Lecture 6 Readings PDF

620 Chapter 23 BOX Mammals at High Altitude, 23.2 With Notes on High-Flying Birds (Continued ) alert to the possibility that some of the of newly arrived lowland- Mixed...

620 Chapter 23 BOX Mammals at High Altitude, 23.2 With Notes on High-Flying Birds (Continued ) alert to the possibility that some of the of newly arrived lowland- Mixed Ambient Alveolar Arterial venous responses seen at high altitude may be ers accelerates the flux of mm Hg air gas blood blood kPa misplaced responses! fresh air to their lungs and Let’s now look at some of the in- clearly helps them maintain 160 Sea level formation available on high-altitude a relatively high O2 partial 20 physiology. The figure depicts the oxygen pressure in their alveolar 140 cascades of native lowland Peruvians gas despite the fact that 120 living at sea level and of native Peruvian they are breathing rarefied 15 O2 partial pressure highlanders at 4500 m in the Andes. air. Nonetheless, based on 100 You’ll notice that despite the large the information available, 4500 m drop in ambient O2 partial pressure at hyperventilation gradu- 80 10 4500 m, the venous partial pressure of ally subsides if lowlanders the highlanders is reduced only a little. spend extended lengths 60 Comparing the two populations, the of time at altitude. Among venous O2 partial pressure is kept similar: native highlanders, Tibetans 40 5 It is conserved. To understand why this and Andeans differ strikingly. 20 occurs, physiologists study all the steps Tibetan highlanders exhibit in the oxygen cascade (see page 594). marked chronic hyperven- 0 0 From inspection of the figure, you can tilation; at a given O2 see that the conservation of venous O2 demand, their ventila- Oxygen cascades of people at sea level and high partial pressure in the Andean highland- tion rate is roughly twice altitude Two groups of native male Peruvians were stud- ers results from significant reductions in that of people residing ied at their altitudes of residence. (Data from Torrance et al. two of the partial pressure drops (steps) at sea level. For them, 1970.) of the oxygen cascade. The drop in hyperventilation is per- partial pressure between ambient air manent! Andean high- and alveolar gas is about 4.3 kPa (32 landers exhibit less of a hyperventilation tissue hypoxia are common, either as a mm Hg) at high altitude and therefore is response. Most species of nonhuman consequence of acclimatization or as a much smaller than the drop at sea level, mammals at high altitude display some result of adaptive evolution. 5.7 kPa (43 mm Hg); and the drop be- degree of hyperventilation. Genomic scientists are trying to iden- tween arterial blood and mixed venous Although processes such as hyper- tify genes that have been subject to blood is about 1.5 kPa (11 mm Hg) at ventilation (and others discussed in natural selection in native highland pop- high altitude, versus 7.3 kPa (55 mm Hg) Box 24.5) help keep O2 partial pres- ulations. These studies have recently hit at sea level. The arterial-to-venous drop sures in the systemic blood capillaries pay dirt in finding that genes in the HIF-2 is a topic in blood gas transport and is from falling excessively at high altitude, signaling pathway (see page 604) have discussed in Box 24.5. Here we exam- capillary O2 partial pressures do in fact been subject to strong positive natural ine lung function and systemic tissue decline. In the people at sea level in the selection in Tibetan highlanders during physiology. figure, blood enters the systemic capil- the approximately 20,000 years since One of the most important defenses laries at an arterial O2 partial pressure the Tibetan Plateau was colonized with that lowland people marshal at high al- of about 12.5 kPa (94 mm Hg) and exits permanent human settlements. These titude is hyperventilation, defined to be at a mixed venous O2 partial pressure of genes may prove to affect HIF-2 signal- an increase in the rate of lung ventilation about 5.2 kPa (39 mm Hg). In the people ing in ways that aid life at high altitude, associated with any given rate of O2 con- at 4500 m, blood enters at a much lower such as by controlling red blood cell sumption. When lowlanders first move to partial pressure, 5.9 kPa (44 mm Hg), and production in advantageous ways (see high altitude, a prompt (acute) increase exits at a modestly lower one, 4.4 kPa (33 Box 24.5). Box Extension 23.2 discusses in their rate of ventilation occurs; this mm Hg). Thus the O2 partial pressure in elevated pulmonary blood pressure in increase is probably activated princi- the capillaries—which drives O2 diffusion humans at high altitude, specific tissue- pally by the reduction in their arterial O2 to the mitochondria in cells—is, on aver- level adjustments, HIF involvement, and partial pressure, sensed by the carotid age, reduced at high altitude, a com- llamas as examples of native highland bodies. As lowlanders pass their first days mon circumstance in mammals. Great mammals. It also addresses high-flying Hill Animal Physiology 4E at high altitude, their rate of ventilation interest is focused at present on how the Sinauer Associates birds, especially the bar-headed goose becomes even higher, evidently because tissues of mammals accommodate Morales Studioto (see page 22). of an increasing physiological sensitivity FigureofBox this condition. Investigations 23.02 12-10-15 various of the breathing control mechanisms to species indicate that tissue-level adjust- hypoxic stimulation. The hyperventilation ments that offset the effects of chronic  External Respiration 621 ventilation is also modulated by conscious con- these variables simultaneously because the time needed for one trol, lung mechanosensors, and direct effects of breathing cycle tends to increase as the tidal volume increases. exercise The most obvious type of modulation of ventilation Nonetheless, during vigorous exercise, trained athletes are able to in humans is conscious control. We can temporarily stop breathing maintain a tidal volume of at least 3 L while breathing at least 30 by choosing to stop. There are, in addition, other types of control times per minute. In this way, their respiratory minute volume can besides the chemosensory ones. reach greater than 100 L/min—more than 15 times the resting value. One well-understood set of controls is based on mechanore- The alveolar ventilation rate, typically expressed as the ceptors in the lungs, which sense stretch or tension in the airways. alveolar minute volume, is defined to be the rate at which new air Information from these receptors is relayed via sensory neurons to is brought into the alveoli and other respiratory airways. This rate the brainstem, where signals for inhalation tend to be inhibited by is important because the air that reaches the respiratory airways is lung expansion and excited by lung compression. Certain of these the air that can undergo gas exchange with the blood. The alveolar mechanosensory responses are known as the Hering-Breuer reflexes. minute volume is calculated by subtracting the volume of the It is now well established that during exercise there are controls anatomical dead space, VD , from the tidal volume and multiplying operating in addition to chemosensory ones. Whereas these other by the breathing frequency: controls are important, they are not well understood. As already Alveolar minute volume = (VT – VD ) × f (23.3) stressed, the arterial partial pressures of O2 and CO2 remain little changed from resting values during light to moderate exercise. This Another property of importance relating to the respiratory airways stability results because of adjustments in the ventilation rate, which is the fraction of all inhaled air that reaches them. This fraction— is increased in tandem with the metabolic rate. However, arterial calculated by dividing the alveolar minute volume (Equation 23.3) gas partial pressures are far too stable during light to moderate by the total minute volume (Equation 23.2)—is (VT – VD)/VT. exercise to account for observed increases in ventilation on the basis From the expression just described, you can see that—with VD of the simple chemosensory negative feedback systems we have assumed