020 molecules.s⫺1 at rest: the quantity rises to about 330 L.h⫺1 during exercise. Unlike certain molecular factors that can be reserved in the body, owing to its high toxicity, molecular oxygen cannot be stored in the
body. It has to be continuously procured from outside. Only an insignificant amount of oxygen exists freely in the body. In humans, at any moment, there are only about 1.55 L of oxygen in the body. Of that, about 370 cm3 is in the alveoli, 280 cm3 in the arterial blood, 600 cm3 in the capillary and venous blood, 60 cm3 dissolved in body tissues, and 240 cm3 is chemically held by the muscle myoglobin (Farhi and Rahn, 1955): the total amount of oxygen in the body can only support life for about 6 min. Life started in an anaerobic environment in the so called ‘primodial broth’ (a mixture of organic molecules; e.g., Bar-Nun and Shaviv, 1975): absence of oxygen, a highly oxidizing molecule, was requisite for the occurrence of the fortuitous event. Subsequently, oxygen paradoxically became an indispensable factor for aerobic metabolism especially in the higher life forms. The rise of an oxygenic environment was a momentous event in the diversification of life. It evoked a dramatic shift from inefficient to sophisticated oxygen dependent oxidizing ecosystems. Anaerobic fermentation, the metabolic process that prevailed for the first about 2 billion years of the evolution of life, was a very inefficient way of extracting energy from organic molecules. A molecule of glucose, e.g., produces only two molecules of ATP (⬇ 15 kCal) compared with 36 ATP molecules (⬇ 263 kCal) in oxygenic respiration. Aerobic metabolism must have developed
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at a critical point when the partial pressure of oxygen rose from an incipient level to one adequately high to drive it passively across the cell membrane. Despite the striking morphological diversification of the respiratory organs, the acquisition of molecular oxygen by diffusion has remained the same for the last about 2 billion years: ways have changed but means have endured! The alternate method of acquisition of oxygen would have been by an active process. This strategy seems to have been rejected very early in the evolution of life, if it was ever attempted. It has, however, been suggested that the transfer of oxygen in organs and tissues such as the lung, liver, placenta, and muscle may be facilitated (e.g., Wittenberg, 1976): hemoglobin, myoglobin, and a specific carrier (cytochrome P450) have been implicated. Supporting aerobic metabolism driven by an active process would obligate an immense energy cost for crucial molecule continuously required in large quantities throughout life. Conceivably, this would render the respiratory process uneconomical or even irreconcilable with the present structural designs of the gas exchangers. Nature is highly inventive and ceaselessly cultivates optimal solutions to functional demands. Amidst the infinite design possibilities, the ultimate structures must offer the best solutions under the conditions that they evolve and the roles that they are programmed to perform.
Figure 2. Exposure of blood to air for efficient gas exchange. A: Blood capillaries (*) protruding into the alveolar space in a mammalian lung (lesser bushbaby—Galago senegalensis): s, interalveolar septum; 3, intercellular junctions of the squamous Type I cells. ⫻1,075. B: A double capillary arrangement in a reptilian lung (snake— Dendroapis polylepis): *, blood capillaries; r, red blood cell; s, interfaveolar septum; 3, thin Type I cells. ⫻3,600. C: Vascular channels (*) bulging into the air space in the lung of a pneumonate gastropd (slug—Trichotoxon copleyi). ⫻270. D: A red blood cell (r) pressing onto a blood-gas barrier (E) causing the blood capillary to bulge out and barrier to become thinner (lung of a lesser bushbaby): 3, Type I cell. ⫻20,000.
Figure 2.
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Confounding Conservativeness in the Evolvement of the Gas Exchangers The modern gas exchangers are products of a long evolutionary process. The present designs have been reached through a fierce cost-benefit analysis. Despite the many forms that have developed, in certain regards, the structure of the gas exchangers has largely been refractory. There are no tissues or cells that are absolutely distinctive to the respiratory organs, e.g., like hepatocytes are to the liver, podocytes to kidneys, osteocytes to bone, erythrocytes to blood, or neurones to nervous tissue. An unspecialized surface, e.g., a cell membrane is the most elementary but practical gas exchanger. In some primitive animals, certain structures once thought to be respiratory are now known to have no meaningful gas exchange role (e.g., Mangum, 1982). The structure of the gas exchangers must be read and interpreted carefully, especially in the so called ‘primitive’ organisms. The population of cells collectively called pneumocytes has very few common morphological characteristics that are specific to the respiratory role of the organs in which they are found. For example, while the Type I pneumocytes are squamous (Fig. 2A,B,D), devoid of organelles, and hence metabolically inert, the Type II cells are cuboidal (Fig. 13D), have many cells organelles (Fig. 13C), and are relatively metabolically active. While the morphological features of the Type I cells promote gas exchange by reducing the thickness of the blood-gas barrier, those of the Type II cells don’t conform to the prescriptions for an efficient respiratory function. Furthermore, in the lungs of the lower vertebrates (e.g., lungfishes, amphibians, and certain reptiles), the pneumocytes have not completely differentiated into Types I and II cells (e.g., Maina, 1987). The morphological nonspecificity of the respiratory organs, especially that of their constitutive structural components, could be ascribed to the fact that in all gas exchangers, simple or complex, wateror air breathing, oxygen uptake occurs by the same process, i.e., diffusion. It would appear that the respira-
