ࡱ> Root Entry Fp1TableSQWordDocument$SummaryInformation(   !"#$%&'()*+,-./0123456789:;<=>?@ABCDEFGHIJKLMNOPQRSTUVWXYZ[\]^_`abcdefghijklmnopqrstuvwxyz{|}~ DocumentSummaryInformation8CompObjX0Table>Root Entry FV1TableSQWordDocument(SummaryInformation(   !"#$%&'()*+,-./0123456789:;<=>?@ABCDEFGHIJKLMNOPQRSTUVWXYZ[\]^_`abcdefghijklmnopqrstuvwxyz{|}~DocumentSummaryInformation8CompObjX0TableEU!respiratory membrane and a short diffusion distance (d) between the external medium and the blood. Flow rates of the medium across the respiratory membrane, and of blood through it, must be slow enough to juxtapose the medium and blood long enough for diffusion to occur. Flow rates must also be fast enough to maintain a difference in the concentration of gases in the medium and blood, that is, to maintain a diffusion gradient (Dp). Ventilation rates or the amount of respiratory membrane in use at any particular time, or both, should be adjustable so that gas exchange matches the needs of the animal as they vary with the animals level of activity. To provide more respiratory surface or ventilation than an animal needs during its greatest activity would be uneconomical. The quantity of gas in the water or air also affects the size of the membrane and its rate of ventilation. The density and viscosity of the medium affect the amount of energy required to move it across the respiratory membrane. The movement of other diffusible molecules, such as water, salts, and nitrogenous wastes, across the membrane may need to be reduced or enhanced. Body size is an important factor because of its effect on surfacevolume relationships. These considerations show that respiratory membranes and the methods of ventilating them differ greatly among vertebrates. The Respiratory System of Fishes A fishs respiratory system must be adapted to two major constraints of life in water. First, the amount of oxygen dissolved in water is much less than the concentration of oxygen in air. The quantity dissolved in water depends on the partial pressure of the oxygen in the air, which is about 160 mm Hg at sea level, because this is the force that drives oxygen into the water. The amount also depends on solubility, and oxygen is not very soluble in water. Although 207C air at sea level contains 210 mL/L of oxygen, fresh water under the same conditions contains only 6.6 mL oxygen/L. Salt water contains somewhat less, 5.3 mL/L. Solubility of oxygen increases slightly in cold water, so fresh water at 07C holds 10.3 mL/L. The second problem for a fish is that the water in which the oxygen is dissolved is much denser and more viscous than air. Because of these two constraints, a fish must have a rather large respiratory surface and move a large volume of water across it at considerable energetic expense. Any design features of the respiratory system that reduce these energetic costs would be to a fishs advantage. Unloading carbon dioxide is less of a problem because it is highly soluble in water. It does, however, combine with water to form carbonic acid (H2CO3). The pH of the medium may decrease, but most fishes live in sufficiently large bodies of near neutral water (pH 7) that this is of no consequence. Several other problems derive from the close proximity of blood and water across the respiratory membrane. Heat is quickly exchanged, so most fishes cannot maintain an overall body temperature different from the water in which they live (Focus 3-4). Water, valuable salts, and nitrogenous wastes also will diffuse through the membrane. Gills Urochordates and cephalochordates are sufficiently small and inactive animals for the body or the pharynx wall to serve as a respiratory membrane. A feeding and respiratory current of water flows through the mouth, into the pharynx, and out numerous pharyngeal slits; gills are not present. Ancestral craniates became larger and more active animals. Gills, which provide a large surface area for the respiratory membrane, evolved where a current of water could ventilate them. The larvae of many fish species have external gills, which are highly vascularized filamentous processes with large surface areas attached to the lateral surface of the head between certain gill slits. Adult fishes, on the other hand, have internal gills. These consist of a great many vascularized plates, the primary gill lamellae, attached to the walls of the gill or branchial pouches (Gr., branchia 5 gills) or to the gill arches. Minute and tightly packed secondary gill lamellae, where gas exchange occurs, attach perpendicularly and transversely to the primary lamellae (see Fig. 18-3). The Structure and Development of Internal Gills The pharyngeal pouches develop embryonically as lateral, endodermal evaginations from the portion of the archenteron that will become the pharynx (Fig. 18-1A). Ectodermal furrows push inward from the body surface to meet the endodermal pouches, and the intervening tissue soon breaks down. In most fishes, the epithelium covering the gills appears to be of ectodermal origin. The plates of tissue between successive pouches, to which the primary gill lamellae attach, are called interbranchial septa (Fig. 18-1B). A skeletal visceral arch lies in each interbranchial septum. The first visceral arch (the mandibular arch of gnatho-stomes) lies rostral to the first embryonic pouch, and the last one (the seventh visceral arch) lies caudal to the last pouch. Skeletal, supporting gill rays usually extend peripherally from the visceral arches into the interbranchial septa or primary gill lamellae. Muscles and nerves are associated with the skeletal elements, and each of the first six interbranchial septa of a jawed fish contains an embryonic artery, known as the aortic arch, that will supply the gills. Gill pouches were numerous in primitive craniates. Some extinct jawless fishes had 15 pairs. One recent species of hagfish has 14 pairs of pouches, but the lamprey has only 7 (Fig. 18-2B). Most chondrichthyan fishes and early bony fishes have six pairs of pouches, the first of which is reduced to a pair of spiracles (Figs. 18-1B and 18-2C). Teleosts have lost the spiracles and so have only five pairs of pouches (Fig. 18-2D). All the gill pouches are lined by gill lamellae in living lampreys and hagfishes, and we believe that this resembled the primitive ancestral craniate condition. The distribution of lamellae is more limited in jawed fishes. Interbranchial septa that bear gill lamellae on both surfaces constitute a complete gill, or holobranch. Jawed fishes usually have four of these. In addition, some sharks, some lungfishes, and some chondrosteans have a half-gill, or hemibranch, on the posterior surface of the hyoid septum (Fig. 18-1B). Gill lamellae seldom are present on the posterior surface of the last gill pouch, for no aortic arch exists here to supply them. The African lungfish, Protopterus, is an exception, for it has a hemibranch in this position that is supplied by a branch of the sixth aortic arch. Only a small, gill-like structure lies in the spiracle. Because it receives oxygenated blood from other gills (Chapter 19), it is called a pseudobranch (Fig. 18-1B). Its function in elasmobranchs is unclear. In teleosts, most of which have retained a pseudobranch even though they have lost the spiracle, it may function as a sense or salt-regulatory organ. Gills of Lampreys Internal gills are arranged in several different ways among fishes, and different patterns of ventilation exist. Jawless fishes have large, saccular branchial pouches that are lined with the primary gill lamellae (Fig. 18-2A and B). These are called pouched gills. Water normally is drawn into the pharynx through the mouth, enters the branchial pouches through pore-shaped internal gill slits, and leaves the pouches through pore-shaped external gill slits. One of the specializations of the lamprey for its sucking mode of feeding is a longitudinal division of the pharynx into a dorsal food passage, the esophagus, and a ventral, blind respiratory tube from which the internal gill slits arise (Fig. 17-2A). When the lamprey is feeding on another fish, water must be pumped in and out of the branchial pouches through the external gill slits. Gills of Elasmobranchs The branchial pouches of chondrichthyan fishes are narrow chambers, and the gill lamellae are borne on the interbranchial septa, which continue to the body surface (Figs. 18-1B and 18-2C). These are septal gills. A vertically elongated internal gill slit leads from the pharynx into each branchial chamber. Gill rakers at the bases of the interbranchial septa keep food in the pharynx. The structure of the gill rakers correlates with the type of food eaten. They are short processes in predacious sharks but form numerous, long, thin filaments in the plankton-feeding basking and whale sharks. Parabranchial chambers lie between the branchial chambers and the small, slit-shaped external gill slits. The distal tips of the interbranchial septa act as valves that can close the external gill slits. The embryonic aortic arches give rise to arteries that supply and drain the gills. Branches of afferent branchial arteries (L., ad 5 toward 1 ferent 5 carrying) carry blood low in oxygen content into all of the primary gill lamellae. Tributaries of pretrematic and posttrematic arteries collect aerated blood from the gills. The pretrematic and posttrematic arteries lead to an efferent branchial artery (L., ex 5 out 1 ferent 5 carrying), which carries blood to the dorsal aorta that distributes the blood to the body. Vascular beds where gas exchange occurs lie in the secondary lamellae between the afferent and the pretrematic and posttrematic arteries (Fig. 18-3A and B). Blood enters small vessels in the interbranchial septum from the afferent branchial artery and then flows through vascular spaces in the secondary lamellae. It is collected by small vessels and carried to the pretrematic and posttrematic arteries at the gill base. As it flows laterally from the internal to the external gill slits, most of the water passes between the secondary lamellae into septal channels beside the interbranchial septum from which it is discharged. Blood and water flow in opposite directions through and across the secondary lamellae (Fig. 18-3B). This countercurrent flow affords a considerably more efficient gas exchange than blood and water moving in the same direction, that is, concurrently (Fig. 18-4). In concurrent flow, oxygen would diffuse from the water and enter the blood until an equilibrium was reached. Because of the presence of hemoglobin that binds with oxygen, the blood would finally contain more oxygen than the water, but considerable oxygen would remain in the water. In countercurrent flow, well-aerated blood leaving the secondary lamellae encounters water that has not yet crossed the secondary lamellae and so contains more oxygen than the blood. The opposite conditions prevail at the septal-channel end of the secondary lamellae. There, water that has