to be constant—the fraction of air reaching the respiratory discussed up to here; for example, whereas an increase of about airways increases as the tidal volume increases. This fact helps 0.5 kPa (4 mm Hg) in the arterial CO2 partial pressure is required resolve a paradox. When the overall ventilation rate is increased, to bring about a doubling of ventilation rate, the measured CO2 the oxygen utilization coefficient increases. Although humans, for partial pressure during exercise may not be elevated to that extent example, use about 20% of the O2 in the air they breathe when their even when ventilation has reached 10–15 times the resting rate! In tidal volume is 500 mL, they use about 30% when their tidal volume addition to the controls mediated by gas partial pressures, there is is 2000 mL. How is this possible if, as we have often emphasized, increasing evidence for the existence of controls that are initiated in the control systems typically keep the alveolar O2 partial pressure direct association with the muscular movements of exercise. These constant? The paradox is resolved by recognizing two aspects controls are postulated to take two forms: First, parts of the brain of gas exchange. First, air that reaches the respiratory airways that initiate motor signals to the exercising muscles might simultane- always gives up about the same fraction of its O2 (accounting for ously initiate stimulatory signals to the breathing centers. Second, the constancy of alveolar O2 partial pressure). Second, however, a sensors of movement or pressure in the limbs might stimulate the greater proportion of all the air that is breathed actually enters the breathing centers based on the vigor of the limb activity they detect. respiratory airways as the tidal volume increases. One persuasive piece of evidence for these sorts of controls is that when people suddenly begin to exercise at a moderate level, their In species of different sizes, lung volume tends ventilation rate undergoes a marked increase within just one or two to be a constant proportion of body size, but breaths; this response is far too rapid to be mediated by changes breathing frequency varies allometrically in the chemical composition of the body fluids. Another piece of If we look at the full range of mammals, ranging in size from shrews evidence is that in many species of mammals, breathing movements to whales, there is a strong inverse (and allometric) relation between and limb movements are synchronized during running. breathing frequency and body size. Humans breathe about 12 times per minute at rest. A mouse breathes 100 times per minute! both tidal volume and breathing frequency are This dramatic effect is a logical consequence of several facts. First, modulated by control systems The overall rate of lung lung volume tends, on average, to be a relatively constant fraction ventilation depends on two properties: the tidal volume, VT , and the of total body volume: Lung volume in liters averages about 6% frequency of breaths, f, usually expressed as the number of breaths of body weight in kilograms. Second, resting tidal volume tends per minute. The product of these is the respiratory minute volume: consistently to be about one-tenth of lung volume or 0.6% of body weight. Third, related to these points, when mammals of all sizes Respiratory minute volume = VT × f  (23.2) are at rest, the amount of O2 they obtain per breath is approximately (mL/min) (mL/breath) (breaths/min) a constant proportion of their body weight. However, as emphasized To illustrate, resting humans have a tidal volume of about 500 mL in Chapter 7, the resting weight-specific rate at which mammals and breathe about 12 times per minute. Thus their respiratory metabolically consume O2 increases allometrically as body size minute volume is about 6 L/min. decreases. If the O2 demand per unit of body weight in a small Both tidal volume and breathing frequency are increased during mammal is greater than that in a large mammal, and yet the small exercise and during other states that increase the rate of metabolism. animal obtains about the same amount of O2 per breath per unit Humans and other mammals, however, cannot maximize both of of weight, then the small animal must breathe more frequently. 622 Chapter 23 Pulmonary surfactant keeps the alveoli to the origins of vertebrate air breathing. The roles of pulmonary from collapsing surfactants in animals other than mammals are incompletely known The alveoli may be thought of as aqueous bubbles because their but are gradually being better understood. gas-exchange surfaces are coated with an exceedingly thin water layer. If the alveoli were composed only of water, they would fol- Summary low the physical laws of simple aqueous bubbles. One such law is Breathing by Mammals that the tendency of a bubble to collapse shut increases as its ra- dius decreases.8 Thus, during exhalation, there is a risk that as the „„The lungs of mammals consist of dendritically radius of an alveolus decreases, the alveolus might collapse shut branching airways that end blindly in small, thin- walled, well-vascularized outpocketings, the alveoli. by emptying entirely into the airways of the lung. This possibility The airways exhibit 23 levels of branching in the may sound like a remote conjecture from a physics book. In fact, human adult lung, giving rise to 500 million alveoli. however, until this application of physics to biology was appreci- The airways in a mammalian lung are categorized as ated, thousands of human babies died every year because of bubble conducting airways, where little gas exchange with the physics, as we discuss soon. blood occurs, and respiratory airways, where most gas The alveoli in normal lungs do not behave as simple aqueous exchange with the blood takes place. bubbles because of the presence of a complex mixture of metabolically „„Because of the blind-ended structure of the mammalian produced lipids and proteins called pulmonary surfactant (surfactant, lung, the gas in the alveoli always has a substantially “surface active agent”). About 90% of pulmonary surfactant is lipids, lower O2 partial pressure and higher CO2 partial mostly phospholipids (amphipathic molecules, as seen in Chapter pressure than atmospheric air. 2). Pulmonary surfactant is synthesized by specialized pulmonary „„Contraction of the diaphragm is a principal force for epithelial cells, which secrete the lipoprotein complex as vesicles. inhalation in mammals, especially large quadrupeds. After secretion, phospholipids from the vesicles associate with the External intercostal muscles may contribute to inhalation; internal intercostal muscles and abdominal surface of the thin water layer that lines each alveolus, where they muscles may contribute to exhalation. Inhalation occurs radically alter the surface-tension properties of the water. Their overall by suction as the lungs are expanded by contraction of effect is to reduce the surface tension below that of pure water. This inspiratory muscles. At rest, exhalation occurs passively effect in itself helps prevent alveoli from collapsing shut because the by elastic rebound of the lungs to their relaxation tendency of bubbles to collapse decreases as their surface tension volume when the inspiratory muscles relax. decreases (explaining why soap bubbles linger longer than bubbles „„The breathing rhythm in mammals originates in a of pure water). The most profound effect of pulmonary surfactant, central pattern generator in the pre-Bötzinger complex however, is that it gives the alveoli a dynamically variable surface in the medulla of the brainstem. tension. With surfactant present, as an alveolus enlarges, its surface „„The most potent chemosensory stimulus for increased tension increases, an effect that impedes further enlargement and ventilation in mammals is a rise in blood CO2 partial helps prevent the alveolus from expanding without limit. Conversely, pressure and/or H+ concentration, sensed in the as an alveolus decreases in size, its surface tension decreases, helping medulla. The blood O2 partial pressure, ordinarily a less to prevent any further decrease in size. Surfactant, therefore, helps influential factor in controlling