tory organs have strictly not evolved a prescribed anatomy. For a process that is as inclusive and important as respiration, whether by default or by design, morphological plasticity may be one of the most important features that has allowed the adaptive radiation of the animal species. Animals at different levels of development can subsist in the same habitat without being severely stifled by lack of a dedicated respiratory organ. Problems with water conservation, osmoregulation, and temperature regulation rather than respiration largely determine the ecological distribution of animals. Contrary to the common notion that the surfaces of lungs are dry, a thin hydrated extracellular layer permanently lines virtually all the invag-
For a process that is as inclusive and important as respiration, whether by default or by design, morphological plasticity may be one of the most important features that has allowed the adaptive radiation of the animal species. inated gas exchangers (e.g., Chinard, 1992). In the large air spaces, the hydrated layer occurs in form of an aqueous subphase that comprises of mostly mucus (a glycoprotein-containing substance which is about 98% water) in which proteins, carbohydrates, ions, and surfactant are dissolved (e.g., Sturgess, 1979). The human lung contains about 15–70 cm3 of the epithelial lung lining fluid (ELLF; Rennard et al., 1986). For oxygen to traverse the blood-gas (tissue) barrier (Fig. 1), it has to dissolve in the ELLF. At the alveolar level, the ELLF is 0.1 to 0.24 m thick (Stephens et al., 1996). During strenuous exercise, accumulation of ELLF on the surface of the lung is thought to produce a transient decrease in the membrane diffusing capacity of the lung (Manier et
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al., 1991). In a delicate processes that entails regulation of hydrostatic and osmotic forces across the blood capillary wall, the pulmonary surface is kept moist but not flooded (Fishman, 1972). Amazingly, The ELLF is preserved despite the fact that the oncotic (colloidal osmotic) pressure of plasma proteins that is about 3.3. to 4 kPa is normally higher than the lung microvascular hydrostatic pressure of about 1.1 to 1.2 kPa, a state that should lead one to expect the surface of the lung to be dry and to absorb rather than filter fluid in its circulation. Paradoxically, when introduced into the alveoli, water quickly passes into the pulmonary capillaries (e.g., Effros et al., 1992; Grimme et al., 1997). In animals in which the pulmonary blood pressure is higher than the oncotic pressure (e.g., turtles), “water” may form a significant portion of the oxygen diffusional pathway in the lung (e.g., Burggren, 1982). In insects, the terminal tracheoles contain fluid that is osmotically imbibed into the tissue cells or discharged into them, depending on the metabolic states of the tissues (Wigglesworth, 1953). Oxygen does not diffuse efficiently across dry respiratory surfaces (e.g., Dupre et al., 1991). From their continued dependency on “water” for oxygen transfer across the blood-gas (tissue) barrier, though physically living on land, it could well be argued that absolute air breathers have not evolved (Maina, 1998). In reptilian and mammalian lungs, inundation of the lungs with fluid (in utero) may provide an important biomechanical force for the formation of the air passages and spaces (Alcorn et al., 1977): on contraction of
Figure 3. Morphology of the avian lung. A: Dorsal view of a cast of the lung-air sac system of the domestic fowl (Gallus domesticus) showing a trachea (E), clavicular air sacs (r), lungs (3), cranial thoracic air sacs (e), caudal thoracic air sacs (n), and abdominal air sacs (t). ⫻0.5. B: Medial view of a cast of a lung of the domestic fowl showing the medioventral secondary bronchi (E), the intrapulmonary primary bronchus (i) and a parabronchial system (p). The lung is compact and inexpansile. ⫻0.5. C: Parabronchi (p) of the lung of an emu (Dromaius novaehollandiae): e, exchange tissue. ⫻75. D: Air capillaries (x) and blood capillaries (e) of the lung of the domestic fowl. ⫻5,230.
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THE ANATOMICAL RECORD (NEW ANAT.) 29
Figure 3.
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the smooth muscles, the pressure in the fluid-filled lung causes formation of the air cells. Though best known for their respiratory function, the gills and the lungs are multifunctional organs (Bakhle, 1975; Neckvasil and Olson, 1986). Gills perform functions such as elimination of carbon dioxide, osmoregulation, acid-base balance, ammonia excretion, regulation of circulating hormones, and detoxification of the plasma borne harmful substances. The lungs metabolize and control the concentrations of many active pharmacological agents in the body, e.g., prostaglandins, serotonin, and bradykinin. The ultimate designs of the respiratory organs must synthesize the primary and the secondary functions. Oftentimes, the structural designs necessary for the performance of such functions conflict. While a minimal amount of structural tissue abets respiration (oxygen diffusion is rapid and the gas exchanger itself utilizes less of it), a critical tissue mass is essential for the nonrespiratory roles. Among the organs in the body, the lungs possess the greatest diversity of constituent cells (e.g., Breeze and Wheeldon, 1977): in the human fetus, as many as 20 cell types are in place by the 14th week of gestation.
