Physiology | CH 23 Notes | Knowt (2024)

Tunas represent one of the pinnacles of water breathing. If they lived on land, where they could be readily observed, they would be classified metaphorically with wolves, African hunting dogs, and other strong, mobile predators. Judging by the length of time spent in motion, tunas are actually more mobile than any terrestrial predator. Using their aero- bic, red swimming muscles, they swim continuously, day and night, at speeds of one to two body lengths per second; some species cover more than 100 km per day during mi- grations.1 Tunas thus rank with the elite endurance athletes among fish, the others being salmon, mackerel, billfish, and certain sharks. To meet the relentless O2 demands of their vigorous lifestyle, tunas require a respiratory system that can take up O2 rapidly from the sea and a circulatory system that can deliver O2 rapidly from the gills to tissues throughout the body. They are, in fisheries ecologist John Magnuson’s memorable phrase, “astounding bundles of adaptations for efficient and rapid swimming.”

Tunas breathe with gills, as do most fish. Their gills are hardly average, however. Instead, tuna gills are exceptionally specialized for O2 uptake, illustrating a general principle in the

1 Burst speeds are 12–15 body lengths per second, but they are not relevant to our discussion here because they are powered relatively anaerobically (by the white swimming muscles).

Throughout the animal king- dom, species that depend on vigorous endurance exercise for survival—such as tunas— must be able to acquire oxy- gen rapidly and steadily Al- though water is not a particularly rich source of O2, tunas have gills and breathing processes that en- able them to live as highly active predators.This is a southern bluefin tuna (Thunnus maccoyii ).

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study of respiration: that a single type of breathing system may exhibit a wide range of evolutionary refinements in various species. Based on studies of yellowfin tunas and skipjack tunas, the gills of a tuna have about eight times more surface area than the gills of a rainbow trout—a relatively average fish—of equal body size. If the gas-exchange membranes of the gills of a small, 1-kg (2.2-pound) tuna were flattened, they would form a square measuring 1.3 m on each side. The gill membranes of tunas are also exceptionally thin: Whereas the average distance between blood and water is about 5 μm in a rainbow trout’s gills, it is 0.6 μm in the gills of a skipjack or yellowfin tuna. Compared with average fish, tunas have evolved gills that present an extraordinarily large surface of extraordinarily thin membrane to the water for gas exchange.

Most fish, including rainbow trout, drive water across their gills by a pumping cycle that is powered by their buccal and opercular muscles (discussed later in this chapter). Some species are adept at alternating between this mechanism of ventilating their gills and another mechanism termed ram ventilation. During ram ventila- tion, a fish simply holds its mouth open while it swims powerfully forward, thereby “ramming” water into its buccal cavity and across its gills; in this way, the swimming muscles assume responsibility for powering the flow of water across the gills. During their evolu- tion, tunas completely abandoned the buccal–opercular pumping mechanism and became obligate ram ventilators, a distinction they share with just a few other sorts of fish. As obligate ram ventilators, they have no choice regarding how much of their time they spend swimming. They must swim continuously forward, or they suf- focate! Physiologists debate whether ram ventilation is intrinsically superior as a way of moving water across the gills. Less debatable is the fact that tunas achieve extraordinarily high rates of water flow using ram ventilation. During routine cruising, a small, 1-kg skipjack or yellowfin tuna drives about 3.6 L of water across its gills per minute; this is seven times the resting flow rate in a 1-kg rainbow trout, and twice the maximum rate of the trout.

Fundamental Concepts of External

Respiration

In all animals, the systems used to exchange respiratory gases with the environment can be diagrammed as in FiguRE 23.1. A gas- exchange membrane or respiratory exchange membrane— a thin layer of tissue consisting typically of one or two simple epithelia—separates the internal tissues of the animal from the environmental medium (air or water).2 External respiration or breathing—the topic of this chapter—is the process by which O2 is transported to the gas-exchange membrane from the environ- mental medium and by which CO2 is transported away from the membrane into the environmental medium. Ventilation is bulk flow (convection) of air or water to and from the gas-exchange membrane during breathing. Not all animals employ ventilation; in some, breathing can occur by diffusion rather than convection.