ventilation, is sensed keep all alveoli similar in size. by the carotid bodies along the carotid arteries (humans) or by carotid and aortic bodies (certain other Infants born prematurely sometimes lack adequate amounts of mammals). The control of ventilation during exercise pulmonary surfactant. Their alveoli therefore lack the protections involves stimuli generated in association with limb of surfactant, and many alveoli collapse shut during each exhala- movement as well as chemosensory controls. tion. An affected infant then must inhale with sufficient force to „„Pulmonary surfactant, a mix of lipids and proteins that reopen the alveoli. The process is tiring and damages the alveoli. affects surface tension, makes a critical contribution to Death rates were very high until therapies based on knowledge of maintaining the proper microscopic conformation of pulmonary surfactant were introduced. the lungs in all air-breathing vertebrates. The use of knockout mice and other genomic methods is leading to rapid advances in understanding of the surfactant proteins. One of them, protein B, is now known to be essential for life, evidently Breathing by Birds because it plays indispensable roles in controlling the distribution The lungs of birds, although they are logical derivatives of the of surfactant lipids. types of lungs thought to exist in the common ancestors of birds Pulmonary surfactants that share basic chemical similarities have and mammals, differ in fundamental structural features from the been reported from the lungs of all groups of terrestrial vertebrates, lungs of mammals and all other modern vertebrates except certain lungfish, and some other air-breathing fish. Thus the pulmonary crocodilian reptiles. The structural difference between avian and surfactants have a long evolutionary history, dating back at least mammalian lungs inevitably invites comparison. Are avian lungs 8 This is an implication of Laplace’s Law, which—applied to bubbles— functionally superior to mammalian lungs? Some authorities states that ΔP = 2T/r, where r is the radius of a bubble, ΔP is the pressure conclude that the designs of the lungs in birds and mammals are difference between the inside and outside of the bubble, and T is the “different but equal”—that is, equal in their gas-exchange ability. tension in the walls of the bubble. If everything is considered constant except ΔP and r, the pressure difference required to keep a bubble open is Other authorities conclude that the lungs of birds are in fact superior seen to increase as the radius r decreases. organs of gas exchange. As evidence, they point to the fact that bird  (A) Anatomy Anterior secondary Parabronchi Posterior secondary External Respiration 623 bronchi bronchi Figure 23.24 Airflow in the lungs and air sacs of Anterior birds (A) Basic anatomy of the avian lung and its connec- air sacs tions with the air sacs. In this presentation, the anterior and posterior groups of secondary bronchi are each represent- Posterior ed as a single passageway. The tubes labeled parabronchi air sacs are those of the dominant paleopulmonal system. (B, C) Primary bronchus Mesobronchus Airflow during (B) inhalation (when the air sacs undergo Neopulmonal expansion) and (C) exhalation (when the air sacs undergo parabronchi compression). Air flows through (B) Inhalation the parabronchi from posterior to The anterior air anterior. sacs expand and fill with gas that The posterior air sacs has passed across expand and fill with the respiratory fresh air coming exchange directly from the surfaces. environment. (C) Exhalation As during inhalation, air flows through the The anterior parabronchi from air sacs are posterior to anterior. compressed, discharging stale gas stored in them. The posterior air sacs are compressed. The fresh air in them is directed primarily into the posterior The gas that is exhaled has passed Outflow to the environment secondary bronchi. across the respiratory exchange along the length of the surfaces even if temporarily held in mesobronchus is minimal, KEY the anterior air sacs. according to available evidence. Fresh air Stale gas (i.e., depleted in O2, enriched in CO2) lungs have relatively large surface areas for gas exchange and thin they are formally termed the medioventral and mediodorsal groups, gas-exchange membranes (see Figure 23.8). They also point to the respectively. Also for simplicity, each group is represented as just a fact that some birds, such as certain geese, cranes, and vultures, single passageway in Figure 23.24A. can fly—not just mope around and survive—near or above the The anterior and posterior secondary bronchi are connected altitude of Mt. Everest. The design of the bird lung, in comparison by a great many small tubes, 0.5–2.0 mm in internal diameter, with the mammalian lung, may be an advantage at high altitude, termed tertiary bronchi or parabronchi (four are shown in Fig- in part because (as we will see) cross-current gas exchange pre- ure 23.24A). As depicted in Figure 23.25, the central lumen of vails in the bird lung instead of tidal exchange. High-flying birds each parabronchus gives off radially along its length an immense are discussed in Box 23.2. number of finely branching air capillaries. The air capillaries A bird’s trachea bifurcates to give rise to two primary bronchi, Hill Animal Physiology 4E are profusely surrounded by blood capillaries and are the sites which Sinauerenter the lungs. Here the similarity to mammals ends. The Associates of gas exchange. They are only 3–14 μm in diameter (large birds primary bronchus that enters each lung passes through the lung, Morales Studio tending to have diameters greater than those of small birds), Figure known being 23.24 12-09-15 as the mesobronchus within the lung. Two groups and collectively they form an enormous gas-exchange surface of branching secondary bronchi arise from the mesobronchus. amounting to 200–300 mm2/mm3 of tissue in the parabronchial One group, which arises at the anterior end of the mesobronchus, walls. Air flows through the central lumen of each parabronchus, spreads over the ventral surface of the lung. The other group origi- but exchange between the central lumen and the surfaces of its nates toward the posterior end of the mesobronchus and spreads air capillaries is probably largely by diffusion. The parabronchi, over the dorsolateral lung surface. For simplicity, we call these air capillaries, and associated vasculature constitute the bulk of the anterior and posterior groups of secondary bronchi, although the lung tissue of a bird. 624 Chapter 23 (A) Scanning electron micrograph of parabronchi in longitudinal section (C) A parabronchus and associated vasculature Air capillaries Efferent blood Parenchyma vessel (intermingled air capillaries and blood capillaries) Openings such as these lead to air capillaries. (B) Scanning electron micrograph of a parabronchus in cross section Parabronchus 0.5 mm This tissue consists of intermingled air capillaries and Afferent blood capillaries. Air flow Blood flow blood vessel Figure 23.25 Parabronchi and air capillaries: The gas-exchange sites in avian lungs (A) Scanning electron micrograph of the lung of a chicken (Gallus). Magnification: 12× (B) Scanning electron micrograph of a single parabronchus of a chicken lung in cross section. Magnification: 43× (C) Diagram of the structure of a para- bronchus and how blood flow relates to the parabronchus. (A and B courtesy of Dave Hinds and Walter S. Tyler.) A bird’s air sacs, which are part of the breathing system, are located outside the lungs and occupy a considerable portion of the thoracic and abdominal body cavities (Figure 23.26). Usually there are nine air sacs, divisible into two groups. The anterior air sacs (cervical, anterior thoracic, and interclavicular) connect to various anterior secondary bronchi. The posterior air sacs (abdominal and posterior thoracic) connect to the posterior portions of the meso- Anterior secondary bronchi. (Each mesobronchus terminates at its connection with an bronchi Cervical abdominal air sac.) The air sacs are thin-walled, poorly vascularized sac Posterior structures that play little role in gas exchange between the air and Primary secondary