BIOENGINEERING ASPECTS IN THE DESIGN OF THE RESPIRATORY ORGANS An inquiring observer cannot fail to be impressed by the excellence of the different designs in biology. In comparative morphology, the main objective is to discern the integrative principles that explain away the basis of animal form. Such prescriptions should diffuse across groups. They must provide a rational explanation of the origin and the basis of form while delineating the specific constraints, compromises, and trade-offs involved in their fabrication. In many morphological accounts, perhaps from their intuitive appeal, differences rather than similarities are routinely stressed. In such cases, the broad picture that animals have evolved from a common ancestor and hence are “historically” related is missed. The most important structural features that promote the diffusing ca-
pacity (influx of oxygen) of a respiratory organ are an extensive surface area and a thin tissue barrier. In the lungfishes, amphibians, and largely in reptiles, the blood capillaries form a double capillary arrangement, i.e., the blood capillaries are located on opposite sides of the septa (Fig. 2A–C). The diametrical disposition of the blood capillaries allows only one side of a capillary and hence only one-half of the potential surface area to be utilized in gas exchange. In such lungs, a high capillary loading (volume of the pulmonary capillary blood per unit respiratory surface area), a state in which a large volume of blood is exposed to air across a limited surface area, occurs. In the mammalian lung, the blood capillaries are organized in a single capillary plan giving a low capillary loading: blood is exposed to air across an extensive surface area, offering more efficient gas transfer. In practically all lungs, the blood capillaries bulge from the respiratory surface, both as a result of prevailing intramural (hydrodynamic) pressure and particularly from compaction of red blood cells (Fig. 2D), enhancing the exposure of the blood to air. In the bird lung, the blood- and air-capillaries, the terminal gas exchange components, interdigitate closely with each other providing a large gas exchange surface area (Fig. 3D). In fish, the surface area of the gills has been increased by way of a stratified design where the gill arches give rise to many gill filaments and the filaments in turn to numerous secondary lamellae (Fig. 4A,B). In lungs, a large respiratory surface area is attained by airway subdivision into small terminal gas exchange units (Fig. 5A–D). In the human lung, the respiratory surface area is about 100 times that of the body. While a geometrical sphere of a volume of 1 cm3 has a surface area of 4.8 cm2, 1 cm3 of the parenchyma of the lung of a shrew (the smallest extant mammal) has an area of 2,100 cm2 (Gehr et al., 1980). There are about 300 million alveoli with an average diameter of 250 m in the about 5 L of the human lung (Weibel, 1963). To enhance gas exchange between the external and internal media, sheet-flow designs (e.g., Fung and Sobin, 1969) predominate in the gas exchangers. Connective tissue (lungs) and pillar
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cells (fish gills) connect parallel rows of epithelial cells, fashioning narrow interconnecting blood passages (Fig. 4C,D): the blood spreads into a thin film over an extensive respiratory surface. In the human lung, some 213 cm3 of capillary blood is “stretched” over an area of about 150 m2 (Gehr et al., 1978), a surface area about that of a tennis court! Evidently, there is a limit to the degree to which internal subdivision of the lung can be used to increase the respiratory surface area without compromising the structural and functional integrity of the organ. Space is always a premium in the body and hence the internal organs must be properly sized and organized. To maximize surface area in a limited volume, increased subdivision produces small gas exchange units (Fig. 5A–D). This engenders high surface tension forces at the air-tissue interface. Small respiratory units are both particularly susceptible to collapse and are costly to inflate. According to Young-Laplace’s Law (e.g., Wilson, 1981), the pressure needed to distend a sphere is proportional to the surface tension and inversely proportional to its radius. The extremely narrow air capillaries (4 –10 m) that comprise most of the parabronchial gas exchange tissue of the bird lung (Fig. 3C) were feasible only because birds evolved a small compact, nonexpansile lung (Fig. 3A,B). In mammals, the smallest alveoli (30 m) are found in the lung of the bat (Tenney and Remmers, 1963). In the shrew, the alveolar surface density [surface area per unit volume of the parenchyma (⫽ the gas exchange tissue) and a relative measure of the intensity of parenchymal subdivision], is 2,800 cm2 䡠 cm⫺3 and the harmonic mean thickness of the
Figure 4. Gills of a teleost fish. A: Gill filaments (f) and secondary lamellae (s). B: Cast of the gill vasculature showing a filament artery (f) giving rise to afferent arterioles that carry blood to the secondary lamellae (s). ⫻175. C: Close up of vascular channels of a secondary lamella separated by pillar cells (p): m, marginal channel. ⫻5,200. D: A secondary lamella separated by pillar cells (p) into vascular channels (x): r, red blood cell; e, epithelial cell; E, waterblood barrier; w, space occupied by water. ⫻27,040.
Figure 4.
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blood-gas barrier (the thickness of the blood-gas barrier that sets the flux of oxygen across the lung) is only 0.25 m (Gehr et al., 1980). Comparing values from a wide range of terrestrial mammals (including the human being; Gehr et al., 1981), bats (Maina et al., 1991), and birds (Maina et al., 1989), among the air breathing vertebrates, the most intense subdivision of the gas exchange tissue (Fig. 6) and the thinnest blood-gas barriers (Fig. 7) occur in the lungs of birds. The principal diagnostic features of a gas exchanger include one or more of the following features: a) the partial pressure of oxygen in the external respiratory medium must exceed that in the internal one, b) agitation of the external medium by forward movement or by specialized structures (e.g., cilia) to increase the partial pressure of oxygen at the body surface/respiratory medium interface, c) partial pressure of oxygen lower and partial pressure of carbon dioxide higher in the effluent (outgoing) respiratory medium and vice versa in the influent (incoming) one, and d) structural modifications such as infolding, outfolding, stratified organization, and internal subdivision. Because they have an extensive surface area per unit volume, the unicells (Fig. 8A) and the modest multicellular organisms do not require a specific respiratory organ. In the more complex animals (where diffusion is inadequate for supplying oxygen to the tissue cells), circumscribed respiratory sites have evolved through evagination (out-folding) and invagination (intucking; Fig. 8B–F): gills model the first category of gas exchangers and the lungs the second. Transitional (amphibious) breathers, animals that subsist at the air/water interface, have developed evaginated respiratory organs that function in water and invaginated ones air (Fig. 8C,D), as exemplified by the catfish, Clarias mossambicus (Fig. 9A–D; Maina and Maloiy, 1986). In advanced animals, a circulatory system was necessary to transfer oxygen from the gas exchanger to the distant tissue cells. Since water and air as respiratory media greatly differ physicochemically (e.g., Dejours, 1988), inescapably, trade-offs and compromises were necessary during the shift from water- to air-breathing. While a large surface area enhances oxygen uptake across a