Oxygen always crosses the gas-exchange membrane by diffu- sion, as stressed in Chapter 22. This means that for O2 to enter an animal from the environment, the partial pressure of O2 on the

2 Membrane is used here in an entirely different way than when speaking of a cell membrane or intracellular membrane. The gas-exchange membrane is a tissue formed by one or more layers of cells.

External respiration (breathing) is this transport of O2 and CO2 to and from the gas-exchange membrane.

O2 CO2

Convection (ventilation) or diffusion

Convection (ventilation) or diffusion

Diffusion

Diffusion (plus sometimes active transport)

Convection O2 (circulation)
or diffusion

Convection CO2 (circulation)
or diffusion

Internal body fluids and tissues

Environmental medium (air or water)

Gas-exchange membrane

FiguRE 23.1 generalized features of animal gas exchange O2 and CO2 move between the environmental medium and the inter- nal tissues of an animal across a gas-exchange membrane.

inside of the gas-exchange membrane must be lower than that on the

outside. The fact that O2 enters animals by diffusion explains why

the area and thickness of the gas-exchange membrane play critical

roles in O2 acquisition. The rate of diffusion across a membrane

increases in proportion to the area of the membrane. Furthermore,

according to the fundamental diffusion equation (see Equation

22.4), the rate of diffusion across a membrane increases as the

thickness of the membrane decreases. These physical laws explain

why an expansive, thin gas-exchange membrane is a great asset

for animals such as tunas that must acquire O2 at high rates. As for

CO2, diffusion is the exclusive mechanism by which it crosses the

gas-exchange membrane in some animals, including humans; in

oHtihllerAs,nhimoawl Pehvyesrio,laolgtyho4EughdiffusionistheprincipalCO2 transport Sinauer Associates

mechanism, active transport also occurs. Active transport of CO2 (as

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HCO –) is best documented in freshwater animals (see Figure 5.15). Figure3 23.01 12-09-15 1/12/16

Usually, just a single part of an animal is identified by name as a “breathing organ.” Other parts may participate in gas exchange with the environment, however. Let’s briefly consider some examples that illustrate the range of possibilities. In mammals and tunas, most of the body surface—the skin—is of very low permeability to gases. Therefore just the identified breathing organs—the lungs and gills—take up almost all O2 and void almost all CO2. In a typi- cal adult frog, by contrast, the skin is permeable to gases; O2 and CO2 are exchanged to a substantial extent across the skin as well as the lungs, and therefore the identified breathing organs—the lungs—are not the only breathing organs. Similarly, some fish breathe with their stomachs as well as their gills, sea stars breathe with their tube feet as well as their gills (branchial papulae), and some salamanders, lacking lungs, breathe only with their skin.

In organs that are specialized for external respiration, the gas- exchange membrane is typically thrown into extensive patterns of invagin*tion or evagin*tion, which greatly increase the membrane surface area. For physiologists, gills and lungs are generic labels that refer to two such patterns (FiguRE 23.2). gills are respiratory structures that are evagin*ted from the body and surrounded by the environmental medium. Lungs, by contrast, are respiratory structures that are invagin*ted into the body and contain the en- vironmental medium. The adjective branchial refers to structures or processes associated with gills, whereas pulmonary refers to those associated with lungs.

Lungs are invagin*ted into the body and contain the environmental medium.

External gills are evagin*ted from the body and project directly into the environmental medium.

Internal gills are evagin*ted from the body and project into a superficial body cavity, through which the environmental medium is pumped.

External Respiration 601 lungs. Within a diffusion lung, the air is still, and O2 and CO2 travel

the full length of the lung passages by diffusion.
A dual breather, or bimodal breather, is an animal that can

breathe from either air or water. Dual breathers often have at least two distinct respiratory structures, which they employ when breathing from the two media. Examples include certain air-breathing fish (with both lung- and gill-breathing) and amphibians (with both lung- and skin-breathing).

