respiration

—respirational, adj.

/res'peuh ray"sheuhn/, n.

1. the act of respiring; inhalation and exhalation of air; breathing.

2. Biol.

a. the sum total of the physical and chemical processes in an organism by which oxygen is conveyed to tissues and cells, and the oxidation products, carbon dioxide and water, are given off.

b. an analogous chemical process, as in muscle cells or in anaerobic bacteria, occurring in the absence of oxygen.

[1400-50; late ME respiracioun < L respiration- (s. of respiratio) a breathing out, equiv. to respirat(us) (ptp. of respirare to RESPIRE) + -ion- -ION]

* * *

Process of taking in air for oxygen and releasing it to dispose of carbon dioxide.

The amount of air inhaled and exhaled in an average human breath (tidal volume) is about one-eighth the amount that can be inhaled after exhaling as much as possible (vital capacity). Nerve centres in the brain regulate the movements of muscles of respiration (diaphragm and chest wall muscles). Blood in the pulmonary circulation brings carbon dioxide from the tissues to be exhaled and takes up oxygen from the air in the pulmonary alveoli to carry it to the heart and the rest of the body. Because the body stores almost no oxygen, interruption of respiration

by asphyxiation, drowning, or chest muscle paralysis

for more than a few minutes can cause death. Disorders affecting respiration include allergy, asthma, bronchitis, emphysema, pneumonia, and tuberculosis. See also respiratory system; respiratory therapy.

* * *

▪ biology

Introduction

 the process by which animal organisms take up oxygen and discharge carbon dioxide in order to satisfy their energy requirements. In the living organism, energy is liberated, along with carbon dioxide, through the oxidation of molecules containing carbon. The term respiration also denotes the exchange of the respiratory gases (oxygen and carbon dioxide) between the organism and the medium in which it lives and between the cells of the body and the tissue fluid that bathes them.

      With the exception of energy used by animal life in the deep ocean, all energy used by animals is ultimately derived from the energy of sunlight. The carbon dioxide in the atmosphere in conjunction with the energy of sunlight is used by plants to synthesize sugars and other components. Animals consume plants or other organic material to obtain chemical compounds, which are then oxidized to sustain vital processes.

      This article considers the gaseous components of air and water, the natural respiratory habitats of animals, and the basic types of respiratory structures that facilitate gas exchange in these environments.

       Oxygen consumption of various animals and its variation with rest and activityAlthough the acquisition of oxygen and the elimination of carbon dioxide are essential requirements for all animals, the rate and amount of gaseous exchange vary according to the kind of animal and its state of activity. In the Table (Oxygen consumption of various animals and its variation with rest and activity) the oxygen consumption of various animals is expressed in terms of millilitres of oxygen per kilogram of body weight per hour, reflecting the gas demands of different species at rest and in motion. A change in the chemical composition of the body fluids elicits a response from the central nervous system, which then excites or depresses the machinery of external respiration.

The gases in the environment

      The range of respiratory problems faced by aquatic and terrestrial animals can be seen from the varying composition and physical characteristics of water and air. Air contains about 20 times the amount of oxygen found in air-saturated water. In order to extract an equivalent amount of oxygen as an air breather, an aquatic animal may find it necessary to pass across the respiratory surfaces a relatively larger volume of the external medium. Moreover, the diffusion rate of oxygen is much lower in water than in air. The problem is further compounded by the higher density (1,000 times air) and viscosity (100 times air) of water, which impose on the machinery of aquatic respiration a much greater work load. Thus, fish may expend about 20 percent of their total oxygen consumption in running the respiratory pump, as compared with about 1 to 2 percent in mammals, including humans.

      The carbon dioxide content of most natural waters is low compared with air, often almost nil. In contrast to oxygen, carbon dioxide is extremely soluble in water and diffuses rapidly. Most of the carbon dioxide entering water combines either with the water (to form carbonic acid) or with other substances (to form carbonates or bicarbonates). This buffering capacity maintains a low level of free carbon dioxide and facilitates the maintenance of a favourable diffusion gradient for carbon dioxide exchange by water breathers. In general, oxygen exchange, which is strongly dependent on the oxygen content of the water, is more critically limiting for aquatic forms than is the exchange of carbon dioxide.

       temperature exerts a profound effect on the solubility of gases in water. A change from 5° to 35° C (41° to 95° F) reduces the oxygen content of fresh water by nearly half. At the same time, a rise in body temperature produces an increase in oxygen consumption among animals that do not closely regulate their body temperatures (so-called cold-blooded animals). A fish experiencing both rising water and body temperatures is under a double handicap: more water must be pumped across its gill surfaces to extract the same amount of oxygen as was needed at the lower temperature; and the increased metabolism requires greater quantities of oxygen.

      The amount of oxygen available in natural waters is also limited by the amount of dissolved salts. This factor is a determinant of oxygen availability in transitional zones between sea and fresh water. Pure water, when equilibrated with oxygen at 0° C, for example, contains about 50 millilitres of oxygen per litre; under the same conditions, a solution containing 2.9 percent of sodium chloride contains only 40 millilitres of oxygen per litre. Bodies of water may have oxygen-poor zones. Such zones are especially evident in swamps and at the lower levels of deep lakes. Many animals are excluded from such zones; others have become remarkably adapted to living in them.

      The Earth's atmosphere extends to a height of many miles. It is composed of a mixture of gases held in an envelope around the globe by gravitational attraction. The atmosphere exerts a pressure proportional to the weight of a column of air above the surface of the Earth extending to the limit of the atmosphere: atmospheric pressure at sea level is on average sufficient to support a column of mercury 760 millimetres in height (abbreviated as 760 mm Hg—the latter being the chemical symbol for mercury). Dry air is composed chiefly of nitrogen and inert gases (79.02 percent), oxygen (20.94 percent), and carbon dioxide (0.03 percent), each contributing proportionately to the total pressure. These percentages are relatively constant to about 80.5 kilometres in altitude. At sea level and a barometric pressure of 760 millimetres of mercury, the partial pressure of nitrogen is 79.02 percent of 760 millimetres of mercury, or 600.55 millimetres of mercury; that of oxygen is 159.16 millimetres of mercury; and that of carbon dioxide is 0.20 millimetres of mercury.