bronchi bronchis blood. Nonetheless, as we will see, they are essential for breathing. The structures of the lung described thus far are present in all birds, and their connections with the air sacs are similar in all birds. These lung structures are collectively termed the paleopulmonal Abdominal Hill Animal Physiology 4E Sinauer, Associates system or simply paleopulmo. Most birds, in addition, have a sac more or Studio Morales less extensively developed system of respiratory para- Trachea Anterior Posterior bronchial tubes—termed Figure 23.25 12-09-15 the neopulmonal system —running thoracic sac thoracic sac directly between the posterior air sacs and the posterior parts of the Syrinx mesobronchi and posterior secondary bronchi (see Figure 23.24A). Mesobronchus The neopulmonal system is especially well developed in songbirds. Interclavicular The paleopulmonal system, nonetheless, is always dominant. sac Figure 23.26 The air sacs of a goose and their connections Ventilation is by bellows action to the lungs Air sacs are blue, lungs are light orange. All the air Avian lungs are compact, rigid structures. Unlike mammalian sacs are paired, except the single interclavicular sac. (After Bracken- lungs, they undergo little change in volume over the course of bury 1981.)  External Respiration 625 BOX Bird Development: Filling the each breathing cycle. The air sacs, by contrast, expand and contract 23.3 Lungs with Air Before Hatching substantially and, like bellows, suck and push gases through the relatively rigid airways of the lungs. To a dramatic extent relative The lungs of both mammals and birds initially develop in a to mammalian ventilation, this avian process is an energetically fluid-filled condition. Young animals of both groups there- inexpensive way to move air. fore face the problem of filling their lungs with air so as to The part of the rib cage surrounding the lungs themselves is be able to breathe when they are born or hatched. When relatively rigid. During inhalation, other parts of the rib cage (es- mammals are born, they are able to fill their lungs sufficiently pecially those posterior to the lungs) are expanded by contraction to survive by inflating them suddenly with their first breath of internal intercostal muscles and certain other thoracic muscles, from the atmosphere (all nonavian reptiles do likewise). and the sternum swings downward and forward. These movements Birds, however, cannot inflate their lungs in this way: The air enlarge all the air sacs by expanding the thoracoabdominal cavity. capillaries in their lungs cannot be inflated suddenly out of Some of the external intercostals and abdominal muscles compress a collapsed state because the lungs are relatively rigid and the thoracoabdominal cavity and air sacs during exhalation. Rest- the air capillaries have extremely small diameters. Another ing birds typically breathe at only about one-half or one-third the obstacle to a sudden-inflation strategy for birds is that avian frequency of resting mammals of equivalent body size, but the lungs probably will not work correctly unless every critical birds have greater tidal volumes. airway becomes gas-filled, because the pattern of airflow through the lungs is determined by complex aerodynamic Air flows unidirectionally through interactions among the airways. Birds have thus evolved a the parabronchi way to fill their lungs with air gradually before the lungs be- Air flows unidirectionally through the parabronchi of the paleo- come essential for breathing. pulmonal system. To see how this occurs, we must describe the During most of a bird’s development inside an egg, its movement of air during both inhalation and exhalation. During breathing organ is a highly vascular chorio-allantoic mem- inhalation, both the anterior and posterior sets of air sacs expand. brane pressed against the eggshell on the inside. Oxygen Suction, therefore, is developed in both sets of air sacs, and both and CO2 pass between the atmosphere and the mem- receive gas. As depicted in Figure 23.24B, air inhaled from the brane by diffusion through gas-filled pores in the eggshell. atmosphere flows through the mesobronchus of each lung to enter As an egg develops, it dehydrates by controlled loss of the posterior air sacs and posterior secondary bronchi. Simultane- water vapor outward through the eggshell pores, a process ously, the air entering the posterior secondary bronchi is drawn that leads to the formation of a gas-filled space, the air anteriorly through the parabronchi by suction developed in the cell, inside the egg at its blunt end. About 1–2 days before expanding anterior air sacs. Three aspects of the events during a young bird hatches, it starts to breathe from the air cell, inhalation deserve emphasis. First, the posterior air sacs are filled inhaling and exhaling gas. During the ensuing hours until with relatively fresh air coming directly from the environment. it hatches, the bird makes a gradual transition from gas ex- Second, the anterior air sacs are filled for the most part with stale change across its chorio-allantoic membrane to full-fledged gas that has passed across the respiratory exchange surfaces in the pulmonary breathing. The air capillaries, in fact, undergo parabronchi. Finally, the direction of ventilation of the parabronchi most of their prehatching development during this period. in the paleopulmonal system is from posterior to anterior. The airways and air capillaries in the lungs fill with gas and During exhalation, both sets of air sacs are compressed and thus are already gas-filled by the time hatching begins and discharge gas. As shown in Figure 23.24C, air exiting the poste- the chorio-allantoic membrane is left behind. rior air sacs predominantly enters the posterior secondary bronchi to pass anteriorly through the parabronchi. This air is relatively fresh, having entered the posterior sacs more or less directly from muscular valves could be present, but evidence for their existence the environment during inhalation. Gas exiting the parabronchi is at best circumstantial. Most present evidence suggests that the anteriorly, combined with gas exiting the anterior air sacs, is directed complex architecture of the lung passages creates aerodynamic into the mesobronchus via the anterior secondary bronchi and conditions that direct air along the inspiratory and expiratory paths exhaled. Recall that the anterior air sacs were filled with stale gas without need of either passive or active valves. from the parabronchi during inhalation. Thus the exhaled gas is Ventilation of the neopulmonal system is incompletely under- mostly gas that has passed across the respiratory exchange surfaces. stood. Probably, however, airflow through many of the neopulmonal Three aspects of the expiratory events deserve emphasis: First, the parabronchi is bidirectional (see Figure 23.24B,C). relatively fresh air of the posterior air sacs is directed mostly to the As discussed in Box 23.3, birds face unique challenges at parabronchi. Second, most of the gas that is exhaled from the lungs hatching because of their lungs, which at that point must take over has passed across the respiratory exchange surfaces. Finally, air full responsibility for gas exchange. flows through the parabronchi of the paleopulmonal system from posterior to anterior, just as it does during inhalation. The gas-exchange system is cross-current One of the greatest remaining questions in the study of avian When the unidirectional flow of air through the paleopulmonal lungs is how air is directed along its elaborate (and in some ways parabronchi in the lungs of birds was first discovered, countercur- counterintuitive) paths through the paleopulmonal system and air rent exchange between the blood and air was quickly hypothesized. sacs. Passive, flaplike valves appear to be entirely absent. Active, Soon, however, this hypothesis was disproved by clever experi- 626 Chapter 23 ments, which showed that the efficiency of gas exchange between internal gills (see Figure 23.2). Certain of the aquatic snails provide air and blood is not diminished if the direction of airflow in the a straightforward example. In them (Figure 23.28A), a series of parabronchi