FiguRE 23.2 Three types of specialized breathing structures

Although exceptions occur, water breathing is usually by gills, whereas air breathing is usually by lungs. The comparative method strongly indicates that lungs are adaptive for terrestrial life (see Figure 1.18). One advantage of lungs on land is that their finely divided elements receive structural support by being embedded in the body. The finely divided elements of gills project into the environmental medium. This is not a problem in water because there, the fine, evagin*ted gill processes are supported by the water’s substantial buoyant effect.

Gills can be external or internal (see Figure 23.2). External gills

are located on an exposed body surface and project directly into the

surrounding environmental medium. internal gills are enclosed

within a superficial body cavity. Whereas external placement permits

Principles of gas Exchange by

Active Ventilation

Active ventilation is very common, and its analysis involves several specialized concepts that apply to a variety of animals. Here we discuss the principles of active ventilation.

When an animal ventilates its breathing organ (e.g., gills or lungs) directionally—either unidirectionally or tidally—a discrete current of air or water flows to and from the gas-exchange membrane. The rate of O2 uptake by the breathing organ then depends on (1) the volume flow of air or water per unit of time and (2) the amount of O2 removed from each unit of volume:

Rate of O2 uptake (mL O2/min) = Vmedium (CI – CE) (23.1)

where Vmedium is the rate of flow (L/min) of the air or water through the breathing organ, CI is the O2 concentration of the inhaled (in- spired) medium (mL O2/L medium), and CE is the O2 concentration of the exhaled (expired) medium. The difference (CI – CE) represents the amount of O2 removed from each unit of volume of the ventilated medium. The percentage of the O2 available in the inhaled medium that is removed is 100(CI – CE)/CI. This ratio—known as the oxygen utilization coefficient, oxygen extraction coefficient, or oxygen extraction efficiency—expresses how thoroughly an animal is able to use the O2 in the air or water it pumps through its lungs or gills.

To illustrate these calculations, consider a fish for which the water entering the mouth contains 6 mL O2/L, the water exiting the gills contains 4 mL O2/L, and the rate of ventilation is 0.5 L/ min. According to Equation 23.1, the fish’s rate of O2 uptake is 0.5 L/min × 2 mL O2/L = 1 mL O2/min. Moreover, its oxygen utilization coefficient is 33%—meaning that the fish is removing 33% of the

ambient water currents to flow over the gills, internal placement

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usually requires an animal to use metabolic energy to ventilate

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them. Internal placement has its advantages nonetheless. When

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tFhigeugreil2ls3.a02re 1in2t-e09rn-1a5l, the enclosing structures physically protect

them and may help canalize the flow of water across the gills in ways that enhance the efficiency or control of breathing.

Ventilation of lungs, gills, or other gas-exchange membranes may be active or passive. Ventilation is active if the animal creates the ventilatory currents of air or water that flow to and from the gas-exchange membrane, using forces of suction or positive pres- sure that it generates by use of metabolic energy (as by contracting muscles or beating cilia). Ventilation is passive if environmental air or water currents directly or indirectly induce flow to and from the gas-exchange membrane (see Box 22.2). Active ventilation, although it uses an animal’s energy resources, is potentially more reliable, controllable, and vigorous than passive ventilation. Ac- tive ventilation may be unidirectional, tidal (bidirectional), ornondirectional. It is unidirectional if air or water is pumped over the gas-exchange membrane in a one-way path. It is tidal if air or water alternately flows to and from the gas-exchange membrane via the same passages (see Figure 22.6); mammalian lungs illustrate tidal ventilation. Ventilation is nondirectional if air or water flows across the gas-exchange membrane in many directions; animals with external gills that they wave back and forth in the water exemplify nondirectional ventilation.

In air-breathing animals with lungs, the lungs are usually venti- lated. Some lungs, however, exchange gases with the environment entirely by diffusion and are termed diffusion lungs. Some insects and spiders, for example, are believed to breathe with diffusion

602 Chapter 23

Tidal gas exchange

O2 partial pressure in environment

Fresh medium mixes with stale medium in the lung, so the O2 partial pressure of the medium at the ex- change surface with the blood is below that in the environ- mental medium.