      The existence of water vapour in a gas mixture reduces the partial pressures (pressure) of the other component gases but does not alter the total pressure of the mixture. The importance of water-vapour pressure to gas composition can be appreciated from the fact that at the body temperature of humans (37° C, or 98.6° F) the atmospheric air drawn into the lungs becomes saturated with water vapour. The water-vapour pressure at 37° C is 47 millimetres of mercury. To calculate the partial pressures of the respiratory gases, this value must be subtracted from the atmospheric pressure. For oxygen, 760 (the atmospheric pressure) - 47 = 713 millimetres of mercury, and 713 × 0.209 (the percentage of oxygen in the atmosphere) = 149 millimetres of mercury; this amounts to some 10 millimetres of mercury lower than the partial pressure of oxygen in dry air at 760 millimetres of mercury total pressure.

      Atmospheric pressures fall at higher altitudes, but the composition of the atmosphere remains unchanged. At 7,600 metres (25,000 feet) the atmospheric pressure is 282 millimetres of mercury and the partial pressure of oxygen is about 59 millimetres of mercury. Oxygen continues to constitute only 20.94 percent of the total gas present. The rarefaction of the air at high altitudes not only limits the availability of oxygen for the air breather, it also limits its availability for aquatic forms, since the amount of dissolved gas in water decreases in parallel with the decline in atmospheric pressure. Lake Titicaca (Titicaca, Lake) in Peru is at an altitude of about 3,810 metres; one litre of lake water at this altitude (and at 20° C, or 68° F) holds four millilitres of oxygen in solution; at sea level, it would hold 6.4.

      The variations in the characteristics of air and water suggest the many problems with which the respiratory systems of animals must cope in procuring enough oxygen to sustain life.

Basic types of respiratory structures

      Respiratory structures are tailored to the need for oxygen. Minute life-forms, such as protozoans, exchange oxygen and carbon dioxide across their entire surfaces. Multicellular organisms, in which diffusion distances are longer, generally resort to other strategies. Aquatic worms, for example, lengthen and flatten their bodies to refresh the external medium at their surfaces. Sessile sponges rely on the ebb and flow of ambient water. By contrast, the jellyfish, which can be quite large, has a low oxygen need because its content of organic matter is less than 1 percent and its metabolizing cells are located just beneath the surface, so that diffusing distances are small.

      Organisms too large to satisfy their oxygen needs from the environment by diffusion are equipped with special respiratory structures in the form of gills, lungs, specialized areas of the intestine or pharynx (in certain fishes), or tracheae (air tubes penetrating the body wall, as in insects).

      Respiratory structures typically have an attenuated shape and a semipermeable surface that is large in relation to the volume of the structure. Within them there is usually a circulation of body fluids ( blood through the lungs, for example). Two sorts of pumping mechanisms are frequently encountered: one to renew the external oxygen-containing medium, the other to ensure circulation of the body fluids through the respiratory structure. In air-breathing vertebrates, alternately contracting sets of muscles create the pressure differences needed to expand or deflate the lungs, while the heart pumps blood through the respiratory surfaces within the lungs. Oxygenated blood returning to the heart is then pumped through the vascular system to the various tissues where the oxygen is consumed.

Respiratory organs of invertebrates (invertebrate)

      Two common respiratory organs of invertebrates are trachea and gills. Diffusion lungs, as contrasted with ventilation lungs of vertebrates, are confined to small animals, such as pulmonate snails and scorpions.

trachea

      This respiratory organ is a hallmark of insects. It is made up of a system of branching tubes that deliver oxygen to, and remove carbon dioxide from, the tissues, thereby obviating the need for a circulatory system to transport the respiratory gases (although the circulatory system does serve other vital functions, such as the delivery of energy-containing molecules derived from food). The pores to the outside, called spiracles (spiracle), are typically paired structures, two in the thorax and eight in the abdomen. Periodic opening and closing of the spiracles prevents water loss by evaporation, a serious threat to insects that live in dry environments. Muscular pumping motions of the abdomen, especially in large animals, may promote ventilation of the tracheal system.

      Although tracheal systems are primarily designed for life in air, in some insects modifications enable the tracheae to serve for gas exchange under water. Of special interest are the insects that might be termed bubble breathers, which, as in the case of the water beetle Dytiscus, take on a gas supply in the form of an air bubble under their wing surfaces next to the spiracles before they submerge. Tracheal gas exchange continues after the beetle submerges and anchors beneath the surface. As oxygen is consumed from the bubble, the partial pressure of oxygen within the bubble falls below that in the water; consequently oxygen diffuses from the water into the bubble to replace that consumed. The carbon dioxide produced by the insect diffuses through the tracheal system into the bubble and thence into the water. The bubble thus behaves like a gill. There is one major limitation to this adaptation: As oxygen is removed from the bubble, the partial pressure of the nitrogen rises, and this gas then diffuses outward into the water. The consequence of outward nitrogen diffusion is that the bubble shrinks and its oxygen content must be replenished by another trip to the surface. A partial solution to the problem of bubble renewal has been found by small aquatic beetles of the family Elmidae (e.g., Elmis, Riolus), which capture bubbles containing oxygen produced by algae and incorporate this gas into the bubble gill. Several species of aquatic beetles also augment gas exchange by stirring the surrounding water with their posterior legs.

      An elegant solution to the problem of bubble exhaustion during submergence has been found by certain beetles that have a high density of cuticular hair over much of the surface of the abdomen and thorax. The hair pile is so dense that it resists wetting, and an air space forms below it, creating a plastron, or air shell, into which the tracheae open. As respiration proceeds, the outward diffusion of nitrogen and consequent shrinkage of the gas space are prevented by the surface tension—a condition manifested by properties that resemble those of an elastic skin under tension—between the closely packed hairs and the water. The plastron becomes “permanent” in the sense that further bubble trapping at the surface is no longer necessary, and the beetles may remain submerged indefinitely. Since the plastron hairs tend to resist deformation, the beetles can live at considerable depths without compression of the plastron gas.