is artificially reversed. Morphological and functional modest-sized gill leaflets hangs in the mantle cavity and is venti- studies have now shown convincingly that blood flow in the respi- lated unidirectionally by ciliary currents. Blood flow through the ratory exchange vessels of the circulatory system occurs in a cross- leaflets, in at least some cases, is opposite to the direction of water current pattern relative to the flow of air through the parabronchi flow. Thus countercurrent gas exchange occurs. (see Figures 23.5 and 23.25C). One major modification of the gills in molluscs is the evolution of extensive sheetlike gills in the clams, mussels, oysters, and other Summary lamellibranch (“sheet-gilled”) groups. In these groups, four gill Breathing by Birds sheets, or lamellae, composed of fused or semifused filaments, hang within the mantle cavity (Figure 23.28B). Cilia on the gill „„The lungs of birds are relatively compact, rigid structures sheets drive incoming water through pores on the gill surfaces into consisting mostly of numerous tubes, running in parallel, water channels that run within the gill sheets; the water channels termed parabronchi. Fine air capillaries, extending then convey the water to exhalant passages. The direction of water radially from the lumen of each parabronchus, are the principal sites of gas exchange. Air sacs, which are flow within the water channels is opposite to the direction of blood nonrespiratory, are integral parts of the breathing system. flow in the major gill blood vessels, meaning that countercurrent gas exchange can again occur. The specialized sheetlike gills of „„The lungs are ventilated by a bellows action generated these molluscs represent, in part, an adaptation for feeding: As by expansion and compression of the air sacs. the abundant flow of incoming water passes through the arrays „„Airflow through the parabronchi of the paleopulmonal of pores leading to the interior water channels of the gill sheets, system (the major part of the lungs) is posterior to anterior during both inhalation and exhalation. Cross- food particles suspended in the water are captured for delivery to current gas exchange occurs. the mouth (a type of suspension feeding; see page 145). In some (not all) molluscs with sheetlike gills, the food-collection function has become paramount: Respiratory gas exchange across general Breathing by Aquatic Invertebrates body surfaces suffices to meet metabolic needs. Thus the “gills” have become primarily feeding organs. and Allied Groups In the cephalopod molluscs—the squids, cuttlefish, and oc- Many small aquatic invertebrates, and some large ones, have no topuses—it is not so much the gills that are specialized, but the specialized breathing organs. They exchange gases across general mechanism of ventilation. The gills are feathery structures that body surfaces, which sometimes are ventilated by swimming mo- follow the usual molluscan plan of being positioned in the mantle tions or by cilia- or flagella-generated water currents. Many larvae cavity (Figure 23.28C). They are ventilated, however, by muscular and some adults also lack a circulatory system. Thus gases move contraction rather than beating of cilia. Cephalopods swim by using within their bodies by diffusion or by the squishing of body fluids muscular contractions of the mantle; they alternately suck water into from place to place. To the human eye, these sorts of gas-exchange the mantle cavity via incurrent openings and then drive it forcibly systems are confining. They suffice only if the animals are tiny (see outward through a ventral funnel by mantle contraction, producing Box 22.1) or have specialized body plans, such as those of flatworms a jet-propulsive force. The gills are ventilated (in countercurrent and jellyfish. Most cells of a flatworm are near a body surface be- fashion) by the vigorous flow of water used for propulsion. Some cause the worm’s body is so thin. Most cells of a jellyfish are near a species move so much water for propulsion that they use only a body surface because a jellyfish’s body is organized with its active small fraction of the O2 in the water: 5%–10%. tissues on the outside and primarily low-metabolism, gelatinous A final specialization worthy of note in molluscs is the evolution tissue deep within. of the mantle cavity into a lung in the dominant group of snails Adults of the relatively advanced phyla of aquatic invertebrates and slugs that live on land, a group known aptly as the pulmonates typically have gills of some sort. The gills of the various major (Figure 23.28D). In the terrestrial pulmonates, gills have disap- phyletic groups are often independently evolved. Thus, whereas peared, and the walls of the mantle cavity have become highly they all are evaginated and project into the water (meeting the vascularized and well suited for gas exchange. Some species are definition of gills), they vary widely in their structures and in how thought to employ the mantle cavity as a diffusion lung, but others they are ventilated (Figure 23.27). ventilate it by raising and lowering the floor of the cavity. Molluscs exemplify an exceptional diversity of Decapod crustaceans include many important breathing organs built on a common plan water breathers and some air breathers The phylum Mollusca nicely illustrates that within a phyletic group, In the decapod crustaceans—which include many ecologically a single basic sort of breathing apparatus can undergo wide diversi- and commercially important crabs, shrimps, lobsters, and cray- fication. In molluscs, outfolding of the dorsal body wall produces a fish—the head and thorax are covered with a continuous sheet sheet of tissue, the mantle (responsible for secreting the shell), that of exoskeleton, the carapace, that overhangs the thorax laterally, overhangs or surrounds all or part of the rest of the body, thereby fitting more or less closely around the bases of the thoracic legs. enclosing an external body cavity, the mantle cavity. The gills of The carapace encloses two lateral external body cavities—the molluscs typically are suspended in the mantle cavity and thus are branchial chambers —in which the gills lie (Figure 23.29A).  External Respiration 627 (A) Polychaete annelid with gill tufts (B) Polychaete annelid with tentacular fan Gills The tentacles function as gills. They also collect food particles. (D) Horseshoe crab (ventral view) showing a single gill composed of many gill sheets This gill plate has been pulled back to show the gill sheets beneath it. (C) Sea star with branchial papulae and tube feet used as gills Radial canal Sea star showing major internal parts of water vascular system Water ring Gill sheets KEY Convection Diffusion Gill plates Branchial papulae Radial canal of water vascular The branchial system Digestive papulae are gills… cecum Perivisceral coelom filled with coelomic fluid Gonad …and the tube feet Oral side function partly as gills. Figure 23.27 A diversity of gills in aquatic invertebrates gases pass between the coelomic fluid and ambient water by diffusion (A) This terebellid worm (Amphitrite), a type of marine annelid, lives through the walls of the papulae. Similarly, gases diffuse between the inside a tube it constructs and can pump water in and out of the tube. coelomic fluid and ambient water through the tube feet and associat- (B) This fanworm, another type of marine annelid, also lives in a tube, ed parts of the water vascular system. Cilia accelerate these processes but when undisturbed, it projects its well-developed array of pinnately by circulating fluids over the inner and outer surfaces of the papulae divided tentacles into the ambient water. The tentacles are used for and tube feet. (D) Horseshoe crabs (Limulus) have unique book gills, both feeding and respiratory gas exchange; they are ventilated by the consisting of many thin gill sheets arranged like pages of a book. The Hillof cilia action Animal onPhysiology 4E (C) Sea stars bear many thin-walled, the tentacles. book gills are protected under thick gill plates, which undergo rhythmic Sinauer fingerlike Associatesfrom their coelomic cavity, termed branchial projections flapping motions that ventilate the gills. (D