lost most of its oxygen is beside blood containing even less oxygen. Thus, a gradient for the diffusion of oxygen from the water to the blood exists along the entire length of the secondary lamellae, and most of the oxygen (8095%) in the water enters the blood. The pathway described is a respiratory pathway because it aerates the blood in the gills and delivers oxygen-rich blood to the tissues. In addition, elasmobranchs and most other fishes have a nonrespiratory pathway, in which some blood can be diverted away from the gill lamellae by directly entering the efferent part of the system or the venous drainage of the gills. This appears to be a mechanism whereby no more blood is aerated than necessary to meet the fishs current level of metabolism because blood passing through the gills in most fishes also may lose or gain water from the environment (Chapter 20). However, the role of the nonrespiratory system in elasmobranchs is less clear because their blood is iso-osmotic to seawater. During inspiration in sharks, the mouth and spiracles open and valves that close the gills shut. The pharynx expands by contractions of the coracomandibu-laris and rectus cervicis (sternohyoideus) muscles (Fig. 18-5A and B), which reduces the pressure within the pharynx relative to that in the surrounding water. Pressure is reduced even more in the parabranchial chambers by the outward bowing of the valves closing the external gill slits. The pharynx and parabranchial chambers act together as a suction pump, creating a pressure gradient that draws water into the pharynx through the mouth and spiracles, across the gills, and into the parabranchial chambers. During expiration (Fig. 18-5C and D), the mouth and spiracles close, the pharynx and branchial chambers are compressed by the adductor mandibulae and most of the branchial muscles, the external gill slits open, and water is driven out. The pharynx and branchial chambers act together as a force pump. Branchial muscles are most active during expiration, compressing the pharynx and branchial chambers. The visceral skeleton also is compressed, and considerable energy is stored in the bent cartilages. Expansion of the system during inspiration occurs partly by the elastic recoil of the visceral skeleton and partly by the contraction of somatic hypobranchial muscles that pull the pharynx floor ventrally. All of this activity minimizes energy consumption. The shark conserves still more energy by moving water fairly steadily in only one direction, rather than in and out external gill slits. The mass of the water need not be alternately accelerated and decelerated. Most sharks rely on an equal balance of the force and suction pumps in their respiratory cycle. Some fast-swimming sharks, and also some teleosts, open their mouths after reaching a certain speed and use the forward motion that is generated by their trunk and tail muscles to drive water across the gills. This is called ram ventilation. Sharks using ram ventilation have reduced or lost their spiracles. Skates and rays, which are bottom-dwelling fish with ventrally placed mouths, have exceptionally large spiracles through which most of the water enters the pharynx. Skates and rays ventilate their gills primarily by the suction pump, whereas the force pump plays only a minor role. Gills of Bony Fishes Bony fishes evolved a branchial apparatus that is somewhat different from that of elasmobranchs. A flap of body wall supported by bones, known as the operculum, extends from the hyoid arch region of the head laterally and caudally over the gills. There is a large, common opercular cavity for all the gills, and one valved, external gill slit, rather than a series of small parabranchial chambers, each with its own external gill slit (Figs. 18-2D and 18-6). The interbranchial septa are reduced, greatly so in teleosts, so the primary gill lamellae extend freely into the opercular cavity. The gills are described as aseptal. With the emergence of the opercular system, teleosts have a respiratory cycle that produces a continuous flow of water in one direction from the oropharynx to the opercular cavity over the gills. The cycle consists of two stages. The suction pump stage is activated by an expansion of the mouth cavity and pharynx by the sternohyoideus muscle and branchial levators (Fig. 18-6A and C). Because the volume of the oropharynx is increased, a pressure lower than the ambient surrounding pressure is created, and water flows into the mouth. At the same time, the opercular cavity is greatly enlarged by dilator muscles, which result in an even lower pressure, causing the water from the oropharynx to be drawn over the gills into the opercular cavity (Fig. 18-6B and C). In the second stage, the force pump is activated by the adductors and geniohyoideus muscles (Fig. 18-6D). The oropharynx is compressed, creating a positive pressure that is even more than the increasing pressure in the opercular cavity. As a result, water continues to flow from the oropharynx through the gills into the opercular cavity and thence to the outside through the opened opercular cavity. The efficiency of the teleostean respiratory system is based on the maintenance of a differential pressure between the oropharynx and opercular cavity, which are separated by a curtain of gills (Fig. 18-6B). It produces an uninterrupted unidirectional flow of respiratory water that runs in the opposite direction of the blood flow for an optimized countercurrent system. The structure of the enormous number of secondary lamellae provides a large surface area (A in the diffusion equation) and an exceptionally short diffusion distance (d in the diffusion equation) between water and blood. The surface epithelium on each side of a secondary lamella often is only one cell thick (Fig. 18-7A). Pillar cells bearing thin cytoplasmic flanges that spread out beneath them hold these epithelial layers apart. Blood flows in the narrow spaces among the pillar cells rather than through typical capillary beds. The total cross-sectional area of all the vascular channels within the secondary lamellae is considerably greater than the sum of the cross-sectional area of the branchial arteries supplying them. Similarly, the cross-sectional area of all the spaces for water passage between the large number of secondary lamellae is greater than the cross-sectional area of the pharynx. Because the velocity of a liquid moving from a narrow area into a larger area decreases, as does water flowing from a stream into a pond, the rate of blood flow through the lamellae and of water flow across them is reduced. Adequate time for diffusion is available. The combined surface area of the secondary lamellae varies greatly among phylogenetically unrelated species of teleosts and probably is adapted to their modes of life. Hughes (1984) calculated that a sluggish, bottom-dwelling toadfish has 151 mm2 of gill surface area per gram of body weight, compared with 1241 mm2/g for an active, pelagic menhaden. Diffusion distance across the gill lamellae is also less in active fishes, and the hemoglobin content of their blood is higher. Gas exchange across the gills is accompanied by the diffusion of other small molecules. Considerable ammonia in most fishes and urea in some teleosts are excreted through the gills. Chondrichthyan fishes are an exception because their gills are impervious to the diffusion of urea, and a large quantity of this molecule accumulates in their bodily fluids and tissues. Water and salts also are lost or gained through the gills, depending on their relative concentrations in the external environment and bodily fluids. Water, for example, is gained by osmosis through the gills of freshwater fishes but lost in most marine species, the environment of which is saltier than are their bodily fluids (Chapter 20). Because of the attendant osmotic problems, it is to a bony fishs advantage not to ventilate its gills, or perfuse blood through them, more rapidly than needed to meet its oxygen requirements at any particular time. Several mechanisms help match the rate of gas exchange with a fishs metabolic requirements: 1. Ventilation rate can be regulated. 2. The primary lamellae of adjacent gills can be brought together or moved farther apart (Fig. 18-7B and C). When adductor muscles within the gills are relaxed, the elasticity of the skeletal gill rays, assisted by the contraction of small abductor muscles, spreads the primary lamellae apart. The tips of adjacent gills meet, a damlike mechanism is formed, and most of the water passing across the gills must pass through the spaces between the secondary lamellae. When the adductor muscles contract, the tips of adjacent gills are pulled apart and much of the water leaves the branchial chambers without crossing the secondary lamellae. 3. The nonrespiratory pathway also can control the amount of blood perfusing the secondary lamellae. Vascular shunts divert some of the blood directly from afferent to efferent branchial arteries or into the venous drainage of the gills without going through the secondary lamellae. In many other species, the number of secondary lamellae being perfused is subject to control. Accessory Air Respiratory Organs The gills of bony fishes are such efficient respiratory organs that 80% to 95% of the limited oxygen available in the water is taken up by the blood. But in some situations, the gills alone cannot provide for a fishs needs. Oxygen levels can be very low in shallow, warm pools or in swamps where considerable decay occurs, and in other bodies of stagnant water. A fish could not live in these habitats without an accessory air respiratory organ that enables it to use the oxygen in the air. Gills are ineffective for this purpose because the delicate gill lamellae cannot be supported in air; they collapse and clump together, greatly reducing the respiratory surface. Many teleost fishes can supplement aquatic gill breathing with accessory air respiratory organs. These fishes mostly, but not exclusively, live in waters low in oxygen, and they become bimodal breathers, breathing both water and air in various proportions, depending on environmental conditions. Some teleosts even become obligate air breathers. Virtually all bimodal breathers retain gills and simultaneously evolve specialized air-breathing organs. Some use a vascular skin as a respiratory organ, such as freshwater eels, which often migrate over land. However, other bimodal breathers possess modifications of many parts of the gut: the linings of the mouth, pharynx, esophagus, intestine, and rectum. Mud or rice eels, which are eel-shaped, perchlike Synbranchiformes, have a highly vascularized mouth, pharynx, and esophagus as an air-breathing organ. They gulp air, which they hold for 30 minutes to 3 hours, taking up oxygen. These fishes exhibit amphibious life and can remain on land for up to six months. Gouramis, the climbing perch (Fig. 18-8A), the Siamese fighting fish, snakeheads, and the