O2 diffuses into the blood flowing along the exchange surface. The O2 partial pressure in the blood rises, therefore, toward that in the lung, but...

100 60

O2 from each volume of water it pumps and is allowing the other 67% to flow out with the exhaled water.

Inhalation

Exhalation

Wall of lung

...the O2 partial pres- sure in blood leaving the lung remains lower than that in

the exhaled medium.

Tunas are especially efficient in using the O in the water they 2

drive over their gills. Whereas rainbow trout use 33%, yellowfin and skipjack tunas use 50%–60%.

The O2 partial pressure in blood leaving a breathing organ depends on the spatial relation between the flow of the blood and the flow of the air or water

many ways be considered the best single measure of the breathing organ’s effectiveness. This is clear from the oxygen cascade concept (see Figure 22.8B): An animal with a high O2 partial pressure in the blood leaving its breathing organ is particularly well poised to maintain an O2 partial pressure in its mitochondria that is sufficiently high for aerobic catabolism to proceed without being O2-limited.

Breathing organs with different designs exhibit inherent differences in the blood O2 partial pressure they can maintain. These differences depend on the spatial relation between the flow of blood and the flow of the air or water. The differences are not absolute, because in all designs, the blood O2 partial pressure is affected by additional factors besides spatial flow relations. Nonetheless, the flow relations between the blood and the air or water have great importance.

To explore the implications of various designs, let’s start by considering tidally ventilated breathing organs, such as the lungs of mammals (FiguRE 23.3). Tidally ventilated breathing organs are distinguished by the fact that the medium (air in this case) next to the gas-exchange membrane is never fully fresh. The explanation is that such breathing organs are never entirely emptied between breaths. Consequently, when an animal breathes in, the fresh medium inhaled mixes—inside the breathing organ—with stale medium left behind by the previous breathing cycle, and because of this mixing, the O2 partial pressure of the medium next to the gas-exchange membrane is lower—often much lower—than the partial pressure in the outside environment. The O2 partial pressure in the blood leaving the breathing organ is lower yet (see Figure 23.3), because a partial-pressure gradient must exist between the medium next to the gas-exchange membrane and the blood for O2 to diffuse from the medium into the blood. Characteristically, in tidally ventilated structures, the O2 partial pressure of the blood leaving the breathing organ is below the O2 partial pressure of the exhaled medium.

When ventilation is unidirectional rather than tidal, the two most obvious relations that can exist between the flow of the medium and the flow of the blood are cocurrent and countercurrent. In the cocurrent arrangement (FiguRE 23.4A), the medium flows along the gas-exchange membrane in the same direction as the blood, resulting in cocurrent gas exchange. In the countercurrent ar- rangement (FiguRE 23.4B), the medium and blood flow in opposite directions, and countercurrent gas exchange occurs. Concurrent is sometimes used as a synonym of cocurrent. Thus cocurrent gas exchange may also be called concurrent gas exchange.

In an organ that exhibits cocurrent gas exchange, when O2- depleted afferent3 blood first reaches the gas-exchange membrane, it

3 Afferent means “flowing toward”; in this case it refers to blood flowing toward the gas-exchange membrane. Efferent means “flowing away” and refers to blood flowing away from the gas-exchange membrane.

The O partial pressure in the blood leaving a breathing organ can in 2

FiguRE 23.3 Tidal gas exchange: O2 transfer from the en- vironmental medium to the blood in a tidally ventilated lung Because a tidally ventilated lung is never fully emptied, fresh medium mixes in the lung with stale medium. Numbers are O2 partial pressures in arbitrary units:The blood arriving at the breathing organ is arbitrarily assigned a value of 0, whereas the atmosphere is arbi- trarily assigned a value of 100.

meets fresh, incoming medium, as shown at the left of Figure 23.4A.