after a drawing by Ralph Morales papulae Studio (“gill processes”), on their upper body surfaces; respiratory Russell, Jr.) Figure 23.27 12-10-15  628 Chapter 23 (A) A transverse section through the thorax of a crayfish The carapace—a sheet of exo- Pericardial skeleton—overhangs the body. (A) Aquatic snail Heart sinus It thus… Gut Gill leaflets hanging in Shell the mantle cavity are Branchial …encloses a branchial chamber chamber on each side. ventilated by water currents generated by The gills are in the ciliary action. branchial chambers. Mantle cavity Gills Gills Lateral Muscle carapace KEY Base of Convection leg Foot Ventral nerve cord (B) Clam (a lamellibranch mollusc) (B) A lateral view showing the gills under the carapace Gill Carapace Shell Visceral mass Water for gill ventilation is drawn into and expelled Foot Gill lamella from the mantle cavity through openings called siphons. Scaphognathite Mantle Exhalant cavity siphon Shell The scaphognathite beats, driving Mantle water out of the branchial cavity chamber. Because of the suction thus produced in the chamber, water enters at multiple places. Foot Inhalant siphon Figure 23.29 The gills and ventilation in a crayfish Gill lamella with pores and internal channels Cilia on the sheetlike gills drive The gills arise from near the bases of the thoracic legs. Each gill water through pores into internal consists of a central axis to which are attached many richly vas- water channels, which convey the water to the exhalant siphon. cularized lamellar plates, filaments, or dendritically branching tufts. The gill surfaces—like all the external body surfaces of (C) Squid (a cephalopod) crustaceans—are covered with a chitinous cuticle. The cuticle on Mantle cavity Gills the gills is thin, however, and permeable to gases. Ventilation in crustaceans is always accomplished by muscular contraction, because the body surfaces of crustaceans lack cilia. In decapod crustaceans, each branchial chamber is ventilated by a specialized appendage—the scaphognathite or gill bailer—located toward its anterior end (Figure 23.29B). Beating of this appendage, Funnel (formed under control of nerve impulses from a central pattern generator in from mantle) Squid gills are ventilated by muscle power. They are theHill central nervous Animal system, Physiology 4E generally drives water outward through positioned in the muscle-driven anSinauer anterior exhalant opening. Negative pressure is thus created Associates water stream the animal uses Morales to swim by jet propulsion. within theStudio branchial chamber, drawing water in at various openings. Figure 23.29 12-10-15 Ventilation is unidirectional, and countercurrent exchange may occur. (D) Pulmonate land snail Some crabs and crayfish have invaded the land, especially in the Lung tropics. All the semiterrestrial and terrestrial species retain gills, which (mantle A pulmonate land snail lacks gills, but has a lung are supported to some degree by their cuticular covering. One trend cavity) derived from the observed in semiterrestrial and terrestrial crabs is that the gills tend mantle cavity. to be reduced in size and number by comparison with aquatic crabs. Shell A second trend is that the branchial chambers tend to be enlarged (“ballooned out”), and the tissue9 that lines the chambers tends to be specialized by being well vascularized, thin, and thrown into folds that increase its surface area. These trends—the reduction of the gills Figure 23.28 The diversification of the breathing system in 9 molluscs This tissue is called the branchiostegites. Hill Animal Physiology 4E Sinauer Associates Morales Studio Figure 23.28 12-10-15  External Respiration 629 and the development of lunglike branchial chambers—are strikingly parallel to those seen earlier in air-breathing fish and air-breathing (pulmonate) snails. The branchial chambers of crabs on land are typically ventilated with air by beating of the scaphognathites. In the species that are semiterrestrial (amphibious), the gills are kept wet by regular trips to bodies of water. Recent evidence suggests that in these crabs, O2 is chiefly taken up by the branchial-chamber epithelium, whereas CO2 is chiefly voided across the gills. In fully terrestrial species of crabs, water is not carried in the branchial chambers, and the branchial-chamber epithelium may bear chief responsibility for exchange of both O2 and CO2. Summary Breathing by Aquatic Invertebrates and Allied Groups „„The gills of various groups of aquatic invertebrates are often independently evolved. Wide variation thus exists in both gill morphology and the mode of gill ventilation. „„A single basic sort of breathing apparatus can undergo wide diversification within a single phyletic group. This general principle is illustrated by the molluscs, the great majority of which have breathing organs associated with the mantle and located in the mantle cavity. Figure 23.30 A praying mantis, one of the largest existing Whereas both aquatic snails and lamellibranchs employ insects To look at a praying mantis, one could imagine it breath- ciliary ventilation, the gills are modest-sized leaflets in ing through its mouth. Nothing could be further from the truth. snails, but expansive sheets (used partly for feeding) in the lamellibranchs. Cephalopods, such as squids, ventilate their gills by muscular contraction. Most land organs that sometimes function in parallel with tracheal systems snails lack gills and breathe with a lung derived from the and sometimes are the sole breathing organs (Box 23.4). mantle cavity. The tracheae of an insect develop as invaginations of the epi- dermis and thus are lined with a thin cuticle. Typically the cuticle is Breathing by Insects and Other thrown into spiral folds, providing resistance against collapse. The tracheae become finer with increasing distance from the spiracles Tracheate Arthropods and finally give rise to very fine, thin-walled end-tubules termed The insects (Figure 23.30) have evolved a remarkable strategy tracheoles, believed to be the principal sites of O2 and CO2 exchange for breathing that is entirely different from that of most meta- with the tissues. Tracheoles are perhaps 200–350 μm long and are bolically active animals. Their breathing system brings the gas- believed to end blindly. They generally taper from a lumen diameter exchange surface itself close to every cell in the body. Thus, with approximating 1 μm at their origin to 0.05–0.20 μm at the end. The some thought-provoking exceptions, the cells of insects get their walls of the tracheoles and the finest tracheae are about 0.02–0.2 O2 directly from the breathing system, and the circulatory system μm thick—exceedingly thin by any standard (see Figure 23.8B). plays little or no role in O2 transport. Insect blood, in fact, usually Although the layout of the tracheal system varies immensely lacks any O2-transport pigment such as hemoglobin. among various species of insects, the usual result is that all tissues The body of an insect is thoroughly invested with a system of are thoroughly invested with fine tracheae and tracheoles. The gas-filled tubes termed tracheae (Figure 23.31A,B). This system degree of tracheation of various organs and tissues tends to vary opens to the atmosphere by way of pores, termed spiracles, located directly with their metabolic requirements. For the most part, the at the body surface along the lateral body wall. Tracheae penetrate tracheoles run between cells. However, in the flight muscles of many into the body from each spiracle and branch repeatedly, collectively species, the tracheoles penetrate the muscle cells, indenting the cell reaching all parts of the animal (only major branches are seen in membranes inward, and run among the individual myofibrils, in Figure 23.31). The tracheal trees arising from different spiracles close proximity to the arrays of mitochondria. The average distance typically join via large longitudinal and transverse connectives to form between adjacent tracheoles within the flight muscles of strong a fully interconnected tracheal system. The spiracles, which number fliers is often only about 3 μm. The nervous system, rectal glands, from 1 to 11 pairs, are segmentally arranged