walking catfish, among others (Fig. 18-8B), develop a dorsal outpocketing above the gills to form a suprabranchial air chamber, which can be filled with air. One of the gill arches develops an elaborate, folded, highly vascularized structure called the labyrinth organ, or arborescent organ, which protrudes into the air chamber and functions as a lung, enabling the fish to live in oxygen-poor waters or even to spend considerable time on land. Some armored catfishes and loaches have parts of their intestines lined with folded epithelia, into which blood capillaries grow, transforming these intestinal segments into accessory air-breathing organs. When in oxygen-poor waters, these fishes supplement gill-breathing with air-breathing by swallowing air into their respiratory intestines and temporarily suspending digestive functions. Teleosts ventilate their suprabranchial air chambers by passing the spent air low in oxygen into the expanding buccal cavity. From here, it is expelled through an opened mouth at the surface of the water. Fresh, oxygen-rich air is sucked in, and the mouth closes when the buccal cavity is filled. Compression of the buccal cavity will force the fresh air into the chamber. Thus, the chamber is emptied by suction and filled by compression of the buccal cavity, which acts as a pump, specifically as a pulse pump, by alternating suction with compression. Similarly, an equivalent pulse pump ventilates air in the intestine. Lungs Lungs are but one of many aerial respiratory organs to have evolved in fishes. Many bony fishes have either lungs or swim bladders, except many bottom-dwelling species, in which they have been secondarily lost, so these organs are a common character of the group. The organ is most lunglike in the primitive members of the group, so lungs appear to have arisen early in evolution. Lungs may have evolved in certain placoderms and primitive bony fishes that were living in stagnant freshwater habitats subject to periodic droughts during the late Silurian and Devonian periods (Chapter 3). Geological evidence suggests that the earth at this time was subject to pronounced fluctuations in rainfall. Dry and wet periods alternated as they do in some tropical habitats today. During the hot, dry seasons, many bodies of fresh water would have become smaller, and water temperatures would have increased. Oxygen levels would have decreased. Some ponds probably became stagnant swamps or dried up completely. Chondrichthyan fishes and placoderms, many of which were marine, would not have been affected by these climatic fluctuations, but early freshwater bony fishes, including the rhipidistian ancestors of tetrapods, would have been unable to survive unless they had accessory air respiratory organs, such as lungs. Among actinopterygians with respiratory lungs are the gar (Lepisosteus), the bichirs and reed fish (Polypterus and Erpetoichthys, Focus 18-1), the bowfin (Amia), and the pirarucu (Arapaima). Actinopterygian fishes ventilate their lungs with a characteristic four-stroke buccal pump: The buccal cavity expands so that spent oxygen-poor air from the lung can pass into it. Once filled, it compresses to expel the spent air. The empty buccal cavity then expands again to take in fresh air and finally compresses to force the new air into the lungs. The bichirs and lungfishes have retained their lungs throughout their evolutionary history in their tropical freshwater environments (Fig. 18-9). Lungs develop embryonically in bichirs, lungfishes, and amphibians as a ventral evagination from the floor of the digestive tract (pharynx or, in some cases, esophagus) just caudal to the last pair of pharyngeal pouches. The primordia of the lungs resemble a pair of displaced pharyngeal pouches in some amphibian larvae, and this has led some investigators to suggest a homology between actinopterygian, lungfish, and amphibian lungs. This would imply that the lungs of tetrapods, commonly thought to be an adaptation for life on land, are in fact a primitive feature of all bony fishes and their descendants. In the bichir (Polypterus), the African lungfish (Protopterus), and amphibians, the bilobed lungs extend into the pleuroperitoneal cavity and grow ventrally, one on each side of the digestive tract (Fig. 18-9). In other lungfishes, the single lung primordium extends caudally and dorsally on one side of the digestive tract and may subsequently become bilobed. The vascular connections of the lungs of lungfishes and those of Polypterus and amphibians are similar. In lungfishes and primitive tetrapods, a slit-shaped opening, the glottis, on the floor of the pharynx or esophagus leads to the lungs. The lungs of lungfish, Polypterus, and indeed all vertebrates with lungs contain specialized cells that secrete a surface film of lipoprotein known as a surfactant. However, some variation in chemical composition of the surfactant has occurred throughout vertebrate evolution. As we shall see (p. 599), mammalian lungs are subdivided into many small chambers (alveoli) in which gas exchange occurs. The composition of their surfactant greatly reduces surface tension in the alveoli and hence the resistance to lung expansion. Less energy is needed to expand them. The lungs of fishes and early tetrapods have far less compartmentalization. The need to decrease surface tension is less. The composition of their surfactant is such that it acts more as an antiglue, preventing adhesion of adjacent epithelial surfaces at low lung volumes. This may have been the primitive function of a surfactant (Daniels et al., 1995). When breathing air, a lungfish comes to the surface and first begins to inhale fresh air. It does so by expanding its buccal cavity and sucking in fresh air (Fig. 18-10). During this process, the glottis opens and spent air is transferred from the lungs to the buccal cavity by elastic recoil of the pressurized lungs and contractions of smooth muscles that surround the lungs. As a result, the spent air mixes with the just inhaled fresh air in the buccal cavity. Excess mixed air escapes from the open mouth. The fish closes its mouth and compresses its buccal cavity, which acts as a force pump, driving the mixed air into the lungs. The glottis closes, and air is held in the lungs under pressure. Thus, the lungfishs ventilation pattern is typically a two-stroke pulse pump. It expands and compresses the buccal cavity only once during the respiratory cycle. Because mixed air is delivered to the lung, this pattern also is called the mixed-air buccal pump system. This mode of ventilation is characteristic of sarcopterygian fishes except coelacanths. High-speed X-ray cinematography and direct measurements of the gas mixture have verified this (Brainerd et al., 1993). Lungfishes hold air in the lung for a considerable time as the oxygen slowly is used. Breathing is not continuous. Long periods of breath holding, or apnea, alternate with short periods of lung ventilation. Some compartmentalization of the lung by internal septa provides a large surface area for gas exchange (Fig. 18-9). The Australian lungfish, Neoceratodus, uses its lung to supplement the gills in oxygen-poor water. It need not use them when oxygen supplies are normal. Internal lung septa are more numerous in Protopterus, which has lost its first two gills and is an obligate air breather. It will drown if prevented from reaching the surface to gulp air. The South American lungfish, Lepidosiren, is also an obligate air breather. Carbon dioxide accumulates in the lungs during the periods of apnea. The hemoglobin of lungfishes, like that of terrestrial vertebrates, must be adapted to bind with oxygen in the presence of more carbon dioxide than normally is present in water. Accumulated carbon dioxide is released during expiration, but the frequency of lung ventilation is too low to unload all the carbon dioxide. Most carbon dioxide continues to diffuse from the gills because it is very soluble in water. The Swim Bladder The lungs of primitive actinopterygian fishes have transformed into swim bladders in most neopterygian species and coelacanths. Neopterygian fishes live in oxygen-rich waters, and selection would favor the conversion of lungs into effective hydrostatic organs, which would endow these fishes with neutral buoyancy and therefore with highly efficient locomotory capacities. In a primitive actinopterygian, the swim bladder arises as a dorsal outgrowth from the caudal end of the esophagus and remains connected to the esophagus by a pneumatic duct (Fig. 18-9). The pneumatic duct remains in physostomous species (Gr., physa 5 bladder 1 stoma 5 mouth), but is lost in more advanced teleosts, known as physoclistous species (Gr., kleiein 5 to close). The swim bladder of primitive actinopterygians continues to be an important site for the uptake of oxygen, but it also has acquired a hydrostatic function. In a teleost, it is primarily a hydrostatic organ that can be regulated, enabling the fish to attain neutral buoyancy and so maintain its position in the water with minimal muscular effort. Neutral buoyancy requires that the density of the fish equal that of the water. Density equals mass or weight divided by volume. One milliliter of pure water weighs 1 g and so has a density of 1. But 1 mL of flesh weighs slightly more than 1 g. Because flesh alone has a density slightly greater than that of water, a fish without a swim bladder, such as many bottom-dwelling fishes and elasmobranchs, tends to sink. A sac of air in the fish decreases weight and can make its overall density equal to that of water. Problems arise, however, when a fish changes depth. When it goes deeper, water pressure increases, the swim bladder is compressed and becomes smaller, and the fishs density increases. The fish would sink faster except for the addition of enough gas to the swim bladder to maintain it at the appropriate size. When the fish rises, surrounding water pressure decreases, the swim bladder tends to expand, and gas must be removed from the bladder to maintain neutral buoyancy. The gas in the swim bladder of most species is about 80% oxygen, and it is secreted into the bladder by a gas gland on one surface of the organ (Fig. 18-11). Often, gas must be secreted against a considerable concentration gradient, for water pressure increases rapidly with depth. At a depth of 500 m, for example, the fish and the gases in its swim bladder are subjected to a pressure of 50 atm, and the partial pressure of oxygen in the swim bladder is 40 atm. The partial pressure, or tension, of oxygen in the water and in the fishs blood, however, is 0.2 atm. (Tension is the term applied to the partial pressure of a gas when in solution.) But a fish can secrete oxygen into the swim bladder against a pressure gradient and keep it there. Oxygen is kept in the bladder by a rete mirabile (L., rete 5 net 1 mirabile 5 wonderful), a set of relatively long, parallel capillaries located just before the gas gland (Fig. 18-11). Together, the