      One extraordinary strategy used by the hemipteran insects Buenoa and Anisops is an internal oxygen store that enables them to lurk for minutes without resurfacing while awaiting food in relatively predator-free but oxygen-poor mid-water zones. The internal oxygen store is in the form of hemoglobin-filled cells that constitute the first line of oxygen delivery to actively metabolizing cells, sparing the small air mass in the tracheal system while the hemoglobin store is being depleted.

      The respiratory structures of spiders (spider) consist of peculiar “book lungs (book lung),” leaflike plates over which air circulates through slits on the abdomen. The book lungs contain blood vessels that bring the blood into close contact with the surface exposed to the air and where gas exchange between blood and air occurs. In addition to these structures, there may also be abdominal spiracles and a tracheal system like that of insects.

      Since spiders are air breathers, they are mostly restricted to terrestrial situations, although some of them regularly hunt aquatic creatures at stream or pond edges and may actually travel about on the surface film as easily as on land. The water spider Argyroneta aquatica, the frogman of the spider world, utilizes the water-beetle method of capturing air bubbles at the surface. The bubble is pressed against the respiratory openings on the abdomen, but, because there is no permanent plastron, trips must be made to the surface for bubble renewal. Most of the life cycle of the water spider, however, including courtship and breeding, prey capture and feeding, and the development of eggs and embryos, occurs below the water surface. Many of these activities take place in a kind of diving bell formed by silk. The spider weaves an inverted basketlike web that is anchored to underwater plants or other objects. Bubbles captured at the surface are ejected into the interior, inflating the underwater house with air. The combination of bubble trapping and web building has given Argyroneta aquatica access to an environment denied most of its relatives.

      Many immature insects have special adaptations for an aquatic existence. Thin-walled protrusions of the integument, containing tracheal networks, form a series of gills (gill) (tracheal gills) that bring water into close contact with the closed tracheal tubes. The nymphs (nymph) of mayflies and dragonflies have external tracheal gills attached to their abdominal segments, and certain of the gill plates may move in a way that sets up water currents over the exchange surfaces. Dragonfly nymphs possess a series of tracheal gills enclosed within the rectum. Periodic pumping of the rectal chamber serves to renew water flow over the gills. Removing the gills or plugging the rectum results in lower oxygen consumption. Considerable gas exchange also occurs across the general body surface in immature aquatic insects.

      The insect tracheal system has inherent limitations. Gases diffuse slowly in long narrow tubes, and effective gas transport can occur only if the tubes do not exceed a certain length. It is generally thought that this has imposed a size limit upon insects.

Gills of invertebrates

      Gills are evaginations of the body surface. Some open directly to the environment; others, as in fishes, are enclosed in a cavity. In contrast, lungs represent invaginations of the body surface. Many invertebrates use gills as a major means of gas exchange; a few, such as the pulmonate land snail, use lungs. Almost any thin-walled extension of the body surface that comes in contact with the environmental medium and across which gas exchange occurs can be viewed as a gill. Gills usually have a large surface area in relation to their mass; pumping devices are often employed to renew the external medium. Although gills are generally used for water breathing and lungs for air breathing, this association is not invariable, as exemplified by the water lungs of sea cucumbers.

      The marine polychaete worms use not only the general body surface for gas exchange but also a variety of gill-like structures: segmental flaplike parapodia (in Nereis) or elaborate branchial tufts (among the families Terebellidae and Sabellidae). The tufts, used to create both feeding and respiratory currents, offer a large surface area for gas exchange.

      In echinoderms (echinoderm) (starfish, sea urchins, brittle stars), most of the respiratory exchange occurs across tube feet (a series of suction-cup extensions used for locomotion). However, this exchange is supplemented by extensions of the coelomic, or body-fluid, cavity into thin-walled “gills” or dermal branchiae that bring the coelomic fluid into close contact with seawater. Sea cucumbers (sea cucumber) (Holothuroidea), soft-bodied, sausage-shaped echinoderms that carry on some respiration through their oral tentacles, which correspond to tube feet, also have an elaborate “respiratory tree” consisting of branched hollow outpouchings off the cloaca (hindgut). Water is pumped in and out of this system by the action of the muscular cloaca, and it is probable that a large fraction of the animals' respiratory gas is exchanged across this system.

      The gills of mollusks (mollusk) have a relatively elaborate blood supply, although respiration also occurs across the mantle, or general epidermis. Clams (clam) possess gills across which water circulates, impelled by the movements of millions of microscopic whips called cilia (cilium). In the few forms studied, the extraction of oxygen from the water has been found to be low, on the order of 2 to 10 percent. The currents produced by cilial movement, which constitute ventilation, are also utilized for bringing in and extracting food. At low tide or during a dry period, clams and mussels close their shells and thus prevent dehydration. Metabolism then shifts from oxygen-consuming (aerobic) pathways to oxygen-free (anaerobic) pathways, which causes acid products to accumulate; when normal conditions are restored, the animals increase their ventilation and oxygen extraction in order to rid themselves of the acid products. In snails (snail), the feeding mechanism is independent of the respiratory surface. A portion of the mantle cavity in the form of a gill or “lung” serves as a gas-exchange site. In air-breathing snails, the “lung” may be protected from drying out through contact with the air by having only a pore in the mantle as an opening to the outside. cephalopod mollusks, such as squid and octopus, actively ventilate a protected chamber lined with feathery gills that contain small blood vessels (capillaries); their gills are quite effective, extracting 60 to 80 percent of the oxygen passing through the chamber. In oxygen-poor water, the octopus may increase its ventilation 10-fold, indicating a more active control of respiration than appears to be present in other classes of mollusks.