gas exchanger, in a dry environment it promotes water loss. A reduced water loss to oxygen extraction ratio was requisite for life on the desiccating terra firma. Since in most land habitats the atmosphere is never 100% saturated with moisture, evaginated gas exchangers are unsuitable for terrestrial habitation. On the plus side, however, by the very nature of their design, the evaginated gas exchangers (Fig. 8B–D) can be continuously and unidirectionally ventilated with water. Perfusion of the gills with blood in the opposite direction to that of the flow of the water produces a counter-current arrangement (Figs. 10 and 12C). Since water with a high partial pressure of oxygen meets venous blood with a low value, a high partial pressure gradient is established between the two media. While water loss across invaginated gas exchangers is curtailed, such respiratory
In a shrewd process, birds and insects overcame this limitation by evolving lung-air sac (Fig. 3A) and trachealair sac (Fig. 11A,B) systems, respectively. organs can unfortunately only be tidally (⫽ bidirectionally) ventilated (i.e., air moves in-and-out). Since the “fresh” inspired air is diluted by the “stale” (dead space) air, tidal breathing is an inefficient mode of ventilating gas exchangers. Espousing a common statement that “the only law that holds true without exception in biology is that exceptions exist for every law,” in a shrewd process, birds and insects overcame this limitation by evolving lung-air sac (Fig. 3A) and tracheal-air sac (Fig. 11A,B) systems, respectively. Simultaneously, water conservation was achieved by way of invagination of the gas exchanger and a very efficient gas exchange system created through continuous unidirectional ventilation of the terminal gas exchange components. Who said that you can’t have your cake and eat it too? In their most elementary form,
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structurally, gas exchangers comprise two compartments containing respiratory media separated by a tissue barrier. The efficiency of a gas exchanger is set both by the size and the geometrical configuration of the constitutive components (Fig. 12A–F): the later feature determines the manner in which the respiratory fluid media are presented to each other. A wide range of respiratory designs, based on reasonably similar engineering principles, has evolved. When the respiratory media flow in the same direction, the arrangement is termed “co-current” (Fig. 12A). If the media run in opposite directions, the design is described as “counter-current” (Figs. 10 and 12C) and when the media approach each other perpendicularly, i.e., their paths cross, the disposition is termed ‘cross-current’ (Fig. 12E). When the external medium is held constant while interfacing with a gas exchanger (e.g., skin and buccal cavity; Fig. 12B) or a gas exchanger is ventilated with a medium in which the partial pressure of oxygen is reasonably uniform (e.g., lung; Fig. 12D), the arrangements are termed ‘infinite pool’ and “uniform pool” respectively (Piiper and Scheid, 1975). Conceivably, owing to its inefficiency, the cocurrent system has rarely developed in biology. The counter-current system is, however, widely found in heat exchangers (e.g. carotid rete of some ungulates and ophthalmic rete in certain birds), salt concentrating systems (e.g., salt glands of marine birds), and in the rete mirabile of gas-secreting organs (e.g., swim bladders of physoclistous— deep water—fish). The efficiency of the counter-current system in the fish gills (Figs. 10 and 12C) is fundamental to survival in water, a medium of low oxygen concentration. The importance of
Figure 5. Subdivision of the lungs into small terminal gas exchange components: A: Mammalian lung (lesser bushbaby—Galago senegalensis): s, alveolar sac; *, alveoli. ⫻600. B: Cross section of a snake lung (black mamba—Dendroapis polylepis) showing faveoli (f) that radiate out (3) from the central air duct (d): v, pulmonary artery. ⫻1.3. C: Lung of a monitor lizard (Varanus exanthematicus): s, septa; e, faveoli. ⫻125. D: Lung of a lungfish (Protopterus aethiopicus): s, septa; e, terminal air cells. ⫻7.
Figure 5.
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Figure 6. Correlation between the respiratory surface density, the surface area of the blood-gas barrier per unit volume of the gas exchange tissue (⫽ parenchyma) [SV (r,p)] and body mass in the lungs of birds, bats, and nonflying mammals. The [SV (r,p)] is a measure of the degree of subdivion of the gas exchange tissue and hence the relative size of the terminal gas exchange components. The air capillaries of the avian lung are remarkably smaller than the alveoli of the mammalian lung. The data on the nonflying mammals are from Gehr et al. (1981), those of the bat from Maina et al. (1991), and birds from Maina et al. (1989).
Figure 7. Relationship between the harmonic mean thickness of the blood-gas barrier (the thickness of the barrier that determines the flux of oxygen) against body mass in the lungs of bats, birds, and nonflying mammals. Birds have particularly thinner barriers than bats and nonflying mammals. The data on the nonflying mammals are from Gehr et al. (1981), those of the bat from Maina et al. (1991), and birds from Maina et al. (1989).
the counter-current arrangement between the water and the blood flow in the fish gills for gas exchange is proved by the fact that if the direction of the flow of one of the medium is reversed (i.e., establishing a co-current system), the oxygen extraction ratio falls to below 10% (Piiper and Scheid, 1975). In birds, through a cross-current exposure of the venous blood to the parabronchial air (Fig. 12E), oxygen concentration in the ar-
terial blood may exceed that in the end expired air. Based on the fact that birds can fly for long distances even at high altitude where the partial pressure of oxygen is low, a feat associated with a remarkably efficient respiratory system, for a long time, a counter-current gas exchange design was speculated to exist in the parabronchial lung. Experimental reversal of the flow of air caused no significant change in the oxygen extraction effi-
ciency of the lung (Scheid and Piiper, 1972): this conclusively showed that a cross-current rather than a countercurrent arrangement exists in the avian lung. Reversal of the direction of flow of one of the respiratory medium in a cross-current design should only change the sequence of the capillary blood arterialization without altering the total amount of oxygen exchanged (Fig. 12E). If a countercurrent design existed in the avian
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Figure 8. Development models of the gas exchangers. A: In the unicells, oxygen transfer occurs by diffusion across a cell membrane. B: Gas exchangers formed as evaginations (e.g., gills) from the body surface. C: Bimodal breathers have evaginated and invaginated gas exchangers. D: Bimodal breathers, where an air breathing organ has been internally modified, e.g., in the catfish, Clarias mossambicus (see Fig. 9). E: Lungs formed by invagination. F: Tracheal system of insects (T) where oxygen is delivered directly to the tissue cells in some cases the tracheoles indenting the cell to lie in the cytoplasm (C). The arrows show the diffusion of oxygen.