rete mirabile and gas gland are called the red body. The tension of the oxygen in the venous capillaries just leaving the swim bladder is high because it is in equilibrium with the partial pressure of oxygen in the swim bladder. Oxygen starts to be carried off, but the venous capillaries are surrounded by arterial capillaries carrying blood with a lower oxygen tension in the opposite direction. A countercurrent exchange occurs: oxygen diffuses from the venous blood into the arterial blood and is carried back to the swim bladder. The rete mirabile acts as an oxygen gate, and the longer the capillaries in this organ, the less oxygen that escapes. Secretion of oxygen into the swim bladder requires a local increase in the acidity of the blood. As the blood becomes more acidic, hemoglobin releases bound oxygen. Acid has two sources. Carbon dioxide entering the blood combines with water to form carbonic acid. This reaction is accelerated greatly in the presence of the enzyme carbonic anhydrase in the red blood cells. In addition, considerable lactic acid is secreted by the gas gland. The release of oxygen by hemoglobin is a far faster reaction than its recombination, so considerable unbound oxygen accumulates in the blood in and near the gas gland, and the rete mirabile prevents most of it from escaping. Additional oxygen is continually being brought into the system by the arterial blood, and it, too, is released. Eventually, the tension of oxygen in the blood in the gas gland exceeds its partial pressure in the swim bladder, and oxygen diffuses into the swim bladder. The rete mirabile and gas gland together form a countercurrent multiplier system. Removal of oxygen from the swim bladder as a fish rises in the water is a far simpler process. Oxygen is released through the pneumatic duct in physostomes, but it is reabsorbed from a special, vascularized compartment of the swim bladder known as the oval in physoclists. A sphincter that normally separates the oval from the main part of the swim bladder relaxes; oxygen enters the oval and, because of its high partial pressure, rapidly diffuses into the blood. Oxygen does not diffuse back into the blood through other parts of the swim bladder because its wall contains a diffusion barrier of guanine plates. The swim bladder, with its energy-efficient regulatory capacity to maintain the size under different pressure regimes, is considered a biological marvel, a true evolutionary innovation that has enabled teleosts to penetrate and occupy countless aquatic habitats in the world. Although the swim bladder is primarily a hydrostatic organ, it has additional functions in certain species. It contains a store of oxygen that can be used in cellular respiration if needed. It is part of the hearing mechanism in most ostariophysan fishes because the bladder can act as a resonator and amplifier (Chapter 12). Drums and some other species can pluck on the swim-bladder wall with specialized muscles to produce sounds. Respiration in Early Tetrapods Because dry, 207C air at sea level contains 210 mL of oxygen per liter, adult terrestrial vertebrates have far more oxygen available to them than do fishes, but they need a moist respiratory membrane because the oxygen must be in solution to diffuse into the blood. Major problems for terrestrial vertebrates are how to expose and ventilate the respiratory membrane without an excessive loss of body water, and how to prevent collapse of the respiratory organ in air, which is less dense than is water. Lungs, which terrestrial vertebrates inherited from fishes, are well adapted to meet these problems. They usually contain internal septa or divisions of the airways that increase the surface area of the respiratory membrane and provide the needed support. Air within the lungs contains a great deal of water vapor; in mammals, it is normally saturated. The respiratory surface is kept moist without a great deal of water loss because the rate of ventilation is low, the air is conditioned by mucous glands in the airways prior to entering the lungs, and not all the air in the lungs is exchanged in each breathing cycle. The low rates of ventilation and exchange are made possible by the high oxygen content of the air in the lungs. Water vapor, which is a gas, reduces the partial pressure of oxygen in the lungs to about 100 mm Hg, compared with 160 mm Hg for dry air at sea level, but this is still ample. Amphibian Respiratory Organs The larvae of two of the three genera of contemporary lungfishes have external gills attached to the surface of their heads, and the larvae of rhipidistian ancestors of tetrapods probably had them, too. Amphibian larvae are aquatic and retain external gills. Fossil evidence indicates that the larvae of some early neotetrapods had external gills. Salamanders retain external gills throughout their larval period (Fig. 18-12), and neotenic species, such as the mudpuppy, Necturus, have them throughout life. The external gills of young frog tadpoles become covered by an opercular fold that opens on the body surface through a single pore called the spiracle (this term is unfortunate because the pore is neither homologous nor analogous to the spiracle of a fish). The operculum is extensive and even envelops the developing forelimbs. Older tadpoles lose the external gills as they develop deeper ones attached to the branchial arches. We are uncertain of whether these deeper gills are homologous to the internal gills of fishes. Lungs develop and begin to function late in larval life. Gills are lost at metamorphosis, the forelimbs push through the operculum, and the remains of the operculum fuse with the body wall. The frog respiratory system (Fig. 18-13) traditionally has been selected as a representative of adult amphibians even though new studies on salamanders have provided new functional and evolutionary perspectives. In frogs, valved, external nostrils lead to short nasal cavities that open through choanae at the front of the palate. Air passes through the buccopharyngeal cavity and enters the glottis, which is supported by small, lateral laryngeal cartilages derived from the sixth visceral arch. The glottis leads to a small, triangular laryngotracheal chamber, from which the lungs emerge. All these passages are lined by cilia and by mucous and serous secretory cells. These secretions keep air moist and trap dirt particles and carry them away from the lungs. The lungs of frogs are sac-shaped organs; in salamanders, they are elongated. The respiratory surface of frog lungs is increased by primary septa, and sometimes also by secondary ones, which form a series of pockets. The interior of the lungs is open. Ventilation of the lungs of a frog resembles that of lungfishes, except that air enters and leaves through the nares and nasal cavities rather than through the mouth opening (Fig. 18-14). In a representative breathing cycle, a lowering of the pharynx floor draws fresh air through the nasal cavities and into the buccopharyngeal cavity. The glottis then opens, and positive pressure in the lungs drives stale air out. Expiration is assisted by the elastic recoil of the lungs, and by the contraction of flank (hypaxial) muscles (DeJongh and Gans, 1969) and, specifically, the transversus abdominis, a newly evolved hypaxial muscle of tetrapods (Brainerd, 1999). The expired air is mainly expelled over the fresh air, which is sequestered to some degree in the floor of the buccopharyngeal cavity, but some mixing of air does occur. The nostrils are closed, the pharynx floor is raised, air is forced into the lungs, and the glottis closes. This pattern resembles the two-stroke cycle of lungfishes. The pumping action of the pharynx may be repeated until the lungs are well inflated. Modifications of this sequence have been described (Vitalis and Shelton, 1990). In addition to buccal-pump breathing for inhalation, salamanders use the transversus abdominis muscle to increase body-cavity pressure and force air out of the lungs. Thus, salamanders exhale actively by means of the transversus abdominis muscle while relying on the buccal pump to inhale. This pattern of inhalation by buccal pump and exhalation by the action of the transversus abdominis muscle is widespread among salamanders and also is found in frogs that have been studied. As in lungfish, amphibians can tolerate prolonged periods of apnea alternating with brief periods of ventilation. Because their metabolism and oxygen needs are low, a lung full of air can provide an amphibian with oxygen for many minutes. Because ventilation rates are low, eliminating carbon dioxide is more problematic than is obtaining oxygen. In addition to lungs, the thin, moist, vascular skin of most extant amphibians acts as a respiratory membrane. Considerable cutaneous gas exchange occurs in most extant species, but much variation exists. Some arboreal, tropical frogs that live in dry habitats have very little cutaneous gas exchange. On the other hand, one large family of salamanders (the plethodontids) have lost their lungs and depend exclusively on cutaneous gas exchange. Loss of lungs is an unexpected adaptation for a terrestrial vertebrate, and various scenarios have been proposed as to how this may have come about (Reagan and Verrell, 1991). Whatever the causes, reliance on cutaneous gas exchange restricts plethodontids to habitats where temperatures are cool and the oxygen supply is dependable. Some live on the bottom of cool mountain streams; others live beneath rocks and logs in damp woods. Plethodontids are also small animals with a surfacemass ratio favorable for gas exchange through the skin, and they are not very active. In species in which both the lungs and skin are used as respiratory membranes, the lungs are usually more important for oxygen uptake than carbon dioxide loss, and the skin is more important for carbon dioxide loss than oxygen uptake (Shoemaker et al., 1992). But the role of the lungs and skin varies with temperature and activity. As temperature rises and/or activity increases, the lungs assume a greater role in the exchange of both gases. Conversely, as temperature or activity decreases, the skin becomes more important. At very low temperatures, the lungs may not be used at all. Cutaneous gas exchange also exposes amphibians to considerable water loss. Amphibians mitigate this loss by living in wet or moist habitats where they can make up for the lost water, and, in some species (i.e., toads), by being most active during the early morning and evening, when humidity is high. As part of their reproductive behavior, frogs have evolved a method of vocalization. Vocal cords are located in the laryngotracheal chamber and can be vibrated by passing air across them. Although both sexes have vocal cords, only the males have resonating vocal sacs. These are evaginations from the floor or lateral walls of the pharynx that can be filled with air. The laryngotracheal chamber of males also is significantly larger