      Many crustaceans (crustacean) (crabs, shrimps, crayfish) are very dependent on their gills. As a rule, the gill area is greater in fast-moving crabs (Portunids) than in sluggish bottom dwellers; decreases progressively from wholly aquatic, to intertidal, to land species; and is greater in young crabs than in older crabs. Often the gills are enclosed in protective chambers, and ventilation is provided by specialized appendages that create the respiratory current. As in cephalopod mollusks, oxygen utilization is relatively high—up to 70 percent of the oxygen is extracted from the water passing over the gills in the European crayfish Astacus. A decrease in the partial pressure of oxygen in the water elicits a marked increase in ventilation (the volume of water passing over the gills); at the same time, the rate of oxygen utilization declines somewhat. Although more oxygen is extracted per unit of time, the increased ventilation increases the oxygen cost of breathing. The increased oxygen cost, together with the decrease in extraction per unit of volume, probably limits aquatic forms of crustaceans to levels of oxidative metabolism lower than those found in many air-breathing forms. This is largely due to the lower relative content of oxygen in water and the higher oxidative cost of ventilating a dense and viscous medium compared with air. Not all crustaceans meet a reduction in oxygen with increased ventilation and metabolism. The square-backed crabs (Sesarma) become less active, reducing their oxidative metabolism until more favourable conditions prevail.

Respiratory organs of vertebrates (vertebrate)

      In most vertebrates the organs of external respiration are thin-walled structures well supplied with blood vessels (blood vessel). Such structures bring blood into close association with the external medium so that the exchange of gases takes place across relatively small distances. There are three major types of respiratory structures in the vertebrates: gills, integumentary exchange areas, and lungs. The gills are totally external in a few forms (as in Necturus, a neotenic salamander), but in most they are composed of filamentous leaflets protected by bony plates (as in fish). Some fishes and numerous amphibians also use the body integument, or skin, as a gas-exchange structure. Both gills and lungs are formed from outpouchings of the gut wall during embryogenesis. Such structures have the advantage of a protected internal location, but this requires some sort of pumping mechanism to move the external gas-containing medium in and out.

      The quantity of air or water passing through the lungs or gills each minute is known as the ventilation volume. The rate or depth of respiration may be altered to bring about adjustments in ventilation volume. The ventilation volume of humans at rest is approximately six litres per minute. This may increase to more than 100 litres per minute with increases in the rate of respiration and the quantity of air breathed in during each respiratory cycle (tidal volume). Certain portions of the airways (trachea, bronchi, bronchioles) do not participate in respiratory exchange, and the gas that fills these structures occupies an anatomical dead space of about 150 millilitres in volume. Of a tidal volume of 500 millilitres, only 350 millilitres ventilate the gas-exchange sites.

      The maximum capacity of human lungs is about six litres. During normal quiet respiration, a tidal volume of about 500 millilitres is inspired and expired during every respiratory cycle. The lungs are not collapsed at the close of expiration; a certain volume of gas remains within them. At the close of the expiratory act, a normal subject may, by additional effort, expel another 1,200 millilitres of gas. Even after the most forceful expiratory effort, however, there remains a residual volume of approximately 1,200 millilitres. By the same token, at the end of a normal inspiration, further effort may succeed in drawing into the lungs an additional 3,000 millilitres.

The gills

      The gills of fishes are supported by a series of gill arches (branchial arch) encased within a chamber formed by bony plates (the operculum). A pair of gill filaments projects from each arch; between the dorsal (upper) and ventral (lower) surfaces of the filaments, there is a series of secondary folds, the lamellae, where the gas exchange takes place. The blood vessels passing through the gill arches branch into the filaments and then into still smaller vessels (capillaries) in the lamellae. Deoxygenated blood from the heart flows in the lamellae in a direction counter to that of the water flow across the exchange surfaces. In a number of fishes the water-to-blood distance across which gases must diffuse is 0.0003 to 0.003 millimetre, or about the same distance as the air-to-blood pathway in the mammalian lung.

      The countercurrent flow of blood through the lamellae in relation to external water flow has much to do with the efficiency of gas exchange. Laboratory experiments in which the direction of water flow across fish gills was reversed showed that about 80 percent of the oxygen was extracted in the normal situation, while only 10 percent was extracted when water flow was reversed. The uptake of oxygen from water to blood is thus facilitated by countercurrent flow; in this way, greater efficiency of oxygen uptake is achieved by an anatomical arrangement that is free of energy expenditure by the organism. Countercurrent flow is a feature of elasmobranchs (sharks, skates) and cyclostomes (hagfishes (hagfish), lampreys) as well as bony fishes.

      A number of vertebrates use externalized gill structures. Some larval fishes have external gills that are lost with the appearance of the adult structures. A curious example of external gills is found in the male lungfish (Lepidosiren). At the time the male begins to care for the nest, a mass of vascular filaments (a system of blood vessels) develops as an outgrowth of the pelvic fins. The fish meets its own needs by refilling its lungs with air during periodic excursions to the water surface. When it returns to the nest, its pelvic-gill filaments are perfused with well-oxygenated blood, providing an oxygen supply for the eggs, which are more or less enveloped by the gill filaments.

      It is theoretically possible for a skin that is well supplied with blood vessels to serve as a major or even the only respiratory surface. This requires a thin, moist, and heavily vascularized skin, which increases the animal's vulnerability to enemies. In terrestrial animals a moist integument also provides a major avenue of water loss. A number of fishes and amphibians (amphibian) rely on the skin for much of their respiratory exchange; hibernating frogs utilize the skin for practically all their gas exchanges.

The lung

      The lungs of vertebrates range from simple saclike structures found in the Dipnoi (lungfishes) to the complexly subdivided organs of mammals and birds. An increasing subdivision of the airways and the development of greater surface area at the exchange surfaces appear to be the general evolutionary trend among the higher vertebrates.

      In the embryo, lungs develop as an outgrowth of the forward portion of the gut. The lung proper is connected to the outside through a series of tubes; the main tube, known as the trachea (windpipe), exits in the throat through a controllable orifice, the glottis. At the other end the trachea subdivides into secondary tubes (bronchi), in varying degree among different vertebrate groups.

      The trachea of amphibians is not divided into secondary tubes but ends abruptly at the lungs. The relatively simple lungs of frogs (frog) are subdivided by incomplete walls (septa), and between the larger septa are secondary septa that surround the air spaces where gas exchange occurs. The diameter of these air spaces (alveoli (pulmonary alveolus)) in lower vertebrates is larger than in mammals: The alveolus in the frog is about 10 times the diameter of the human alveolus. The smaller alveoli in mammals are associated with a greater surface for gas exchange: although the respiratory surface of the frog (Rana) is about 20 square centimetres per cubic centimetre (50.8 square inches per one cubic inch) of air, that of humans is about 300 square centimetres.