and may occur on the and other active tissues—including muscles besides the flight thorax, abdomen, or both (but not the head). Usually they can be muscles—also tend to be richly supplied by the tracheal system, closed by spiracular muscles. Although tracheal breathing is best although intracellular penetration is not nearly as common as in understood in insects, there are other tracheate arthropods: Most flight muscles. In the epidermis of the bug Rhodnius, which has been notably, certain groups of spiders and ticks have tracheal systems. carefully studied, tracheoles are much less densely distributed than Some spiders and other arachnids have book lungs, unique breathing in active flight muscles, but nonetheless, cells are usually within 630 Chapter 23 BOX 23.4 The Book Lungs of Arachnids Some arachnids possess a novel type thrown into many lamellar folds: the of respiratory structure, the book lung. “pages of the book.” Blood streams Atrium Scorpions have only book lungs. Many through the lamellae, whereas the species of spiders also have book lungs, spaces between adjacent lamel- but they may have systems of tracheae lae are filled with gas. The lamellae as well. The number of book lungs in an commonly number into the hun- individual arachnid varies from a single dreds, and the blood-to-gas dis- Lamellae pair (as in certain spiders) to four pairs tance across their walls is often less Air spaces (in scorpions). Book lungs are invagina- than 1 μm. Some book lungs may tions of the ventral abdomen, lined with function as diffusion lungs, whereas Spiracle a thin chitinous cuticle. Each book lung others are clearly ventilated by A book lung The section shows the internal consists of a chamber, the atrium, which pumping motions. They oxygenate structure of a book lung in a two-lunged spider. opens to the outside through a closable the blood, which then carries (After Comstock 1912.) ventral pore, the spiracle (see figure). The O2 throughout the body. dorsal or anterior surface of the atrium is 30 μm of a tracheole. In other words, no cell is separated from a ones. This trend could represent an evolutionary compensation branch of the tracheal system by more than two or three other cells! for diffusion limitations in large-bodied insects. If so, the trend The terminal ends of the tracheoles are sometimes filled with would suggest that a tracheal breathing system poses obstacles liquid when insects are at rest. During exercise, or when the insects to the evolution of large body size. are exposed to O2-deficient environments, the amount of liquid When considering an individual insect, a question that arises is decreases and gas penetrates farther into the tracheoles. This process how the rate of diffusion can be varied to correspond to the insect’s facilitates the exchange of O2 and CO2 because of the greater ease needs for O2. Although diffusion may sound like a process that of diffusion in gas than liquid. is purely physical and therefore independent of animal needs, in Distensible enlargements of the tracheal system called air fact its rate responds to an insect’s metabolic needs because the sacs are a common feature of insect breathing systems (Figure animal’s metabolism alters the partial pressures of gases. Suppose 23.31C) and may occur in the head, thorax, or abdomen. Some that an insect breathing by diffusion has an adequate rate of O2 air sacs are swellings along tracheae, whereas others form blind transport Hillwhen Animal (1)Physiology 4E the atmospheric O2 partial pressure is at the Sinauer Associates endings of tracheae. Air sacs tend to be particularly well developed level marked ➊ in Figure 23.32A and (2) the O2 partial pressure Morales Studio in active insects, in which they may occupy a considerable fraction at the inner end Figure Boxof23.04 its tracheal 12-10-15system is at the level marked ➋. If of the body volume. the insect suddenly increases its rate of O2 consumption, its end- tracheal O2 partial pressure will fall because of the increased rate Diffusion is a key mechanism of gas transport of O2 removal from the tracheae. This decline in the end-tracheal through the tracheal system partial pressure will increase the difference in partial pressure The traditional dogma has been that the tracheal system of most between the two ends of the tracheal system and thus acceler- insects functions as a diffusion lung, meaning that gas transport ate O2 diffusion. Suppose that the difference in partial pressure through the system occurs solely by diffusion. This dogma is pres- between level ➊ and level ➌ in Figure 23.32A is sufficient for ently undergoing profound revision. Diffusion, nonetheless, seems O2 to diffuse fast enough to meet the insect’s new (higher) O2 likely to be an important gas-transport mechanism in subparts need. The end-tracheal partial pressure will then fall to level ➌ of the tracheal system in most or all insects and may be the sole and stabilize. In this way, the rate of diffusion will automatically transport process in some. Diffusion can occur fast enough to play increase to meet the insect’s heightened O2 need. this role because the tracheae are gas-filled. Of course, there are limits to the ability of the process just Because of the importance of diffusion in insect breathing and described to increase the rate of O2 diffusion. The end-tracheal because diffusion transport tends to be slow when distances are O2 partial pressure must itself remain sufficiently high for O2 great, physiologists have long wondered whether insect body size to diffuse from the ends of the tracheae to the mitochondria in is limited by the nature of the insect breathing system. A recent cells. If an insect’s oxygen cascade follows line ➊-➋-➍ in Figure study using a new X-ray technique to visualize the tracheal system 23.32B when the insect has a low rate of cellular O2 use, it might (see Figure 23.31B) revealed that in beetles of different body sizes, follow line ➊-➌-➎ when the insect’s rate of O2 use is raised. The the volume of the tracheal system is disproportional to body size. mitochondrial O2 partial pressure would then be very low, and a In stark contrast to mammals, a greater proportion of body space further increase in the rate of O2 diffusion might not be possible is devoted to the breathing system in big beetles than in small while keeping the mitochondrial O2 level adequate.  (A) Major parts of the tracheal system in a flea (C) Air sacs in the abdomen of External Respiration 631 a worker honeybee Abdominal spiracles 1–7 Abdominal Thoracic spiracle 8 Figure 23.31 Insects breathe using a tra- spiracle 1 cheal system of gas-filled tubes that— branching and rebranching—reach all Air sac tissues from the body surface (A) The principal tracheae in a flea in the genus Xeno- Origins of psylla—an insect that has ten pairs of spiracles tracheae (two thoracic pairs and eight abdominal). (B) The tracheae in a tiny living adult carabid Transverse beetle in the genus Notiophilus, visualized by tracheal a cutting-edge technique, synchrotron X-ray Tracheae connective phase-contrast imaging. (C) Air sacs and as- sociated tracheae in the abdomen of a worker honeybee (Apis). Additional air sacs occur in 0.5 mm the head and thorax. (A after Wigglesworth 1935; B from Socha et al. 2010; image courtesy of Jake Socha.) (B) Tracheae in a carabid beetle A new X-ray method is permitting physiologists to see, for the first time, large parts of the tracheal system in living insects. Inner end of Eye (A) Ambient air tracheal system O2 partial pressure 1 Trachea in head 2 Slow O2 transport Location of a spiracle (note tuft of tracheae Trachea 3 Fast O2 transport originating here) in leg Inner end of Mitochondria (B) Ambient air tracheal system in cells 1 O2 partial pressure 2 1 mm 4 Slow O2 transport 3 Some insects employ conspicuous ventilation Conspicuous (macroscopic) ventilation of the tracheal system oc- 5 Fast O2 transport curs in some large species of insects at rest and is common among active insects. Grasshoppers and locusts, for example, are easily Figure 23.32 Insect oxygen cascades assuming oxygen seen to pump their abdomens, and abdominal pumping occurs transport by diffusion These diagrams outline simplified thought