than is that of females of comparable size in species in which this feature has been examined. It is the distinctive call of male frogs in the spring that attracts conspecific females. The Reptile Respiratory System Gas exchange in the embryos of reptiles, birds, and egg-laying mammals is through the allantois, a vascularized extraembryonic membrane that extends from the hindgut to unite with the chorion just beneath the eggshell (Chapter 4). The chorioallantoic membrane contributes to the placenta in placentals and a few marsupials. Neck length increases in reptiles, and the primitive laryngotracheal chamber becomes divided into a larynx (Gr., larynx 5 gullet) and trachea (Gr., tracheia 5 rough artery). The larynx wall is supported by a pair of arytenoid cartilages that flank the glottis and by a ring-shaped cricoid cartilage. These cartilages are derivatives from the lateral laryngeal cartilages of amphibians. Vocal cords are absent, but some reptiles can squeak, hiss, or bellow by rapidly expelling air. Cartilaginous rings, or partial rings, in the tracheal wall keep the trachea open for the free flow of air. The horny skin of most reptiles precludes effective cutaneous gas exchange, so the lungs of adults are the primary or only site for gas exchange. Certain aquatic turtles exchange some gases through their skin and also the buccopharyngeal cavity and cloaca, in and out of which they can pump water. Some species of turtles have accessory, vascular bladders that evaginate from the cloaca for this purpose (Fig. 17-8). Sphenodon retains amphibian-like lungs with only a slight increase in internal surface area, but most reptiles have lungs that are relatively more compartmentalized and larger than are those of amphibians (Fig. 18-15). A wide central bronchus (Gr., bronchos 5 windpipe) leads from the trachea into each lung, secondary bronchi branch from it, and alveolar sacs of varying size bud off them. Lung structure varies considerably among species. The anterior part of the lung is more compartmentalized in lizards and snakes than is the posterior part, which is frequently a simple sac with poorly vascularized walls. The posterior region appears to serve for air storage or acts as a bellows to help ventilate the rest of the lung. This region parallels the development of air sacs in birds. One lung usually is lost in amphisbaenians and long-bodied squamates, including snakes. As one would expect, large species have more compartmentalization of the lungs than do smaller ones. This maintains an adequate ratio between respiratory surface and body mass. Of particular significance is the reptilian method of ventilating the lungs. Reptiles use an aspiration pump. During inspiration, contraction of intercostal muscles simultaneously on both sides of the body enlarges the pleuroperitoneal cavity in which the lungs lie by abducting the ribs and expanding the ribcage, pressure within the pleuroperitoneal cavity decreases to below atmospheric pressure, the lungs expand, and air is sucked into them, hence the term aspiration pump. The glottis is closed, and air is held in the lungs until the next breathing cycle. Prolonged periods of apnea occur, as in lungfishes and amphibians. Expiration results from opposite rib movements and from the contraction of smooth muscle fibers in the lung wall. Aspiration by a suction-pump mechanism is more efficient than a gular (buccal) force pump because air can be transferred into the lungs in one movement. Thus, in general, reptiles breathe by aspiration breathing, but some lizards also use a gular (buccal) pump to assist lung ventilation, especially during or just after moderate to rapid locomotion. Lateral undulations that accompany locomotion appear to reduce the effectiveness of costal respiratory movements because intercostal muscles are being used to help bend the body from side to side. They contract first on one side and then on the other and not simultaneously as in costal respiration (Owerkowicz et al., 1999). The first aspiration pump in vertebrate evolution has been documented for a primitive actinopterygian fish, Polypterus (Focus 18-1), even though it evolved here as an analogous system that does not use a costal pump. Crocodilians evolved an unusual method of ventilation. Their lungs lie in separate pleural cavities anterior to the liver. The contraction of a unique diaphragmatic muscle, which extends from the liver to the pelvic girdle, pulls the liver caudad and enlarges the pleural cavities (Fig. 18-16), causing fresh air to be sucked into the lungs. (This muscle is not homologous to the mammalian diaphragm.) Expiration occurs by the contraction of abdominal flank muscles, which increases intra-abdominal pressure and pushes the liver forward. Thus, crocodilians ventilate their lungs with a hepatic piston pump in addition to the primitive costal aspiration pump. Because turtles are encased by a dorsal carapace and a ventral plastron, they cannot use ribs for aspiration pumping. At first it was believed that they can change the pressure in the lungs by in-and-out movements of their limbs, but recent studies have shown that these movements contribute insufficiently. Instead, they possess a transversus abdominis and a diaphragmaticus muscle to lift the ventral plastron toward the carapace. This decreases the volume of the body cavity, causing the lungs to exhale. Inhalation occurs when the obliquus abdominis muscle increases the body cavity volume. Respiration in Birds Because they are endothermic and flying animals, birds need an exceptionally efficient and compact respiratory system that will sustain a high level of metabolism and not add greatly to their weight. Bird lungs are relatively small organs that adhere to the dorsal wall of the pleural cavities and do not change appreciably in volume (Fig. 18-17A). The lungs themselves are only half the size of those of a mammal of comparable size, but they connect to a system of air sacs that pass among the viscera and even extend into many of the bones. Together, lungs and air sacs have a volume two to three times that of the lungs of a comparable mammal. The air-sac walls are not heavily vascularized, so they do not contribute to the gas-exchange surface. Rather, the air sacs, in combination with a unique pattern of airways within the lungs, make possible a unidirectional flow of air through the lungs. In other pulmonate vertebrates, in which the air moves in and out of the lungs through the same passages, a certain amount of stale air always mixes with inspired air. But in birds, the one-way flow carries relatively fresh air, with more oxygen and less carbon dioxide, across the respiratory surfaces during both inspiration and expiration. The morphology of the avian respiratory system is complex. A number of investigators have studied the system using various techniques, including inserting minute probes into the airways to determine the composition of the air within them and the direction of its flow. The numerous air sacs can be grouped functionally into an anterior and a posterior set (Fig. 18-17A). The trachea bifurcates into a pair of primary bronchi, each of which passes rather directly through the center of a lung in a mesobronchus, which connects with the posterior air sacs (Fig. 18-18A). Air in the posterior sacs returns to a lung through mediodorsal bronchi, which connect with thousands of small parabronchi. Innumerable short air capillaries bud off the parabronchi and branch and anastomose with adjacent air capillaries (Fig. 18-17B). The air capillaries are interwoven by dense vascular capillary beds, forming a respiratory labyrinth in which gas exchange occurs. Distances are short, and diffusion appears to keep the composition of the air in the air capillaries nearly in equilibrium with that flowing unidirectionally through the parabronchi. The parabronchi lead to medioventral bronchi, which in turn connect with the anterior air sacs and primary bronchus (Fig. 18-18B). The parabronchi are parallel to each other throughout the lung in early birds and in most of the lung in other species. This part of the lung is called the paleopulmo. A small neopulmo, in which the parabronchi form a network, also is incorporated into the lungs of many birds. The lungs are ventilated by rocking movements of the sternum, which alternately expand and compress the bellows-like air sacs. Hinges between the dorsal and the ventral parts of the ribs allow the sternum to move (Fig. 8-17A). The uncinate processes on the dorsal parts of the ribs act as lever arms on which certain respiratory muscles attach. Because flight muscles also cause movements of the sternum, clavicle, and ribs, ventilation and the flight movements are coupled and occur in synchrony (Jenkins et al., 1988). The glottis is held open most of the time because bird lungs are ventilated continuously, and no prolonged periods of apnea occur. Two inspirations and expirations are needed to move a unit of air through the system (Fig. 18-18). During the first inspiration, fresh air is drawn through the primary bronchus and mesobronchus into the posterior air sacs (Part A). This air moves through the mediodorsal bronchi and parabronchi during the first expiration (Part B). It is drawn into the anterior air sacs during the second inspiration (Part C) and finally is expelled from the system during the second expiration (Part D). Air, of course, enters and leaves the lungs and air sacs during each cycle of inspiration and expiration, but it is a different volume of air. During inspiration, one volume of air passes through the lungs to the posterior air sacs (Part A), and a volume of air inhaled previously is drawn out of the lungs into the anterior air sacs (Part C). During expiration, air in the posterior sacs (Part B) is driven into the lungs, and the stale air is expelled from the anterior air sacs through the main bronchi and trachea to the outside (Part D). Air flows through the system along the line of least resistance, and this is determined partly by the diameters and directions of the openings of the various bronchi and partly by aerodynamic valves (Focus 18-2). Blood in the vascular capillaries flows transversely to the air flow in the parabronchi and air capillaries in a pattern called cross-current flow (Fig. 18-19). As air flows from right to left in the model, it loses oxygen to the blood; blood flowing across the air gains oxygen. Because air and blood flow across each other, a gradient for the transfer of oxygen exists at each crossing of parabronchi and vascular capillaries, but the gradient is different at each intersection. The net result of this system, as in the countercurrent flow of blood and water in a fishs gills, is that the blood leaving the system has removed most of the oxygen from the air. In the lungs of other vertebrates, the oxygen content of the blood and air reach an equilibrium. The unidirectional flow of air through a birds lungs, the cross-current flow of air