      An important characteristic of lungs is their elasticity. An elastic material is one that tends to return to its initial state after the removal of a deforming force. Elastic tissues behave like springs. As the lungs are inflated, there is an accompanying increase in the energy stored within the elastic tissues of the lungs, just as energy is stored in a stretched rubber band. The conversion of this stored, or potential, energy into kinetic, or active, energy during the deflation process supplies part of the force needed for the expulsion of gases. A portion of the energy put into expansion is thus recovered during deflation. The elastic properties of the lungs have been studied by inflating them with air or liquid and measuring the resulting pressures. Muscular (muscle) effort supplies the motive power for expanding the lungs, and this is translated into the pressure required to produce lung inflation. It must be great enough to overcome (1) the elasticity of the lung and its surface lining; (2) the frictional resistance of the lungs; (3) the elasticity of the thorax or thoraco-abdominal cavity; (4) frictional resistance in the body-wall structures; (5) resistance inherent in the contracting muscles; and (6) the airway resistance. The laboured breathing of the asthmatic (asthma) is an example of the added muscular effort necessary to achieve adequate lung inflation when airway resistance is high, owing to narrowing of the tubes of the airways.

      Studies of the pressure–volume relationship of lungs filled with salt solution or air have shown that the pressure required to inflate the lungs to a given volume is less when the lungs are filled with liquid than when they are filled with air. The differences in the two circumstances have been thought to result from the nature of the environment-alveolar interface, that interface being liquid–liquid in the fluid-filled lung and gas–liquid in the air-filled lung. In the case of the latter, the pressure–volume relationship represents the combined effects of the elastic properties of the lung wall plus the surface tension of the film, or surface coating, lining the lungs. Surface tension is the property, resulting from molecular forces, that exists in the surface film of all liquids and tends to contract the volume into a form with the least surface area; the particles in the surface are inwardly attracted, thus resulting in tension. Surface tension is nearly zero in the fluid-filled lung.

      The alveoli of the lungs are elastic bodies of nonuniform size. If their surfaces had a uniform surface tension, small alveoli would tend to collapse into large ones. The result in the lungs would be an unstable condition in which some alveoli would collapse and others would overexpand. This does not normally occur in the lung because of the properties of its surface coating (surfactant (surface-active agent)), a complex substance composed of lipid and protein. Surfactant causes the surface tension to change in a nonlinear way with changes in surface area. As a result, when the lungs fill with air, the surface tensions of the inflated alveoli are less than those of the relatively undistended alveoli. This results in a stabilization of alveoli of differing sizes and prevents the emptying of small alveoli into larger ones. It has been suggested that compression wrinkles of the surface coating and attractive forces between adjacent wrinkles inhibit expansion. Surfactants have been reported to be present in the lungs of birds, reptiles, and amphibians.

Dynamics of vertebrate respiratory mechanisms

Fishes

      Among the most primitive of present-day vertebrates are the cyclostomes (cyclostome) (lampreys and hagfishes), the gill structures of which are in the form of pouches that connect internally with the pharynx (throat) and open outward through slits, either by a fusion of the excurrent gill ducts into a single tube (in Myxine) or individually by separate gill slits (in Petromyzon). The gill lamellae of cyclostomes form a ring around the margins of the gill sac, and the series of sacs is supported in a flexible branchial skeleton. The number of paired pouches varies in different forms from six to 14. The pharynx of lampreys (lamprey) divides into an esophagus above and a blind tube below, from which the gill pouches arise. The upper pharynx of hagfishes communicates to the exterior through a nostril, a structure absent in lampreys. When the parasitic lampreys are embedded in the flesh of fish, upon which they live, they maintain a flow of water through the gills by alternate contractions of the gill pouches. When the gill-pouch muscles relax, the pouches expand, and water is sucked in. The water is forced out through the gills by muscular contraction; the branchial musculature apparently prevents reflux of the water into the pharynx while the head of the lamprey is embedded in the flesh of its prey.

      In the hagfish Myxine glutinosa, the major oxygen supply is derived from water drawn in through the nostril that opens into the pharynx. A peculiar respiratory structure, the velum, just behind the nostril opening, dangles from the upper midline of the pharynx, resembling an inverted T. Membranous scrolls attached to this horizontal bar can extend downward and then roll upward like window shades. A combination of velar and gill-pouch contractions directs the flow of water through the gill pouches. Foreign material entering the nostril is expelled from both the mouth and nostril by a violent “sneeze.” This reaction probably protects the respiratory surfaces, since the animals have common respiratory and alimentary ducts. Blood flow in the gills of cyclostomes, as in those of bony fishes (bony fish), is in a direction counter to that of water flow—an arrangement that increases the efficiency of gas exchange across the respiratory surface.

      Cartilaginous fishes (sharks (shark) and rays (ray)) and bony fishes employ a double-pumping mechanism to maintain a relatively constant flow of water over the gill exchange surfaces. In sharks and rays a small forward gill slit, the spiracle, also provides a channel for water flow into the gill chamber. Bottom-dwelling forms (e.g., skates) have relatively larger spiracles, and the major portion of the water flow passes through them rather than through the downward-oriented mouth.

      The pumping mechanism is not the only method of ventilation; sharks have been observed to keep both mouth and gill flaps open while swimming, ensuring a constant water flow across the gill surfaces. When they slow down or settle to the bottom, the pumping activity is resumed. Tunas (tuna) and mackerel cannot stop swimming: They have no active respiratory mechanism and are dependent for their gill ventilation on the current that results from their forward motion through the water.

      A number of fishes depend in varying degree on aerial respiration. The ability to breathe air enables them to live in places where the oxygen content of water may be low or nil. Two general means of acquiring oxygen are employed. Some fishes stay near the surface of the water, where the oxygen pressure resulting from surface diffusion is highest. Others have developed ancillary respiratory structures in the pharynx or the stomach; (stomach) the gulping of air at the surface is a means of charging these respiratory surfaces (such as the pharyngeal epithelium in Electrophorus or the stomach in Plecostomus). The frequency with which these fishes rise to the surface to gulp air corresponds to their current need for oxygen.