Then, as the blood and medium flow along the exchange membrane

in the same direction, they gradually approach equilibrium with

each other at an O2 partial pressure that is intermediate between

their respective starting partial pressures. When the blood reaches

the place where it leaves the exchange membrane, its final exchange

of O2 is with medium that has a partial pressure considerably

bHeillowAnthimaatloPfhtyhsieoleongyvi4rEonmentalmedium.Cocurrentgasexchange Sinauer Associates

therefore resembles tidal exchange, in that the O2 partial pressure

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of blood leaving the breathing organ cannot ordinarily rise above

Figure 23.03 12-09-15

the partial pressure of exhaled medium.
In an organ that exhibits countercurrent gas exchange, when

O2-depleted afferent blood first reaches the gas-exchange mem- brane, it initially meets medium that has already been substantially deoxygenated, as shown at the right of Figure 23.4B. However, as the blood flows along the exchange surface in the direction opposite to the flow of medium, it steadily encounters medium of higher and higher O2 partial pressure. Thus, even as the blood picks up O2 and its partial pressure rises, a partial-pressure gradient favor- ing further uptake of O2 is maintained. The final exchange of the blood is with fresh, incoming medium of high O2 partial pressure. Countercurrent exchange is thus an intrinsically more effective mode of exchange than either tidal or cocurrent exchange. One way to see this clearly is to note that the blood O2 partial pressure created by countercurrent exchange is characteristically much higher than the partial pressure in exhaled medium; in principle, the O2 partial pressure of the blood leaving the breathing organ might even ap- proach equality with the O2 partial pressure in inhaled medium. Moreover, if you compare Figures 23.4A and B, you will see that the O2 partial pressure of the medium falls more—and that of the blood rises more—in 23.4B: Countercurrent exchange achieves a more complete transfer of O2 from the medium to the blood than cocurrent (or tidal) exchange under comparable conditions.

Medium

60

30 50 55 0 Blood

(A) Cocurrent (concurrent) gas exchange

External Respiration 603

100

50

As blood and medium flow in the same direction, they gradually approach equilibrium with each other.

Medium
100 70 56 52

0 30 44 48 Blood

Cross-current gas exchange

Blood

FiguRE 23.5 Cross-current gas exchange: A third mode of O2 transfer from the environmental medium to the blood when ventilation is unidirectional Numbers are O2 partial pressures in arbitrary units, as specified in the caption of Figure 23.3. The afferent blood vessel breaks up into many vessels that “cross” the path followed by the medium; each of these vessels makes exchange contact with just a limited part of the structure through which the medium is flowing.These vessels then coalesce to form

a single efferent vessel. Cross-current exchange is intermediate between cocurrent and countercurrent exchange in its intrinsic gas- transfer efficiency.

exchange. As already noted, however, this ranking is not absolute because additional factors affect the ways in which real breathing organs function in real animals.

Arterial CO2 partial pressures are much lower in water breathers than air breathers

Thus far we have discussed only O2 in the blood leaving the gas- exchange surface. What about CO2? The most important pattern in blood CO2 partial pressure is a distinction between water and air breathers. In water breathers, the partial pressure of CO2 in the blood leaving the breathing organs is always similar to the CO2 partial

(B) Countercurrent gas exchange

100

50

As blood flows in the direction opposite to the medium and picks up O2, it steadily encounters medium of higher O2 partial pressure, so that a partial-pressure gradient favoring O2 diffusion into the blood is maintained.

Distance along exchange surface

Medium
100 75 50 25

Distance along exchange surface

FiguRE 23.4 Cocurrent and countercurrent gas exchange: Two modes of O transfer from the environmental medium

pressure in the ambient water, regardless of whether gas exchange Hill Animal Physiology 4E

2
to the blood when ventilation is unidirectional The upper

diagram in each case depicts the flow of medium and blood along the gas-exchange membrane. Numbers are O2 partial pressures in arbitrary units,as specified in the caption of Figure 23.3.The blood reaches a higher O2 partial pressure when the exchange is counter- current because in that case the blood exchanges with fresh me- dium just before leaving the gas-exchange membrane.