and blood, and the very large gas-exchange surface combine to produce an extraordinarily efficient respiratory system. Birds extract a greater proportion of oxygen from the air than do mammals, and they can live and fly at high altitudes where mammals cannot survive. Birds have also evolved a vocal apparatus that is associated with the airways. The calls and songs of birds are used in species recognition, for sounding alarms, in establishing territories, and in reproductive behavior. The vocal box is not the larynx, as in frogs and mammals, which is situated at the top of the trachea, but a syrinx (Gr., 5 panpipe) that is located at the bifurcation of the trachea into the main bronchi (Fig. 18-20A). Syrinx structure varies among species, but usually one or more tympanum-like membranes lie between cartilaginous rings in its wall, and they are vibrated by air moving across them. Air vibrations are transformed into meaningful sounds by changes in tension on these tympani, by the configuration of the trachea and buccopharyngeal cavity, and by tongue movements. Trumpeter swans and whooping cranes have exceedingly long tracheae, half or more of which loops within the sternal keel (Fig. 18-20B). This gives their calls their deep, resonating, and somewhat trombone-like quality. Respiration in Mammals The synapsid line of evolution culminating in mammals and the sauropsid line to reptiles and birds diverged millions of years ago, near the time of the origin of amniotes. Although mammals, too, evolved an efficient respiratory system, needed by endothermic animals, the mammalian system differs in many ways from that of birds because it evolved its complex design from the generalized amniote condition independently. The evolution of the secondary palate in mammals and their therapsid ancestors made possible a separation of food and respiratory passages (Chapter 7). The paired nasal cavities of mammals, which lie dorsal to the hard palate, are relatively larger than those of other vertebrates. Each contains three folds or scrolls of bones, known as the turbinates, or conchae, which greatly increase the surface area (Fig. 18-21). The mucous membrane that covers the turbinates and lines the other respiratory passages as they continue into the lungs is very vascular and ciliated and contains cells that produce mucous and serous secretions. Considerable conditioning of the air thus occurs as it passes across these surfaces to the lungs. The air is warmed and moistened, and dirt trapped in the mucus is carried by ciliary action to the throat to be swallowed or expectorated. The nasal cavities connect through the choanae with the nasopharynx, which is separated from the oropharynx by the soft palate. Food and air passages cross in the laryngopharynx, but food normally does not enter the respiratory passages because the larynx and hyoid apparatus are pulled forward against the base of the tongue during swallowing. A troughlike fold, the epiglottis, flips back over the glottis or deflects food around it into the esophagus. A newly evolved cartilage that appears to have no homologue in other species supports the epiglottis. Except when food is swallowed, the glottis, which is bounded laterally by the vocal cords, is held open because mammalian lungs are ventilated continuously. The mammalian larynx is more complex than that of other tetrapods (Fig. 7-26). It continues to be supported caudally by the ring-shaped cricoid cartilage, and the paired arytenoid cartilages, which also extend into the vocal cords, support its rostrodorsal wall. A new thyroid cartilage supports its lateroventral wall. The thyroid cartilage evolved from the fourth and fifth visceral arches as they became dissociated from the hyobranchial apparatus. The intrinsic muscles of the larynx that shape it and control the vocal cords are muscles of the fourth, fifth, and sixth visceral arches; as would be expected, they are innervated by a branch of the vagus nerve. Vibrations of air produced by the vocal cords are shaped by movements of the pharynx, soft palate, tongue, and lips. The trachea continues down the neck and gives rise within the thorax to primary bronchi, which enter the lobes of the lungs. The internal passages within mammalian lungs are more finely compartmentalized than are those of amphibians or reptiles, so a great increase in internal surface area has occurred (Figs. 18-15C and 18-22). Whereas a frog has about 20 cm2 of lung surface area per cubic centimeter of lung tissue, a human has 300 cm2 per cubic centimeter. The airways within the lungs branch and rebranch at least 20 times, forming a respiratory tree that terminates in bronchioles, alveolar sacs, and individual alveoli. The walls of the airways become progressively thinner along the course of the respiratory tree. Supporting cartilages, smooth muscle, and secretory and ciliated cells gradually disappear. The walls of the alveoli, through which gas exchange occurs, consist only of an exceedingly thin squamous epithelium that is nearly completely covered by vascular capillaries. Diffusion distance is about 0.2 mm. Only in birds is the distance shorter, on the order of 0.1 mm. The alveoli are tightly packed, and the capillaries lie between them. This arrangement allows for diffusion of gases to occur across two or more surfaces of the capillaries (Fig. 18-22C). A costal aspiration pump ventilates mammalian lungs. Air is moved in and out by changes in the size of the pleural cavities, alternately increasing and decreasing the pressure within the lungs relative to atmospheric pressure. Pleural cavity size is increased primarily by the contraction and caudal movement of the muscular diaphragm (Fig. 18-22A). During stronger inspiration, the external intercostal and other respiratory muscles pull the ribs rostrally and increase the dimensions of the thorax. Pressure within the lungs must be reduced enough during inspiration to overcome the frictional resistance of the numerous airways to the inflow of air and also to overcome the surface tension of the walls of the many thousands of alveoli. This surface tension tends to collapse the alveoli. The resistance of the airways is reduced by a pattern of branching that maximizes the diameters of the major airways, by cartilaginous supports in their walls, and by the secretion of surfactants (p. 585). Surfactants are particularly important in mammals because of the small size and large surface area of their alveoli. Expiration in quadrupeds is largely a passive process that depends on the elastic recoil of the lungs, ribs, and abdominal viscera, which are pushed caudally by the contraction of the diaphragm. Internal intercostal, abdominal, and other respiratory muscles become active during forced expiration. Although certain intercostal muscles become active during strong inspiration and expiration, the primary function of these muscles is to maintain the integrity of the chest wall so that the intercostal spaces do not bulge outward or cave in as pressure within the thorax changes. In mice, the ribs are used in lung ventilation when the animal is at rest, whereas the diaphragm becomes the major ventilatory component during activity. Evolution of Respiratory Patterns in Air-Breathing Vertebrates Traditionally, lung ventilation has been viewed as a clear dichotomy: fishes and amphibians breathe with a buccal pulse pump, whereas amniotes breathe with an aspiration pump generated by body muscles. There is no doubt that the primitive pattern of vertebrate air-breathing is the buccal pulse pump found in actinopterygian fishes. This primitive buccal pump pattern is characterized by four-stroke breathing; the buccal cavity expands during exhalation to draw spent air out of the lung or accessory air-breathing organ and then compresses fully to expel all of the exhaled gas (Fig. 18-23). The buccal cavity then expands a second time to take fresh air in and compresses to force fresh air into the lungs or other accessory air-breathing organs. In sarcopterygian fishes and salamanders the two-stroke breathing cycle evolved. Here, the buccal cavity expands to draw in fresh air, while spent air also flows in to mix with the fresh air. Some of this mixture is subsequently pumped into the lungs, and the rest exits by the mouth and gill slits. Brainerd (1999) has experimentally established that salamanders exhibit a primitive intermediate evolutionary step toward aspiration breathing (Fig. 18-23). In addition to the two-stroke buccal pump to inhale, salamanders exhale by using the transversus abdominis muscle. Amniotes employ full aspiration breathing, in which body muscles are used for not only exhalation but also inhalation. In all amniotes, except for turtles, intercostal muscles and ribs are recruited for inhalation by costal aspiration. The costal aspiration mechanism is primitive in amniote evolution. The patterns seen in turtles, crocodilians, and birds are evolutionary specializations. In mammals, a new structure, the diaphragm, is interposed between the pleural and peritoneal cavities. Contractions of the diaphragm assume the primary function in perfecting the mammalian aspiration pump. SUMMARY 1. Gases diffuse between the external medium (water or air) and the blood in the body through a respiratory membrane. Vertebrates require a means of ventilating this membrane by the bulk flow of the medium across it. 2. The respiratory system of a fish must be adapted to the limited supply of oxygen available in water and to the high density of this medium. Unloading carbon dioxide is not a problem for a fish because this gas is very soluble in water. Heat, salts, and water are also exchanged across the respiratory membrane. 3. Many larval fishes have external gills, but gas exchange in adults occurs through internal gills. 4. The gill pouches of fishes develop from endodermal pharyngeal pouches that meet ectodermal furrows extending inward from the body surface. The first pouch is reduced to a spiracle or has been lost. 5. A complete gill, or holobranch, bears primary gill lamellae on each surface. These support numerous secondary gill lamellae through which gas exchange occurs. A skeletal branchial arch, gill rays, vascular derivatives of an embryonic aortic arch, muscles, and nerves lie within the holobranch, often in an interbranchial septum. 6. The pouched gills of agnathans line spherical gill pouches. The pouches are numerous. 7. Elasmobranchs have septal gills borne on interbranchial septa and facing narrow branchial chambers. Each chamber opens into a parabranchial chamber and to the surface through an external gill slit. 8. A countercurrent flowwhereby water flows across the secondary lamellae in the opposite direction that blood flows through themincreases the efficiency of gas exchange. 9. The valvular action of the mouth and external gill slits allows the pharynx and parabranchial chambers, by their concurrent expansion and contraction, to act together first as a suction pump and then as a force pump in ventilating the gills. 