      The swamp-dwelling Erythrinus of Guyana uses both aquatic and aerial respiration, varying them according to the gaseous composition of the water. When the oxygen content is low, respiration through the gills ceases; when the oxygen content of the water is high, the fish relies primarily upon its gills except when the carbon dioxide content is also high—when, again, aerial respiration predominates. In other conditions it uses both modes of respiration. This apparently extends the range of conditions in which Erythrinus can survive.

      Eels (eel) (Anguilla) use their skin as a major respiratory surface in addition to their gills. In water, about 15 percent of their oxygen uptake is across the skin, and this rises to around 50 percent when in air. They are capable of making extensive overland migrations during which, in the first few hours, they draw upon oxygen in the swim bladder. Like most fishes, eels when out of water exhibit a reduced heart rate and less oxygen consumption. When they return to water, their heart rate rises, and both oxygen consumption and blood lactic-acid (lactic acid) levels rise. Lactic-acid production results from metabolism without oxygen, and such acid products must themselves be metabolized through higher oxygen consumption. Such patterns have been observed in grunions of the California coast that come ashore to breed, and even in flying fishes during their brief aerial excursions.

      The lungfishes (lungfish) (Dipnoi) are remnants of the Devonian period and a transitional form between water and air breathers. Like amphibians, they rely on the buccal (mouth) force pump mechanism to inflate the lung. They are adapted for bimodal respiration so that oxygenated blood leaving the air-exchange organ, either gills or lung, can pass to the afferent branchial circulation and then to the body tissues or can be dispatched to the lungs. The three dipnoan genera differ with respect to their reliance on the gills or lungs. In the Australian lungfish (Neoceratodus), the bulk of oxygen uptake and carbon dioxide elimination is by way of well-developed gills; in the African lungfish (Protopterus) and the South American lungfish (Lepidosiren), the gills are reduced and ventilation depends heavily on the lungs. In the latter two, which rely primarily on lung ventilation, separation of oxygenated and deoxygenated blood is much more complete than in the Australian lungfish.

      During long periods of drought, both Protopterus and Lepidosiren build a subterranean cocoon that opens to the surface via a thin tunnel. They then enter into a state of estivation in which metabolism, respiration, and heart rate fall to low levels. This state of diminished oxygen requirement enables the lungfish to remain viable without food or water for months or years, until the waters return.

      The bowfin, Amia calva, has both gills and an air bladder (swim bladder) that may be used for respiration. It is almost exclusively a water breather at 10° C (50° F), a temperature at which it shows low physical activity. Its air-breathing rate increases with temperature and activity, and, at around 30° C (86° F), it draws about three times as much oxygen from air as from water. As in lungfishes, carbon dioxide elimination is predominantly across the gills. The bowfin's air-breathing frequency varies inversely with the oxygen content of the water; when oxygen tensions in water decline below 40 or 50 millimetres of mercury at 20° C (68° F), air breathing largely replaces water breathing. When an exchange surface (gill or air bladder) is not being utilized as the primary oxygen-exchange site, there is a tendency for blood to bypass it.

      The so-called electric eel of South America (Electrophorus electricus (electric eel)) inhabits muddy streams that may become severely oxygen deficient. It is an obligatory air breather that depends upon the exchange of oxygen across the membranes of its mouth, expelling the air through its gill slits. Its blood has a high percentage of red corpuscles, is high in hemoglobin, and has an oxygen-absorbing capacity similar to that of mammals. Carbon dioxide elimination is primarily across the skin and, to a lesser extent, through the vestigial gills.

Fred N. White Alfred P. Fishman

Amphibians (amphibian)

      The living amphibians (frogs, toads, salamanders, and caecilians) depend on aquatic respiration to a degree that varies with species, stage of development, temperature, and season. With the exception of a few frog species that lay eggs on land, all amphibians begin life as completely aquatic larvae (larva). Respiratory gas exchange is conducted through the thin, gas-permeable skin and the gills. In addition to these structures, frog tadpoles use their large tail fins for respiration; the tail fins contain blood vessels and are important respiratory structures because of their large surface area. As amphibian larvae develop, the gills (and in frogs, the tail fin) degenerate, paired lungs (lung) develop, and the metamorphosing larvae begin making excursions to the water surface to take air breaths.

      The lungs of amphibians are simple saclike structures that internally lack the complex spongy appearance of the lungs of birds and mammals. The lungs of most amphibians receive a large proportion of the total blood flow from the heart. Even though the amphibian ventricle is undivided, there is surprisingly little mixture of blood from the left and right atrial chambers within the single ventricle. As a consequence, the lungs are perfused primarily with deoxygenated blood from the systemic tissues.

      By the time the larva has reached adult form, the lungs have assumed the respiratory function of the larval gills. A few species of salamanders (salamander) (for example, the axolotl) never metamorphose to the adult stage, and although they may develop lungs for air breathing, they retain external gills throughout life. Another exception to the usual pattern of respiratory development is seen in the Plethodontidae family of salamanders, which lose their gills upon metamorphosis but never develop lungs as adults; instead, gas exchange is conducted entirely across the skin. In almost all amphibian species, the skin in adults continues to play an important role in gas exchange.

      The relative contributions of lungs and skin, and even local areas of skin, to gas exchange differ in different species and in the same species may change seasonally. In frogs, the skin of the back and thighs (the areas exposed to air) contains a richer capillary network than the skin of the underparts and therefore contributes more to gas exchange. The aquatic newt Triton utilizes both lung and skin respiration, the skin containing about 75 percent of the respiratory capillaries. At the other extreme, the tree frog Hyla arborea is much less aquatic, and its lungs contain over 75 percent of the respiratory capillary surface area. Similar differences are found even in closely related forms: In the relatively more terrestrial frog Rana temporaria, uptake of oxygen across the lung is about three times greater than across the skin; in R. esculenta, which is more restricted to water, the lungs and skin function about equally in the uptake of oxygen. carbon dioxide is eliminated mainly through the skin in both these species; in fact, the skin appears to be a major avenue for carbon dioxide exchange in amphibians generally.