lung, such action would create a cocurrent system (Fig. 12A) with a dramatic drop in the gas exchange efficiency. A counter-current system (Fig. 10) is feasible in the fish gills only because the gills have developed through envagination (Fig. 8B). Except in birds, among the air-breathing vertebrates, uniform pool arrangement occurs in tidally ventilated lungs (Fig. 12D). On account of their design, the internalized gas exchangers fail to fully exploit the high ambient partial pressure of oxygen available to the air breathers since the stale residual air in the passages dilutes the inspired air. In the mammalian lung, the driving pressure at the alveolar surface is reduced from 21 kPa to about 13 kPa, a loss of about one-third of the initial head pressure. On a plus side, however, in an invaginated gas exchanger, stable and well-controlled local respiratory conditions can be conceived. In the vertebrate lung, the alveolar partial pressure of oxygen is lower and the partial pressure of carbon dioxide higher than in the atmosphere: the high alveolar partial pressure of carbon dioxide is used in the important
bicarbonate (HCO3⫺) ion mediated buffer system in pH regulation. Respiratory microenvironments are unrealizable in the evaginated and the infinite pool respiratory designs.
SURFACTANT: ITS FUNCTIONAL SIGNIFICANCE Conspicuously absent in the gills, in various forms and quantities, surfactant is prevalent in the lungs. The primary process of formation of the surfactant has been unchanged at least in the last 300 million years (Power et al., 1999). Initially evolved as a protective cover, with increased partitioning of the lung in the more advanced animals, the surfactant (a phospholipid substance— dipalmitoylphosphatidylcholine) assumed an important role of reducing surface tension and thus stabilization of the extremely small terminal gas exchange components (Fig. 5A–D): the surfactant is spread on the respiratory surface as a monomolecular phospholipid film layer (Cochrane and Revak, 1991) and serves to smooth the alveolar-liquid interface (Bastacky et al., 1995). The gas exchangers with adequate external sup-
port, e.g., the trachea of insects (kept open by the cuticular taenidia), and the gill filaments and the secondary lamellae of the fish gills, respectively supported by cartilages and water, do not have a surfactant. In birds and mammals, the surfactant is secreted by the granular (type II) pneumocytes (Fig. 13C,D). In the lungfishes and amphibians, and generally in reptiles, animals that have large terminal gas exchange units in their lungs (Fig. 5B–D), the pneumocytes are not fully differentiated into type I and II cells. The role of the surfactant in such lungs where the “outermost” gas exchange units are not highly susceptible to collapse from surface tension forces is obscure. However, in addition to the better known roles of reducing respiratory work and stabilizing the gas exchange units, the surfactant plays other important functions such as prevention of transendothelial transudation of blood plasma across the blood-gas barrier, immune suppression, and attraction (chemotaxis) of macrophages (Fig. 13A). The multifarious roles of the surfactant may explain why even simple lungs, where the substance may appear redundant, posses a surface lining. In certain animals, surfactant-like lipids prevent epithelial adhesion during apnea and during deep dives when high hydrostatic pressure may cause the lung to collapse (Daniels et al., 1994). The antiglue role of the surfactant may be more important in the lungs of those animals that do not have well-developed intrapulmonary conducting airways (e.g., amphibians and reptiles) and a diaphragm (e.g., amphibians, reptiles, and birds). In the later, the lung is more vulnerable to the displacements of the organs in the coelomic cavity. The presence of the surfactant on the air capillaries of the avian lung (Fig. 3D), respiratory units that are as narrow as 4 m and virtually rigid (Macklem et al., 1979), is intriguing. However, while the presence of a surfactant on the surface of the avian lung may simply be a phylogenetic carry through from the ancestral reptilian lung, the lining may curtail fluid filtration from the blood capillaries onto the respiratory surface, a process that would curtail the gas exchange process.
Figure 9.
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Figure 10. A counter-current system. The exchange media flow in opposite directions. The numbers are theoretical percentage concentrations of oxygen in the respiratory media; 3, oxygen flow down a concentration gradient; T, a trilaminar tissue barrier; W, direction of water flow; E, erythrocyte; B, direction of blood flow; P, plasma.
GILLS: THE PRIMARY WATER BREATHING ORGANS Combining simplicity of design with functional complexity, gills occur in different sizes, forms, and locations. The common expression ‘like a fish out of water’ describes the general inability of most fish, and other aquatic life forms that use gills, to survive in air. Paradoxically, though exposed to a medium with a higher oxygen concentration, out of water, fish generally die of hypoxia rather than from complications of desiccation, osmoregulation, or temperature shock. Moreover, since carbon dioxide is less ‘soluble’ in air than in water, the animal becomes severely acidotic. While gills are highly efficient aquatic gas exchange organs, in air, the filaments and lamellae (Fig. 4A,B) dry up and become im-
Figure 9. Respiratory organs of a bimodally breathing fish (catfish—Clarias mossambicus). A: Gills (g) and air breathing organs, the suprabranchial chamber membrane (s) and the labyrinthine organ (o). ⫻7. B: Part of a labyrinthine organ showing marked vascular tracts on the surface. ⫻60. C: Close up of the surface of the suprabranchial chamber membrane showing blood capillaries (t) separated by nonvascular tracts (F). ⫻920. D: Cross section of the suprabranchial chamber membrane showing vascular channels (3) separated by the nonvascular tracts (*): g, goblet cells. ⫻1,500.