When ventilation is unidirectional, a third possibility is cross-

is tidal, cocurrent, countercurrent, or cross-current. If the ambi-

current gas exchange. In this type of exchange, the blood flow Hill Animal Physiology 4E

ated water, the partial pressure of CO2 in blood leaving the gills is typically about 0.3 kilopascals (kPa) (2 millimeters of mercury [mm Hg]). In sharp contrast, in air breathers the partial pressure of CO2 in the blood leaving the breathing organs is usually far above the CO2 partial pressure in the atmosphere. In mammals and birds, for example, the partial pressure of CO2 in blood leaving the lungs is more than ten times the corresponding value in fish; in humans it is 5.3 kPa (40 mm Hg)! In vertebrates, systemic arterial blood pumpedbythehearttosupplyO2tothebodyisderivedfromthe blood leaving the breathing organs. Thus, from what we have said, if we survey species in which arterial CO2 partial pressure has been measured, we can understand why the arterial CO2 partial pres- sure is typically only 0.1–0.6 kPa (1–4 mm Hg) in water-breathing vertebrates, whereas it is far higher, 4.0–5.3 kPa (30–40 mm Hg), in air-breathing vertebrates. When vertebrates and other animals emerged onto land in the course of evolution, the level of CO2 in their blood and other body fluids shifted dramatically upward.

These patterns are explained principally by the differing physical and chemical properties of water and air. More specifically, they are explained by the analysis of capacitance coefficients, as explained in BOx 23.1.

breaks up into multiple streams, each of which undergoes exchange

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with the medium along just part of the path followed by the medium

Morales Studio (FFigiugreu2R3E.04231.52-)0.9S-o15mebloodthereforeundergoesgasexchange exclusively with O2-rich medium (although other blood exchanges with O2-poor medium). Cross-current exchange permits the O2 partial pressure of the mixed blood leaving the breathing organ to be higher than that of exhaled medium, but it does not permit as high a blood O2 partial pressure as countercurrent exchange under comparable circ*mstances.

The modes of exchange between the blood and the medium can be ranked in terms of their intrinsic ability to create a high O2 partial pressure in the blood leaving the breathing organ (corresponding to their intrinsic efficiency in transferring O2 from the medium to the blood): Countercurrent exchange is superior to cross-current exchange, and cross-current exchange is superior to cocurrent or tidal

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ent water is near equilibrium with the atmosphere and therefore

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nFeigaurrzee2r3o.0i5n it1s2C-0O9-15partial pressure (see Figure 22.1), the blood is

2
also near zero in CO2 partial pressure. For example, in fish in aer-

75 50 25 0 Blood

O2 partial pressure O2 partial pressure

604 Chapter 23

Low O2: Detection and Response

Most animals are fundamentally aerobic. Thus when the O2 levels in an animal’s tissues become unusually low, the low O2 levels typi- cally mean trouble. Animals detect low O2 levels—and respond to them—at two different scales. The mechanisms involved in detection and response are elaborate. Their elaborateness reflects the extreme importance of O2.

One scale of response to low O2 is that of the whole body: the scale of organ systems. In many types of animals, the O2 partial pressure in the circulating blood is monitored continuously, and if the blood O2 partial pressure falls, the function of the breathing system is modulated to reverse this trend. Water breathers, for example, commonly respond to a decreased blood O2 partial pressure by increasing their rate of gill ventilation. Air breathers may increase their rate of lung ventilation by breathing at a higher rate. Responses such as these—which we will discuss often in this chapter—help protect an animal’s cells from experiencing hypoxia.4

Hypoxia-inducible factors 1 and 2 (HiF-1 and HiF-2) are the most central players in the intracellular responses. They are closely related transcription factors, which bind with specific hypoxia-response elements (nucleotide base sequences) of DNA to activate gene transcrip- tion. In the last two decades there has been an explosion of knowledge regarding these transcription factors, which are implicated in many disease states as well as playing crucial roles in the ordinary lives of animals. HIF-1 is an ancient molecule, identified in inverte- brates as well as in all groups of vertebrates.