      In temperate climates, as winter approaches, the colder environmental temperature (and thus lower body temperature) induces a marked lowering of the metabolic (metabolism) rate in amphibians. Terrestrial forms (e.g., toads and some salamanders) may burrow into the ground to overwinter. Aquatic species burrow into the mud at the bottom of lakes or ponds. Because their metabolic rate is much lower during winter, adequate gas exchange can be provided entirely by the skin in either terrestrial or aquatic habitats.

      The mechanism of lung inflation in amphibians is the buccal cavity (mouth-throat) pumping mechanism that also functions in air-breathing fishes. To produce inspiration, the floor of the mouth is depressed, causing air to be drawn into the buccal cavity through the nostrils. The nostrils are then closed, and the floor of the mouth is elevated. This creates a positive pressure in the mouth cavity and drives air into the lungs through the open glottis. Expiration is produced by contraction of the muscles of the body wall and the elastic recoil of the lungs, both acting to drive gas out of the lungs through the open glottis. In aquatic amphibians the pressure of water on the body wall can also assist expiration. Many amphibians show rhythmic oscillations (wave motion) of the floor of the mouth between periods of lung inflation; these oscillations are thought to be involved in olfaction by producing a flow of gas over the olfactory epithelial surfaces.

Reptiles (reptile)

      To survive on land, the reptiles had to develop a skin relatively impermeable to water, so as to prevent dessication, and hence not well suited for respiration. Thus, while a few specialized reptiles (for example, sea snakes) can acquire nearly half of their oxygen supply through their skin, most reptiles depend almost entirely on the lungs for gas exchange. Reptilian lungs are considerably more complex than those of amphibians, showing much more internal partitioning to provide additional surface area for gas exchange between lung gas and blood. The most complex reptilian lungs are found in sea turtles such as Chelonia mydas, the green turtle. This species can develop a high metabolic rate associated with its prolific swimming ability. Its lungs are suited to providing a high rate of gas exchange, with extensive branching of the airways leading to the numerous gas sacs of the lungs.

      The mechanism for lung inflation in reptiles is an aspiration (suction) pump, which is the same in general principle as the lung inflation mechanism in birds and mammals. In most reptiles inspiration is produced by muscular expansion of the rib cage and body wall, creating a subatmospheric pressure within the lungs that causes air to flow in. Crocodiles and alligators have a specialized muscle attached to the posterior surface of the liver; the anterior surface of the liver in turn is attached to the posterior surface of the lungs. Contraction of this muscle pulls on the liver and results in expansion of the lungs.

      The adoption of a rigid shell by turtles (turtle) and tortoises (tortoise) necessitated the development of highly specialized skeletal muscles to inflate the lungs. In the tortoise Testudo graeca, lung ventilation is achieved by changing the volume of the body cavity. Expiration is brought about by the activity of muscles that draw the shoulder girdle back into the shell, compressing the abdominal viscera. The increased pressure in the body cavity is transmitted to the lungs. Inspiration involves opposite muscular actions that produce an increase in the volume of the body cavity and thus a subatmospheric lung pressure. Because of the rigidity of its shell, the tortoise, unlike other reptiles, cannot use the potential energy of abdominal wall structures to assist in respiration, and hence both expiration and inspiration are active energy-consuming events. In aquatic turtles, however, the pressure of water on the front and rear limbs assists expiration.

      The breathing patterns of most reptiles are not regular, usually consisting of a series of active inspirations and expirations followed by relatively long pauses. In aquatic reptiles diving occurs during these pauses, which may last an hour or more in some turtles and aquatic snakes. Even terrestrial reptiles show intermittent periods of breathing and breath holding. The metabolic rate of most reptiles is one-fifth to one-tenth that of birds (bird) or mammals, and constant lung ventilation is unnecessary in most reptiles.

Birds

      Birds must be capable of high rates of gas exchange because their oxygen consumption at rest is higher than that of all other vertebrates, including mammals, and it increases many times during flight. The gas volume of the bird lung is small compared with that of mammals, but the lung is connected to voluminous air sacs (air sac) by a series of tubes, making the total volume of the respiratory system about twice that of mammals of comparable size. The trachea divides into primary bronchi, each of which passes through a lung and onward to the paired abdominal air sacs; they also give rise to secondary bronchi supplying the other air sacs. Tertiary bronchi penetrate the lung mass and, from the walls of the tertiary bronchi, rather fine air capillaries arise. These air capillaries have a large surface area; their walls contain blood capillaries connected with the heart. Gas exchange takes place between the air capillaries and blood capillaries, making this surface analogous to the alveolar surface in mammals.

      There are several important differences in the mechanism and pattern of lung ventilation in birds compared with other vertebrates with lungs. The lungs of birds do not inflate and deflate but rather retain a constant volume. Also, the lungs are unidirectionally ventilated rather than having a tidal, bidirectional flow, as in other vertebrates with lungs. To achieve this unidirectional flow, the various air sacs are inflated and deflated in a complex sequence, like a series of interconnected bellows. The lungs, which are located midway between air sacs in terms of the flow of gas, are continuously ventilated in a single direction with freshly inspired air during both inspiration and expiration at the nostrils. Aspiration into the air sacs is produced by expansion of the chest and abdominal cavity. The sternum (breastbone) swings forward and downward, while the ribs and chest wall move laterally. Expiration is caused by compression of the air sacs by skeletal muscle.

      As a consequence of the continual, unidirectional airflow, the lungs of birds are more completely ventilated than the lungs of mammals. The flow of gas and blood within the bird lung is carefully arranged to maximize gas exchange, which is far more efficient than in the mammalian lung: Himalayan geese (goose) have been observed not only to fly over human climbers struggling to reach the top of Mount Everest, but to honk as they do so. The ventilation of pigeons (pigeon) increases around 20-fold during flight, brought about by more rapid breathing and not by taking in more air at a breath. There is a precise synchrony between breathing and wing motion: the peak of expiration occurs at the downstroke of the wingbeat. The pigeon's in-flight ventilation is about two and one-half times that needed to support metabolism; around 17 percent of the heat production during flight is lost through evaporative cooling, suggesting that the excess ventilation is for regulating body heat. Studies of evening grosbeaks and ring-billed gulls show that their ventilation, in contrast to that of pigeons, increases in proportion to oxygen consumption. The increased ventilation in these birds is brought about by deeper as well as by more rapid breathing.