permeable to oxygen. Furthermore, they cohere due to surface tension and collapse under their own weight in a manner that shore weeds do at low tide. These events result in a reduced respiratory surface area, large interlamellar dead air spaces, and high branchial vascular resistance. Terrestrial vertebrates that can permanently use gills in air have never evolved partly because of the intrinsic constraints on gas exchange and partly because gills serve other important functions, e.g., ammonia excretion and ion regulation, processes that can only be performed satisfactorily in an aquatic medium. The most complex gills are the internal ones of the bony fish (Pisces; Figs. 4A–D, 9A). Gas exchange occurs through the secondary lamellae, thin semicircular flaps that arise bilaterally from a gill filament (Fig. 4A–D). The epithelial surface of a gill arch is structurally and functionally zoned. The filaments are covered by an elaborate epithelium (primary epithelium) while a simple one (secondary epithelium) covers the lamellae. The nonrespiratory functions of the gills take place in the elaborate primary epithelium while gas exchange occurs in the thin secondary epithelium (Fig. 9D). Pavement cells are attenuated broad cells that line the lamella surface (Fig. 13B). Chloride cells (iono-
cytes) are highly specialized osmoregulatory cells found in the primary epithelium (Fig. 13B): they lie in close proximity to the blood vessels. Characteristically, the chloride cells have numerous mitochondria and a dense intracytoplasmic tubular network. The lamellae are divided into channels by pillar cells that span the vascular space interconnecting parallel epithelial cell layers (Fig. 4B–D). The pillar cells maintain the structural integrity of the secondary lamellae, preventing collapse or overdistension under undue intramural blood pressures. They possess contractile microfilamental actomyosin elements and collagen (Bettex-Galland and Hughes, 1973). By altering the diameters of the vascular channels, the pillar cells control blood flow through the lamellae. In a process termed “osmorespiratory compromise” (Randall, 1982; Butler and Metcalfe, 1983), fish can vary the surface area of their gills to balance ionic- with oxygen exchange. The epithelial cell, interstitial space, and endothelial cell essentially constitute the water-blood barrier, a composite tissue space (Figs. 1 and 4D).
LUNGS: AIR BREATHING ORGANS Restriction of gas exchange to a specific site where the process could be well controlled, water loss reduced, the inhaled air cleared off harmful particles and physically adjusted, and protection from trauma afforded were requisite for aerial respiration and successful terrestrial habitation. Theoretically, if the human lungs were formed like the external gills, i.e., were evaginated organs freely exposed to air (Fig. 8B), even in a moderately desiccating environment, the water loss would be about 500 L.day⫺1 (McCutcheon, 1964), a value about 1,000 times greater than the routine water loss. Amidst the advantages conferred by invagination (Fig. 8E), the development of internalized gas exchangers was beset with certain major shortcomings. The most important one was that ‘dead-ended-organs’ could only be forcefully tidally ventilated through a narrow opening, at a significant energetic cost. Invaginated gas exchangers do not fully exploit the high ambient partial pressure of oxy-
38 THE ANATOMICAL RECORD (NEW ANAT.)
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Figure 11.
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Figure 12. Interactions between the respiratory media in different gas exchangers. The respiratory efficiencies are shown by the partial pressure of oxygen and partial pressure of carbon dioxide profiles in the inspired air (I), expired air (E), venous blood (V), and arterial blood (A). A: Co-current system—media flow in the same direction. B: Infinite pool design, e.g., of the skin—the gas exchanger is perfused but not ventilated. C: Counter-current arrangement. D: Uniform-pool design, e.g., of the mammalian lung. E: Cross-current design in the bird lung. Air and blood cross each other perpendicularly. F: The insect tracheal system— oxygen is delivered directly to the tissue. The partial pressure of oxygen in the arterial blood may exceed that in the expired respiratory medium only in models C and E. T, trachea; M, respiratory medium (air or water); p, parabronchus; c, cell; v, blood (venous); o, arterial blood; w, water; 3, directions of flow of respiratory media; a s partial pressure profiles of oxygen and carbon dioxide; ) tidally ventilated gas exchangers.
gen since the residual (dead space) air in the respiratory passages dilutes the inspired air. In a resting human being where the dead space air is about 140 cm3, about 28% of the 500 cm3 of the inhaled air doesn’t reach the gas exchange region.
TRACHEAL SYSTEM: THE MOST EFFICIENT GAS EXCHANGER The insect respiratory system is unique and in many ways astonishing both for its remarkable simplicity and exceptional functional efficiency. In insects, the circulatory and respira-
Figure 11. Respiratory system of insects. A: Air sacs of a grasshopper (Chrotogonous senegalensis): s, spiracular end; t, trachea. ⫻21. B: Air supply to the flight muscle of a locust (Locusta migratoria): t, trachea. ⫻750. C: Tracheolar air supply to cells in the gastrointestinal wall of a grasshopper: 3, trachea; E, presumptive intracytoplasmic tracheoles. ⫻6,700. D: Proximity to the mitochondria (m) of cells of the gastrointestinal wall of a locust: 3, cell walls of adjacent cells; t, trachea. ⫻35,000.