also in bumblebees, ants, and some other insects. The abdominal exercises. (A) A drop in the O2 partial pressure at the inner end pumping motions alternately expand and compress certain of the of the tracheal system from level ➋ to level ➌ will speed diffusion tracheal airways, either causing tidal ventilation or causing air to through the tracheal system by increasing the difference in partial be sucked in via certain spiracles and expelled via others, flowing pressure from one end to the other. (B) For the rate of diffusion to the unidirectionally through parts of the tracheal system in between. mitochondria to be accelerated, the difference in partial pressure between the inner end of the tracheal system and the mitochondria AirHillsacs, when Animal present4E Physiology (as they are in grasshoppers and bumble- Sinauer Associates must be increased—as well as the difference between the ambient bees, for example), commonly act as bellows during such muscular air and the inner tracheae. Eventually no further increase in the rate Morales Studio pumping movements; they may be compressed to only 25%–50% Figure 23.31 12-10-15 of diffusion will be possible because the mitochondrial partial pres- of their full size during each cycle of compression. A mechanism of sure will become too low for mitochondrial function. 632 Chapter 23 conspicuous tracheal ventilation that is important in many insects In addition to the forms of microscopic ventilation we have during flight is autoventilation: ventilation of the tracheae sup- already discussed, several other types have been reported during plying the flight muscles driven by flight movements. the last 25 years. These include processes named miniature ventila- Physiologists have generally hypothesized that during conspicuous tion pulses in grasshoppers and tiny Prague cycles of CO2 release ventilation, air is forced to flow only in major tracheae, with diffusion in beetles. being the principal mode of gas transport through the rest of the According to the old dogma, insects that were not conspicu- tracheal system. According to this hypothesis, the function of con- ously pumping their abdomens or ventilating in other conspicuous spicuous ventilation is essentially to reduce the path length for diffusion ways were breathing entirely by diffusion. The evidence is now by moving air convectively to a certain depth in the tracheal system. overwhelming that convective phenomena are widely employed by visibly motionless insects, but many mysteries remain regarding the Microscopic ventilation is far more common exact interplay of convection and diffusion in the tracheal system. than believed even 15 years ago A revolution is underway in the understanding of microscopic Control of breathing ventilation: forced airflow that occurs on such fine scales that it is A vulnerability of the insect respiratory system is that it can per- impossible to detect without the use of technology. Probably the mit rapid evaporative loss of body water. The gas in the tracheal most dramatic recent discovery is that when microscopic X-ray airways is humid—ordinarily saturated with water vapor—and videos are made of various insects—such as beetles, crickets, and when the spiracles are open, only a minute distance separates the ants—the major tracheae in the head and thorax are observed to humid tracheal gas from the atmosphere. Outward diffusion of undergo cycles of partial compression and relaxation, a process water vapor can accordingly be rapid. Insects commonly solve this named rhythmic tracheal compression. These pulsations occur ev- problem by keeping their spiracles partly closed—or by periodi- ery 1–2 s and are substantial: Each compression reduces the vol- cally opening and closing them—whenever compatible with their umes of the tracheae to 50%–70% of their relaxed volumes. These needs for O2 and CO2 exchange. If the spiracles of resting insects microscopic cycles of tracheal compression probably move gases are experimentally forced to remain fully open all the time, the rate convectively. They may be particularly important for O2 delivery of evaporative water loss increases 2- to 12-fold, demonstrating the to the head and brain, recognizing that tracheae to the head con- importance of keeping them partly closed. nect to the atmosphere at thoracic spiracles and thus may be long. In insects using diffusion transport, it is common for the spiracles Similar X-ray studies have revealed that in some insects under to be opened more fully or frequently as the insects become more some conditions, tracheae undergo massive rhythmic collapsing active. The greater opening of the spiracles facilitates O2 transport to movements during which they completely empty and refill. This is the tissues, although it also tends to increase evaporative water loss. observed, for example, in some moth caterpillars exposed to hypoxia. Insects that ventilate their tracheal systems by abdominal pumping One of the first sorts of evidence for microscopic ventilation or other conspicuous mechanisms are well known to increase their was the discovery and analysis of discontinuous gas exchange rates of ventilation as they become more active. in diapausing pupae10 of moths some decades ago. The hallmark What is the chemosensory basis for spiracular control? The and defining feature of discontinuous gas exchange is that an insect most potent stimulus for opening of the spiracles in insects is an releases CO2 to the atmosphere in dramatic, intermittent bursts, increase in the CO2 partial pressure and/or H+ concentration of the whereas the insect takes up O2 from the atmosphere at a relatively body fluids. A decrease in the O2 partial pressure in the body fluids steady rate. The observed pattern of CO2 release arises in large part may also stimulate spiracular opening but typically offers far less from spiracular control. In the periods between one burst of CO2 potent stimulation. In these respects, the control of the spiracles in release and the next, the spiracles are closed or partly closed, and insects resembles the control of pulmonary ventilation in mammals. CO2 produced by metabolism accumulates in body fluids by dissolving and reacting to form bicarbonate (HCO3 –). Because O2 is removed Aquatic insects breathe sometimes from the from the tracheal airways by metabolism during these periods, but water, sometimes from the atmosphere, and the CO2 produced by metabolism temporarily accumulates in the sometimes from both body fluids rather than in the airways, a partial vacuum—a negative Many insect species live underwater in streams, rivers, and ponds pressure—can develop in the airways. When such a negative pres- during parts of their life cycles. The aquatic life stages of some of sure develops, it sets the stage for microscopic ventilation because these species lack functional spiracular openings and obtain O2 atmospheric air can be sucked into the tracheal airways convectively by taking up dissolved O2 from the water using superficial arrays on an inconspicuous, microscopic scale when the insect partly or fully of fine tracheae. These insects often have dense proliferations of opens its spiracles. Investigators have directly assessed in several fine tracheae under their general integument. Many have tracheal species whether inward suction of air actually occurs, and it does gills: evaginations of the body surface that are densely supplied in some (not all) of the species tested. No one knows the depth to with tracheae and covered with just a thin cuticle—a remarkable which air is drawn, but it travels by convection at least through the parallel with the evolution of ordinary gills in numerous other spiracles and into the major tracheae. Discontinuous gas exchange groups of aquatic animals. Tracheal gills may be positioned on the is known today to occur widely in quiescent or resting insects, plus outer body surface or in the rectum. In aquatic insects that breathe certain ticks, mites, and spiders. with tracheal gills or other superficial tracheae, the tracheal system remains gas-filled. Oxygen diffuses into the tracheal airways from 10 Diapause is a programmed resting stage in the life cycle. the water across the gills or other super