10. Teleosts have aseptal gills, which extend into a common opercular cavity that opens to the surface through a single gill slit. The absence of septa increases the efficiency of the countercurrent exchanges of gases between blood and water. The pharynx and opercular cavity act alternately and in sequence as suction and force pumps. The combination of suction and force is described as a pulse pump. 11. The structure of the secondary lamellae provides a large surface area and a short diffusion distance between water and blood. 12. Because of the attendant osmotic problems, a fish does not ventilate its gills more than necessary to meet its oxygen needs. Various mechanisms regulate the amount of ventilation. 13. Lungs probably evolved in ancestral bony fishes as accessory respiratory organs that permitted them to live in unstable freshwater environments. 14. Lungfishes ventilate their lungs with a pulse pump. Some mixing of fresh and spent air occurs, and this mixed air is held in the lungs under positive pressure for a prolonged period of apnea. Some carbon dioxide accumulates in the lungs, but most is eliminated through the gills. 15. The lungs of the first bony fishes have transformed into hydrostatic swim bladders in most contemporary species. 16. Fishes attain neutral buoyancy by regulating the amount of air in the bladder. In most species, oxygen is secreted into the bladder by a gas gland and held in the bladder by a countercurrent rete mirabile. Oxygen can be reabsorbed through the oval. 17. Terrestrial vertebrates must avoid an excess loss of body water through their lungs. The large amount of oxygen in air and a low metabolic rate allow amphibians to avoid water loss by ventilating their lungs at a low rate. 18. Contemporary adult amphibians ventilate their lungs by a buccopharyngeal pump and retain air in the lungs under positive pressure for a prolonged period of apnea. Oxygen also is gained and carbon dioxide is eliminated by cutaneous respiration. 19. Plethodontid salamanders have lost their lungs and rely on cutaneous respiration for the exchange of gases. 20. Lung surface area is relatively larger in reptiles than in amphibians. Reptiles use rib movements and (in crocodiles) an unusual muscle that pulls the liver caudad to ventilate the lungs. Reptiles continue to have prolonged periods of apnea. Reptiles have a costal aspiratory pump. 21. Birds have small lungs that are connected to an extensive system of air sacs. Their lungs are ventilated continuously by rib and sternal movements and a bellows-like action of the air sacs. 22. The airways of birds are arranged in such a way that a unidirectional flow of air passes through numerous parabronchi and across air capillaries. Little stale air is retained in the lungs. A cross-current flow of blood over the parabronchi and of air within them thoroughly aerates the blood. 23. 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Respiration Physiology, 44:1164.#Chapter 18The Respiratory SystemThe Respiratory System of Fishes#Figure 18-1 A frontal section through the pharynx of an elasmobranch. An early developmental stage is shown in A; the adult condition, in B.#Chapter 18The Respiratory SystemFigure 18-2 Frontal sections through four fishes, showing the configuration and numbers of branchial pouches and the types of gills. A, Pouched gills of an osteotrachan. B, Pouched gill of a lamprey. C, Septal gills of a shark. D, Aseptal gills of a teleost.The Respiratory System of Fishes#Figure 18-3 A, A stereodiagram of portions of the gills of a dogfish. Water (arrows) flows between the secondary lamellae to septal channels located beside the interbranchial septum, whence it is discharged. Blood flow (not shown) is in the opposite direction through the secondary lamellae. B, Enlarged portion of primary and secondary gill lamellae with associated blood flow (black arrows) and water flow (blue arrows). (A, After Hughes.)#Chapter 18The Respiratory SystemFigure 18-4 Graphs showing the changes in oxygen content of blood and water during concurrent flow (left) and countercurrent flow (right).The Respiratory System of Fishes#Figure 18-5 The mechanics of gill ventilation in the dogfish as seen in lateral views (left) and frontal sections (right) of the pharynx. Relative pressures are indicated by 1 and 2. Narrow black arrows indicate the flow of water that entered the pharynx through the mouth; dashed black arrows, that of water that entered through the spiracle. Orange arrows indicate muscle activity, with the width expressing the relative level of activity. Wide black arrows depict movements of the hyoid. A and B show inspiration; C and D show expiration. (B and D, After Hughes.)#Chapter 18The Respiratory SystemFigure 18-6 The gills in a teleost. A, A lateral view of the opened opercular chamber. The black arrows indicate the movements of the hyoid. B, The countercurrent flow of water and blood in a gill. Blue arrows indicate the flow of water across the gills; black arrows indicate the flow of blood within the gills. C, Mechanics of inspiration. Blue arrows show the direction of water movement. D, Mechanics of inspiration. (B, After Dorit et al.)The Respiratory System of Fishes#Figure 18-7 Gill structure of a teleost. A, A transverse section through a secondary lamella, showing the close proximity of the vascular channels through which blood flows and the surface across which water flows. B, Primary gill lamellae of adjacent gills meet when adductors relax, so water must cross the secondary lamellae. C, Primary gill lamellae of adjacent gills separate when the adductor muscles constrict, and much water leaves the opercular chamber without crossing the secondary lamellae. (A, After Hughes; B and C, after Bijtel.)#Chapter 18The Respiratory SystemFigure 18-8 Air-breathing adaptations in teleosts. A, Climbing perch. B, Walking catfish.The Respiratory System of Fishes#Focus 18-1FocusThe First Aspiration Pump in the Evolution of Vertebrates Virtually all air-breathing fishes and amphibians ventilate their lungs by using a pulse pump. In pulse-pump systems, air forces the lung to expand, whereas in aspiration systems, air is sucked into the already expanding lung. Air-breathing fishes and amphibians begin to fill the lung only after the mouth is closed and the compressive muscles act on the buccal force pump. A remarkable exception is found in the polypterid fishes Polypterus (bichir) and Erpetoichthys (reedfish). The first appearance of lung ventilation by aspiration in the evolutionary history of vertebrates is exhibited by the pattern of ventilation in these primitive actinopterygians. Polypterid fishes are encased in a stiff scale jacket analogous to the dermal armor of early tetrapods (Fig. A, Part I). Cineradiographic analysis, pressure recordings, and strain-gauge recordings sensing deformations of the dermal armor by Brainerd et al. (1989) have elucidated an evolutionarily early aspiration pump. The fish exhales first by contraction of smooth muscles around the lung (Part II). Spent air is forced into the pharynx and exits from the opercular slit (Part III). The reduction in size of the lungs will cause a decrease in volume of the space occupied by organs within the peritoneal cavity, causing the ventral dermal armor to buckle inward (Part III). Such buckling is made possible by the nature of the peg and socket articulations between the thick scales. These articulations have the capacity to undergo recoil after the initial deformation. As the dermal armor passively recoils to its original resting position, it creates a subatmospheric pressure in the pleuroperitoneal cavity, causing the lung to expand (Parts IV and V). The resulting subatmospheric pressure in the expanding lung will draw air in through the widely opened mouth very rapidly. The use of recoil aspiration by polypterid fishes demonstrates that a stiff body wall capable of storing energy can contribute to inhalation in vertebrates. The ribs of polypterid fishes are confined to the dorsal part of the body and are not directly involved in the ventilation process even though they provide stiffness of the body, thus allowing for deformation of the belly. The discovery of recoil aspiration in polypterid fishes has important implications for our attempts to understand the ventilation mechanics of early Paleozoic amphibians. Early Paleozoic amphibians retained ventral, bony scales from their air-breathing fish ancestors. These V-shaped scale rows are very similar to the rhomboid scale body armor of polypterid fishes. The configuration of their ribs suggests that they confer stiffness on the body wall. The presence of recoil aspiration in polypterid fishes encased in a thick dermal scale jacket suggests that the ventral dermal armor of early amphibians may well have played an important role in aspiration breathing.A. A diagrammatic summary of the recoil aspiration model for polypterid ventilation. (After Brainerd et al.)The Respiratory System of Fishes#Figure 18-9 A cladogram showing the evolution of lungs and swim bladders.#Chapter 18The Respiratory SystemFigure 18-10 Ventilation of the lung by a buccal pulse pump in the South American (Lepidosiren) and African (Protopterus) lungfishes. Black arrows indicate air flow; orange arrows indicate muscle action. A, A lungfish at the surface opens its mouth and takes fresh air into its oropharyngeal cavity. B, The glottis opens, and spent air expelled from lungs mixes with fresh air. Excess air escapes through the mouth. C, The mouth closes, and mixed air is forced into the lungs. D, The glottis closes, and air is held in the lungs.Respiration in Early Tetrapods#Figure 18-11 The operation of the swim bladder in a physoclistous teleost. (Modified from Alexander.)#Chapter 18The Respiratory SystemFigure 18-12 The development of the external gills in the larva of a salamander. (After Glaesner.)Figure 18-13 A schematic dissection of the respiratory system of the frog. (After Dorit et al.)The Reptile Respiratory System#Figure 18-14 Lung ventilation in amphibians. AD, The exchange of air in a frog. Long arrows show air movements; short arrows, expansion and contraction of the lungs and buccal cavity; open arrows, the movements of the hyoid and floor of the buccopharyngeal cavity and pleuroperitoneal cavity. E, Drawings from videographs of a larval salamander showing closing and opening of the glottis. (AD, After DeJongh; E, after Brainerd.)#Chapter 18The Respiratory SystemFigure 18-15 AC, The degree of compartmentalization of the lungs of different tetrapods: A, an amphibian; B, a reptile; C, a mammal. D, The lung of a lizard, Ophiosaurus. (After Portmann.)Respiration in Birds#Figure 18-16 Ventilation of the lungs in a caiman. Small arrows within the body show contraction of different muscles; large arrows beneath the animal, the movements of the abdominal wall. (Modified from Gans and Clark.)Figure 18-17 The anatomy of the respiratory system of a bird. A, A lateral view of the lungs and major air sacs. B, A lateral view of a parabronchus and air capillaries. Arrows show the unidirectional flow of air across the respiratory surfaces. C, A small portion of the wall. (A, After Salt; B and C, modified from Smith et al.)Figure 18-18 The movement of a volume of air (shaded) through the lungs and air sacs of a bird. Two cycles of inspiration and expiration are needed to move a specific mass of air through the system. (After Bretz and Schmidt-Nielsen.)