      The respiratory system of birds is also used for communication through song (birdsong). The “voice box” is the syrinx, a membranous structure at the lower end of the trachea. Sound is produced only when air flows outward across the syrinx. In canaries, notes or pulses are synchronous with chest movements; the trills, however, are made with a series of shallow breaths. The song of many small birds is of long duration relative to their breathing frequencies.

Mammals (mammal)

      To provide the gas exchange necessary to support the elevated metabolic rate of mammals, mammalian lungs are subdivided internally. The repetitive subdivisions of the lung airways provide gas to the tiny alveoli (gas sacs) that form the functional gas-exchange surface area of the lungs. Human lungs have an estimated 300,000,000 alveoli, providing in an adult a total surface area approximately equivalent to a tennis court.

      Inspiration in mammals, as in reptiles, is powered by an aspiration (suction) pump. Expansion of the chest lowers the pressure between the lungs and the chest wall, as well as the pressure within the lungs. This causes atmospheric air to flow into the lungs. The chief muscles of inspiration are the diaphragm and the external intercostal muscles (intercostalis muscle). The diaphragm is a domelike sheet of muscle separating the abdominal and chest cavities that moves downward as it contracts. The downward motion enlarges the chest cavity and depresses the organs below. As the external intercostal muscles contract, the ribs rotate upward and laterally, increasing the chest circumference. During severe exercise other muscles may also be used. Inspiration ends with the closing of the glottis.

      In expiration, the glottis opens, and the inspiratory muscles relax; the stored energy of the chest wall and lungs generates the motive power for expiration. During exercise or when respiration is laboured, the internal intercostal muscles and the abdominal muscles are activated. The internal intercostals produce a depression of the rib cage and a decrease in chest circumference.

Fred N. White Warren W. Burggren

Additional Reading

General features of the respiratory process

August Krogh, The Comparative Physiology of Respiratory Mechanisms (1941, reissued 1968), is classic in its field. Julius H. Comroe, Jr., Physiology of Respiration: An Introductory Text, 2nd ed. (1974) covers the basic aspects of respiration in mammals. More recent texts include John Widdicombe and Andrew Davies, Respiratory Physiology (1983), a good introduction; Peter Sebel et al., Respiration: The Breath of Life (1985), an overview of respiration, the respiratory system, and its diseases; N. Balfour Slonim and Lyle H. Hamilton, Respiratory Physiology, 5th ed. (1987); and Allan H. Mines, Respiratory Physiology, 2nd ed. (1986). F. Harold McCutcheon, “Organ Systems in Adaptation: The Respiratory System,” in D.B. Dill (ed.), Handbook of Physiology, sect. 4, Adaptation to the Environment (1964), pp. 167–191, discusses respiration in relation to the environment, including chemical regulation, gas transport, and evolutionary patterns. Stephen C. Wood (ed.), Evolution of Respiratory Processes: A Comparative Approach (1979), compares respiratory processes in modern animals to gain insights into evolutionary changes. David J. Randall et al., The Evolution of Air Breathing in Vertebrates (1981), begins with the aquatic ancestral form.

Respiration in animals

Introductions to the field are provided by G.M. Hughes, Comparative Physiology of Vertebrate Respiration, 2nd ed. (1974); Rufus M.G. Wells, Invertebrate Respiration (1980), a short but useful study; F. Reed Hainsworth, Animal Physiology: Adaptations in Function (1981), which includes chapters on respiration, circulation, temperature, and energetics and their interplay; William S. Hoar, General and Comparative Physiology, 3rd ed. (1983), in which phylogeny in animal functions is used as a framework for depicting animal physiology; Martin E. Feder and Warren W. Burggren, “Skin Breathing in Vertebrates,” Scientific American, 253(5):126–142 (Nov. 1985); Knut Schmidt-Nielsen, Animal Physiology: Adaptation and Environment, 3rd ed. (1983), which explains systematically how animals cope with their environments; and a supplement to it, C. Richard Taylor, Kjell Johansen, and Liana Bolis (eds.), A Companion to “Animal Physiology” (1982), which probes certain topics, including respiratory physiology. See also V.B. Wigglesworth, The Principles of Insect Physiology, 7th ed. (1972, reprinted 1982), an excellent introduction to the form and function of insect respiration. C. Ladd Prosser, “Oxygen: Respiration and Metabolism,” ch. 5 in C. Ladd Prosser (ed.), Comparative Animal Physiology, 3rd ed. (1973), pp. 165–211, is a comprehensive chapter on oxygen and its role. Charlotte P. Mangum, “Oxygen Transport in Invertebrates,” The American Journal of Physiology: Regulatory, Integrative and Comparative Physiology, 248(5):R505–R514 (May 1985), provides a succinct overview of oxygen-carrying proteins.Alfred P. Fishman Fred N. White The principles of gas exchange in animals and humans are discussed in Malcolm S. Gordon, Animal Physiology: Principles and Adaptation, 4th ed. (1982), a consideration of the mechanisms of gas exchange among animals; “Gas Exchange and Circulation,” in R. McNeill Alexander (ed.), The Encyclopedia of Animal Biology (1987), pp. 50–65; and Handbook of Physiology, sect. 3, The Respiratory System, vol. 4, Gas Exchange, ed. by Leon E. Farhi and S. Marsh Tenney (1987), a critical, comprehensive presentation of physiological knowledge and concepts.Alfred P. Fishman Robert A. Klocke The interplay between respiration, circulation, and metabolism is outlined by Ewald R. Weibel, The Pathway for Oxygen: Structure and Function in the Mammalian Respiratory System (1984); R. Gilles (ed.), Circulation, Respiration, and Metabolism: Current Comparative Approaches (1985), essays on oxygen transport and utilization in animals; and C.R. Taylor et al., “Adaptive Variation in the Mammalian Respiratory System in Relation to Energetic Demand,” Respiration Physiology, 69(1):1–127 (July 1987), an entire issue devoted to the subject.Ewald R. Weibel

* * *