tory systems have been totally dissociated and the circulatory system relegated from any meaningful role in gas exchange. Oxygen is transported by the trachea (which are analogous to vertebrate blood capillaries) directly to the body tissues and probably to individual body cells (Figs. 8F, 11C,D, 12F). In highly metabolically active tissues, tracheoles indent the cells in the manner of a finger poked into a balloon (Weis-Fogh, 1967). The partial pressure of oxygen between the tracheoles and the tissue cells in insects is about 5.3 kPa compared with that of less than 0.3 kPa in the mammalian tissues. In the flight muscle of insects, the terminal tracheoles are never more than 0.2– 0.5 m away from a mitochondrion and the trachea can supply 10 times more oxygen per gram tissue than the blood capillary system (Bursell, 1970). With the spiracular valve serving as a carburetor, in mechanical terms, the trachea functions both as a compressor and an exhaust pipe. The limitation set by diffusion as a means of delivering oxygen has con-
signed the tracheates, the insects in particular, to very small body sizes. The average tracheolar length for optimal diffusion is 5–10 mm and the minimum diameter is 0.2 m (WeisFogh, 1967). Through synchronized action of the spiracles and the air sacs, organs that increase the tidal volume by as much as 70% of the total air capacity (Bursell, 1970), the trachea are ventilated unidirectionally and continuously. Such a ventilatory process reduces or totally eliminates dead space air at the gas exchange level, ensuring that the tissue cells are supplied with air at a near atmospheric partial pressure of oxygen. In much the same way as the degree of capillarization of tissues correlates with metabolic activity in vertebrates, in insects, tracheolar tissue density corresponds with the metabolic activities (Weis-Fogh, 1964).
LUNG-AIR SAC SYSTEM OF BIRDS: AN UNIQUE VERTEBRATE GAS EXCHANGER Among the air-breathing vertebrates, the lung-air sac system of birds is the most complicated and efficient gas exchanger (Scheid, 1979). The respiratory system is separated into the lung (the gas exchanging part) and the air sacs (the nonrespiratory part; Fig. 3A). Experimental injection of carbon monoxide into the air sacs after blocking the ostia (the connections between the lung and the air sacs) does not cause poisoning. Lacking a diaphragm, in birds, the lungs have been displaced to the roof of the coelomic cavity where they are closely attached to the ribs. The avian lungs are fairly quadrilateral in shape, compact, and inexpansile (Fig. 3A,B). Compared with nonflying mammals, birds have relatively small lungs (Fig. 14). Intercalated between the air sacs, the lungs (Fig. 3A) are largely continuously ventilated back-to-front by a concerted action of the cranial and caudal groups of air sacs. During breathing, the volume of the lungs varies by a mere 1.4% (Jones et al., 1985) and even squeezing them doesn’t cause significant collapse of the air capillaries (Macklem et al., 1979). Through a cross-current multicapillary serial arterialization arrangement between the parabronchial air and the pulmo-
Figure 13.
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fluid must be removed from the lung mainly through the lymphatics and the airways (by evaporation) soon after birth. Irrespective of the respiratory medium used and the habitat occupied, in all the evolved gas exchangers, oxygen acquisition occurs by simple passive diffusion. In view of these observations, an interesting question as whether air breathers can survive by breathing water or other liquids and water breathers endure by breathing air may be asked. How far apart have the gas exchangers adaptively diverged from the simple nonspecialized cell membrane of the early unicells? To what extent have the structural transformations of the aerial gas exchangers (lungs) separated from those of the water breathers (gills)? Figure 14. Relationship between the lung volume and body mass in birds, bats, and nonflying mammals. The volume of the lung in birds is smaller than that of the nonflying mammals. Bats have remarkably large lungs. The intense subdivision of the parabronchial gas exchange tissue into remarkably small terminal gas exchange units, the air capillaries, yields a large respiratory surface area in a smaller lung. The air capillaries of the avian lung are remarkably smaller than the alveoli of the mammalian lung. The data on the nonflying mammals are from Gehr et al. (1981), those of the bat from Maina et al. (1991), and birds from Maina et al. (1989).
nary venous blood (Fig. 12E), an auxiliary counter-current system between the air capillaries and the blood capillaries, a large tidal volume, continuous and unidirectional ventilation of the lung (e.g., Scheid, 1979), and exceptional morphometric parameters (Maina et al., 1989; Figs. 6 and 7), a greatly efficient gas exchanger has been contrived in birds. The similarity in the structure (i.e., presence of air sacs and rigid air conduits: air capillaries [birds] and tracheoles [insects]) and function (i.e., unidirectional and continuous air-flow in the trachea [insects] and the parabronchi [birds]) between the avian (Figs. 3A–D, 12E) and
Figure 13. Certain cells on the surface of some gas exchangers. A. Surface macrophages (*) on the lung of a tree-frog (Chiromantis petersi). ⫻3,033. B: The primary epithelium of fish gills showing the osmoregulatory chloride cells (F): 3, open and closed (E) chloride cells. ⫻1,100. C: A type II (granular) pneumocyte discharging surfactant (*) onto the alveolar surface of a bat (Miniopterus minor) lung.⫻133,333. D: A type II (granular) pneumocyte in a bat lung packed with osmiophilic lamellated bodies (3): r, red blood cell. ⫻9,300.
insectan (Figs. 8F, 11, 12F) respiratory systems is of great interest. For two groups of animals that were separated by some 150 million years of evolution, this is clearly a classic case of convergence in evolution of efficient gas exchangers.