#Respiration in Birds#Focus 18-2FocusAerodynamic Valves in the Avian Lung In the absence of flaps or other mechanical valves in the avian airways, how the unidirectional flow of air is maintained has been a puzzle. The diameters of the openings into the various bronchi and air sacs, and the direction in which they face, certainly play an important role in determining the path of least resistance. But many investigators have postulated that aerodynamic valves, the operation of which depends on subtle factors, such as air pressure and composition, also operate. An inspiratory valve of this type has been found in geese by Wang et al. (1992). The caudal region of the primary bronchus has considerable circularly arranged smooth muscle in its wall. This section, which they call the accelerating segment, contracts during inspiration (Fig. A). As a consequence, air passing through it accelerates so that it bypasses the openings of the medioventral bronchi and continues into the mesobronchus and onto the posterior air sacs and mediodorsal bronchi. The stimulus for changes in dimensions of the accelerating segment appears to be changing carbon dioxide (CO2) levels. The smooth muscle fibers relax, and the segment dilates in the presence of increased level of CO2, which would occur during expiration. Whether an aerodynamic expiratory valve exists that would help air leaving the posterior air sacs to bypass the mesobronchus and enter the mediodorsal bronchi and parabronchi is unknown. Brown et al. (1995) believe that they may have found one in geese. They present evidence that the mesobronchus does narrow during expiration, which, of course, would help direct air into the mediodorsal bronchi. The mechanism for this is not entirely clear but appears to involve a dynamic compensation, in which a reduced air pressure in the mesobronchus during expiration of air from the anterior air sacs causes its wall to partially collapse. Valve efficacy was positively correlated with the rate of expiratory air flow. It was 95% efficient at flow rates assumed to occur during exercise, when dynamic compensation would be the greatest, and less efficient at lower flow rates.A. The principal airways in the lung of a goose, showing the contracting segment during inspiration. Its diameters during expiration are shown by the dashed lines. (Modified from Wang et al.)#Chapter 18The Respiratory SystemFigure 18-19 A comparison of the movement of blood and the external medium (water or air) across the respiratory surface of a fish, bird, and mammal. (After Piiper and Scheid.)Figure 18-20 Vocalization in birds. A, A frontal section through the syrinx of a male blackbird, Turdus merula. B, A lateral view of a dissection of the sternum and trachea of a whooping crane. (A, After Pettingill; B, after Portmann.)Respiration in Mammals#Figure 18-21 A sagittal section through a part of the head of a human showing the nasal and mouth cavity, pharynx, esophagus, and trachea.#Chapter 18The Respiratory SystemFigure 18-22 Diagrams of the mammalian respiratory system. A, An overview of the location and structure of the airways and lungs. B, An enlargement of the alveoli. C, The capillary bed that covers the alveoli. D, A drawing based on an electron micrograph of a portion of a mammalian lung. Notice that most of the capillaries have alveoli on two of their surfaces. (AC, After Dorit et al.; D, after Kessel and Kardon.)Evolution of Respiratory Patterns in Air-Breathing Vertebrates#Figure 18-23 A cladogram showing major stages in the evolution of lung ventilation. 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The oxygen that is needed, like the carbon dioxide produced as a by-product, enters and leaves the body by diffusion at a respiratory membrane. Water or air, which contains oxygen and carbon dioxide, must be moved across the respiratory membrane by a ventilation process. Many evolutionary changes occurred as vertebrates moved from water to land and eventually became endothermic animals. Outline The Respiratory System of Fishes Gills The Structure and Development of Internal Gills Gills of Lampreys Gills of Elasmobranchs Gills of Bony Fishes Accessory Air Respiratory Organs Lungs The Swim Bladder Respiration in Early Tetrapods Amphibian Respiratory Organs The Reptile Respiratory System Respiration in Birds Respiration in Mammals Evolution of Respiratory Patterns in Air-Breathing Vertebrates Focus 18-1 The First Aspiration Pump in the Evolution of Vertebrates Focus 18-2 Aerodynamic Valves in the Avian Lung Most of the bodys energy needs are supplied by the cellular oxidation of absorbed food products. In very small animals, the oxygen needed for this, and the carbon dioxide produced as a by-product, can be carried between the external environment and the cells by diffusion, but diffusion is a slow process, and it is efficient only for short distances. Diffusion plays a role in vertebrates in the movement of gases over short distances, but systems also are needed for the bulk flow, or movement by a muscular pump, of the medium containing the gases over longer distances. First, some sort of a pump must move the medium containing the gaseswater or airacross a thin, moist, and vascular membrane through which the gases can diffuse and be exchanged with those in the blood. A membrane of this type is called a respiratory membrane. Second, another pump, the heart, must move the blood through vessels that extend between the respiratory membrane and the vicinity of the cells, where diffusion of gases again takes place. We will consider the first set of problems, that is, the nature of the respiratory membrane and the bulk flow of the external medium across it, a process called ventilation, in this chapter. An efficient respiratory system optimizes the diffusion and exchange of gases between the body and the external environment, but many factors affect the nature of the respiratory membrane and the way it is ventilated. The rate of diffusion, R, follows the general equation for diffusion: R 5 D 3 A 3 (Dp/d) D is a diffusion constant, the value of which depends on the properties of the medium (density, temperature) through which diffusion takes place. A is the surface area across which diffusion is occurring (i.e., the respiratory membrane). Dp is the difference in partial pressures of the gas on either side of the respiratory membrane, and d is the distance (i.e., the thickness of the respiratory membrane) along which diffusion occurs. High diffusion rates require a large surface area (A) in the  "$&(#d  "$d "(  $bhjn"j"p""####B*CJ 5;B*CJ$ 56B*B*CJB* 5B*CJ 5;B*CJ$ A stereodiagram of portions interbranchial septum, whence      "$dfh $$d #d  showing closing and opening of mall arrows within hjln"""l"n"p"#####d   "#$%&'()*AAEB88-16BD-11D5-8953-0030653D7088} Oh+'0P    $08@H'18s8sHBCPofBCPNormalfHBCPlf11PMicrosoft Word 8.0d@ @Ϫ@Jxf4* of the sternum and trachea of (A, After Pettingill; $$$$#d c pjbjbSS (11h]"DT$T$T$T$\$tfQTz%z%z%z%z%z%z%z%M M M M M M M,SU>6Mz%z%z%z%z%6MvLz%z%@%:vLvLvLz%z%z%M&$z%MvLvLMM$%eҶf T$ErM18 The Respiratory System PRCIS The metabolic energy used by animals is derived from the cellular oxidation of food molecules. The oxygen that is needed, like the carbon dioxide produced as a by-product, enters and leaves the body by diffusion at a respiratory membrane. Water or air, which contains oxygen and carbon dioxide, must be moved across the respiratory membrane by a ventilation process. Many evolutionary changes occurred as vertebrates moved from water to land and eventually became endothermic animals. Outline The Respiratory System of Fishes Gills The Structure and Development of Internal Gills Gills of Lampreys Gills of Elasmobranchs Gills of Bony Fishes Accessory Air Respiratory Organs Lungs The Swim Bladder Respiration in Early Tetrapods Amphibian Respiratory Organs The Reptile Respiratory System Respiration in Birds Respiration in Mammals Evolution of Respiratory Patterns in Air-Breathing Vertebrates Focus 18-1 The First Aspiration Pump in the Evolution of Vertebrates Focus 18-2 Aerodynamic Valves in the Avian Lung Most of the bodys energy needs are supplied by the cellular oxidation of absorbed food products. In very small animals, the oxygen needed for this, and the carbon dioxide produced as a by-product, can be carried between the external environment and the cells by diffusion, but diffusion is a slow process, and it is efficient only for short distances. Diffusion plays a role in vertebrates in the movement of gases over short distances, but systems also are needed for the bulk flow, or movement by a muscular pump, of the medium containing the gases over longer distances. First, some sort of a pump must move the medium containing the gaseswater or airacross a thin, moist, and vascular membrane through which the gases can diffuse and be exchanged with those in the blood. A membrane of this type is called a respiratory membrane. Second, another pump, the heart, must move the blood through vessels that extend between the respiratory membrane and the vicinity of the cells, where diffusion of gases again takes place. We will consider the first set of problems, that is, the nature of the respiratory membrane and the bulk flow of the external medium across it, a process called ventilation, in this chapter. An efficient respiratory system optimizes the diffusion and exchange of gases between the body and the external environment, but many factors affect the nature of the respiratory membrane and the way it is ventilated. The rate of diffusion, R, follows the general equation for diffusion: R 5 D 3 A 3 (Dp/d) D is a diffusion constant, the value of which depends on the properties of the medium (density, temperature) through which diffusion takes place. A is the surface area across which diffusion is occurring (i.e., the respiratory membrane). Dp is the difference in partial pressures of the gas on either side of the respiratory membrane, and d is the distance (i.e., the thickness of the respiratory membrane) along which diffusion occurs. High diffusion rates require a large surface area (A) in the  "$&(#d  "$d "(  $bhjn"j"p""####$$L$z$~$$$$$B*CJ 5;B*CJ$ 56B*B*CJB* 5B*CJ 5;B*CJ- A stereodiagram of portions interbranchial septum, whence      "$dfh $$d #d  showing closing and opening of mall arrows within hjln"""l"n"p"####$$$$ $ $$z$|$~$$$$$ $$d #d  A lateral view of ross the respiratory surfaces. expiration are needed to move a specific mass of air through (After Bretz and