HIF-1 and HIF-2 increase in concen- tration in a cell when the cell experiences hypoxia, and they affect the transcription of dozens or hundreds of target genes, which have been identified through transcription profiling (transcriptomics) (see Chapter 3). HIF-1 and HIF-2 are different in their effectiveness in activating various genes in a tissue. Moreover, their target genes differ to some extent from tissue to tissue within a single species, and they also differ among species. Overall, HIF-1 and HIF-2 have extremely broad ranges of potential action, and many of their actions aid cells that are confronting hypoxia. In vertebrates they cause certain types of cells to increase secretion of erythropoietin, which enhances production of red blood cells (see Box 24.2). They also increase intracellular synthesis of several types of molecules, including enzymes of anaerobic glycolysis and a form of mitochondrial cytochrome oxidase that is particularly efficient in using O2. Besides these effects and many others, they also promoteangiogenesis, the development of new blood capillaries. The increase in capillaries shortens the average distance between tissue cells and

capillaries, thereby aiding O2 diffusion into the cells.
The basic manner in which the intracellular concentrations of these transcription factors are regulated is exemplified in FiguRE 23.6 using HIF-1. A complete HIF-1 molecule consists of α and β subunits. The β subunits are present regardless of cellular O2 level. Moreover, the α subunits are constantly being not only synthesized but also tagged for breakdown by the ubiquitin–proteasome system (see Figure 2.23). When the O2 level in a cell decreases, breakdown of α subunits is inhibited. Therefore the concentration of α subunits

The second scale of response is intracellular, in cells throughout the body. The intracellular responses are elicited if the rate at which the breathing and circulatory systems supply O fails to keep pace

Synthesis
of α subunits

Breakdown of α subunits

Low intracellular O2 inhibits break- down of α sub- units, thereby...

HIF-1

...promoting dimerization of
β subunits with
α subunits to form HIF-1.

2
with the rate of mitochondrial O2 utilization—resulting in cellular

HIF-1 enters the nucleus and combines with hypoxia- response elements in DNA.

hypoxia.

4 Hypoxia, as mentioned in Chapter 8, refers to an especially low level of O2 in tissues or cells.

FiguRE 23.6 Formation and action of HiF-1

α

β

α

β

Nuclear envelope

αβ

Hypoxia-response element

DNA

3.0

External Respiration 605

2.5

2.0

1.5

1.0

0.5

0.0

hif-1

hif-2

phd1 phd2 fih

Gene studied

to a major role for the HIF signaling system in allowing these people to succeed.

The two scales of response to low O2 that we noted at the start of this section in fact interact with each other. As already mentioned, for example, in vertebrates HIF-1 and HIF-2 play central roles in controlling the production of red blood cells. In this way, HIF-1 and HIF-2 help control the O2-carrying ability of each unit of volume of blood, which is a major factor at the scale of organ systems.

introduction to Vertebrate Breathing

The vertebrates living today are usually thought of, in a rough way, as representing an evolutionary sequence. In actuality, of course, today’s fish were not the progenitors of today’s amphibians, and today’s lizards (or other nonavian reptiles) were not the progenitors of today’s mammals and birds. Thus when we think of the sequence from fish to mammals and birds, caution is always called for in think- ing of it as an evolutionary sequence. Comparisons among today’s animals nonetheless often provide revealing insights into trends that occurred during evolution. Before we start our study of breath- ing in the various vertebrate groups, an overview of general trends will help place the individual vertebrate groups in a larger context.