CAN AIR BREATHERS BREATHE WATER AND CAN WATER BREATHERS BREATHE AIR? Fluid is not a foreign factor during the prenatal development of lungs. During fetal life, the lung is filled with liquid that flows into the developing air spaces in response to chloride ion secretion across the epithelium of the respiratory tract (Olver and Strang, 1974). In sheep, the rate of production may be as high 2 ml 䡠 kg⫺1 䡠 h⫺1 and at birth the total pulmonary fluid is as much as 30 ml 䡠 kg⫺1 (Normand et al., 1971). About 1 week before hatching, in the loggerhead turtle, Caretta caretta and during stage one of development of Salamandra salamandra the lungs are filled with fluid. To ensure that the inspired air reaches the blood-gas barrier, the intrapulmonary
It is pertinent to stress that it is not the nature of the respiratory media but rather the partial pressure gradient between two gas exchange media that determines the flux of oxygen across a tissue barrier. Due to their physicochemical differences (Dejours, 1988), water breathing presents formidable problems to an air breather and vice versa. Because of its higher viscosity, applying the same force, the flow rate of a liquid in the pulmonary passages should be slower than that of air. Moreover, to maintain equal flow rates, an air breather has to expend 60 times more energy to move liquid than air (Kylstra et al., 1966). Removal of the surfactant by the physical presence of a liquid on the respiratory surfaces reduces the driving pressure available for maximum expiratory flow of air in the lung to a value no greater than that generated by the elastic recoil of the lung tissue. This is only a small fraction of the total static recoil pressure available during air breathing
42 THE ANATOMICAL RECORD (NEW ANAT.)
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Figure 15. Caudal end of the tropical swamp worm (Alma emini) showing a respiratory groove (3). At the end of a breathing episode, the groove is closed by interlocking hooks (E) presumably entrapping some air in the cavity. The worm may continue extracting oxygen from the air on submergence. ⫻15.
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(Kylstra and Schoenfisch, 1972). Using an isotonic solution supercharged with oxygen to a pressure equivalent to that of air at sea level, mechanically ventilated dogs have been kept alive for days (Kylstra et al., 1966): the transfer of oxygen to the tissues during liquid breathing was more than adequate. When breathing liquid, death occurs from fatigue of the respiratory muscles and accumulation of carbon dioxide (Shaffer et al., 1976). It is pertinent to stress that it is not the nature of the respiratory media but rather the partial pressure gradient between two gas exchange media that determines the flux of oxygen across a tissue barrier. For this reason, the risk of losing oxygen from the blood through the gills when a fish moves into severely hypoxic waters is very real. Similarly, depending on the partial pressure of oxygen in water, bimodally breathing fish (Fig. 9A–D) can lose oxygen acquired through the air breathing organs across the gills. As regards the question of water breathers breathing air, adaptations such as stiffening and wider spacing of secondary lamellae, and presence of swellings that keep the lamellae physically apart thus reducing cohesion and collapse have developed. Land crabs and amphibious fish like mudskippers use gills in air. The tropical swamp worm (Alma emini) has evolved an extraordinary respiratory mechanism. Alma lives in hypoxic putrefying plant matter. It makes regular sojourns to the surface where it folds its caudal end into a groove forming a temporary ‘lung’ that it uses to breathe under water or in air (Maina et al., 1998; Fig. 15).
CONCLUSIONS Notwithstanding their different phylogenetic levels of development and hence their diverse morphological complexities, animals face fundamentally similar challenges for survival, including those for acquisition of oxygen. The foremost factors that have determined the construction and progression of the gas exchangers and adoption of distinctive respiratory stratagems include the habitat occupied, the respiratory medium utilized, and the lifestyle pursued. The aphorism “necessity is the mother of inven-
THE ANATOMICAL RECORD (NEW ANAT.) 43
tion” is as relevant in the development of novel biological states and processes as it is in the advancement of human activities. During their growth and advancement, theoretically an infinite number of fabrications and hence forms of respiratory organs could have resulted. Through a stiff cost-benefit analysis in cultivation for optimal solutions, however, only a limited number of designs have been crafted and preserved. Evaginated gas exchangers (gills) are the archetypal water breathing organs, while the invaginated ones (lungs) are the air breathing organs. In the bimodal breathers, animals that subsist at the air/water interface, combinations of these designs have developed. Regarding the presentation and exposure of blood to water or air, only countercurrent, cross-current, uniform, and
Terms such as “primitive,” “better,” “poor,” or “imperfect” have no proper place in comparative respiratory morphology—and I believe in comparative physiology. to a small extent (in amphibious animals) infinite pool designs have evolved. It would appear that optimal outcomes have obliged finite designs. The similarities in the design of the gas exchangers especially in phylogenetically remarkably different animals, e.g., the prevalence of a sheetflow plan supports the concept that in biology there are no rules but only necessities. Solutions are aggressively pursued within available resources and capacities. For example, while retaining the basic mammalian pulmonary morphology, by morphometrically refining their lungs (e.g., Maina et al., 1991; Figs. 6, 7, 14) and combining the structural parameters with exceptional physiological adaptations, e.g., high haemoglobin concentration, venous haematocrit, and oxygen affinity of blood (e.g., Jurgens et
al., 1991), bats achieved volancy, a very energetically expensive mode of locomotion. As depicted by insects, the extinct pterosaurs (of which the pulmonary morphology may never be known), and the bats (chronologically in that order), the design of the lungair sac system of birds is not a prerequisite to flight. The uncompromisingly high demands of oxygen for flight can and have been met through other novel pulmonary designs. Regarding the entire spectrum of the evolved gas exchangers, the human lung is lacking in many ways. Unfortunately, it has been used as the focal point in comparative pulmonary morphology and as a yardstick for comparing respiratory efficiency. The gas exchangers, especially in invertebrates, have been regarded to be “primitive” and hence deemed “less efficient.” It is poignant to underscore that gas exchangers have evolved only so far as to optimally meet prescribed needs: elegance has not been pursued for its own sake. Terms such as “primitive,” “better,” “poor,” or “imperfect” have no proper place in comparative respiratory morphology—and I believe in comparative physiology.
ACKNOWLEDGMENTS I am grateful to Professor (Emer.) A.S. King, Prof. G.M.O. Maloiy, and Dr. M.A. Abdalla, my foremost collaborators of over the years. Funding and fellowships to advance my research work have been kindly given by the British Council, The Royal Society, Fulbright Program, Leverhume Trust, Canadian International Development Agency (CIDA), National Scientific and Engineering Research Council of Canada (NSERC), University of Nairobi, and The University of the Witwatersrand.
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