One property of breathing organs that is of enormous impor- tance is the total surface area of the gas-exchange membrane. This area is typically an allometric function of body size among species within any one group of phylogenetically related vertebrates. The allometric relation differs, however, from one group to another, as seen in FiguRE 23.8A. To explore Figure 23.8A, let’s first focus on the lines for amphibians and reptiles other than birds. These lines are similar. Moreover, the lines for most groups of fish (e.g., toadfish and dogfish) are also similar. These similarities tell us two things. First, the total lung area of a nonavian reptile is roughly similar to the total lung area of an amphibian of the same body size. Second, the total gill area of a fish of particular body size is roughly similar to the total lung area of an amphibian or reptile of that size—sug- gesting that when vertebrates emerged onto land, there was not immediately much of a change in the area of the gas-exchange surface in their breathing organs. If we now turn our attention to the lines for mammals and birds, we notice that those groups, although independently evolved, are similar to each other. Moreover, they exhibit a dramatic step upward in the area of gas-exchange surface in their lungs by comparison with amphibians or nonavian reptiles. In brief, the mammals and birds independently evolved lungs with markedly enhanced gas-exchange surface areas—probably in association with their evolution of homeothermy. As we saw in Chapter 10, homeothermy increases an animal’s metabolic rate by a factor of at least four to ten. Thus lungs with an enhanced ability to take up O2 and void CO2 are required by homeothermic animals. Remarkably, tunas—noteworthy for being extremely active fish, as discussed at the opening of this chapter—have gill surface areas that approximate the lung surface areas of equal-sized mammals and birds!

The fact that mammals and birds have exceptionally large gas-exchange surface areas does not mean that they have large lungs compared with reptiles or amphibians. In fact, the opposite is often true. For example, if a rodent is compared with a like-size lizard, snake, or turtle, the lung volume of the reptile is likely to be

FiguRE 23.7 A genomic assessment of acclimation in the HiF signaling system Expression of five genes that code for compounds in the HIF signaling system was measured in the heart in two groups of epaulette sharks (Hemiscyllium ocellatum). One group lived continuously in aerated water.The other experienced eight

brief (2-h) episodes of hypoxic water over a period of 4 days. Expres- sion is measured on a relative scale. For each group, the upper and lower box limits correspond to the 75th and 25th percentiles of the data, the line in the box marks the median, and the bars extending from the box show the data range.The differences between the two groups were statistically significant for the hif-1 gene (which codes for HIF-1) and the phd2 gene. (After Rytkönen et al. 2012.)

rises, and more HIF-1 molecules are formed by dimerization of α and β subunits. The HIF-1 molecules enter the nucleus, where they bind with specific DNA sequences (the hypoxia-response elements), whHilcl hAinimtuarl Pnhcyosinoltorgoyl4gEene transcription.

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Some species of animals are well adapted to living in environ-

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ments where the ambient O level is prone to fall to low levels. For

Figure 23.07 12-16-15 1/12/16

2
example, the epaulette shark (Hemiscyllium ocellatum) lives in places

where it experiences periods of very low environmental O2. In a recent genomic study, researchers asked whether the HIF signaling system undergoes acclimation when fish that have been living in high-O2 water begin to experience low O2. One can reason that if a fish that’s been living in high-O2 water is about to confront a period of low environmental O2, the fish might profit by upregulating its HIF-1 signaling system, recognizing that it will depend on the HIF signaling system to help its tissues cope with the hypoxia they may soon experience. Using genomic methods, researchers measured the expression in the heart muscle of five genes that code for HIF-1 and other compounds in the HIF signaling system. Sharks that were exposed to a series of eight brief episodes of low O2 in their environment showed upregulation of expression of some of these genes, compared with sharks that lived in high-O2 water all the time (FiguRE 23.7).

Some human cultural groups live at high altitudes, where they steadily experience low atmospheric O2 concentrations. As we will discuss later in this chapter (see Box 23.2), recent evidence points

Relative messenger RNA expression

(A) Area of the gas-exchange membrane vs. body size

(B) Thickness of the gas-exchange membrane vs. body size

50,000

10,000 5000

1000 500

100

10 5

1 0.5

0.110

50 100
Body weight (g) on log scale

5000 10,000

10 50 100
Body weight (g) on log scale

5000 10,000

FiguRE 23.8 Total area and thickness of the gas-exchange membrane in the gills or lungs of vertebrates as functions of body size The lines for mammals and birds in both (A) and (B) and those for amphibians and reptiles other than birds in (A) are for many species (e.g., about 40 species of mammals, ranging in size from shrews to horses).The lines for fish in (A) are for various-sized individuals of single species.The thickness in (B) is the average dis- tance between the blood and the water or air. (After Perry 1990.)

at least five times greater than that of the rodent. Yet the surface area of the gas-exchange membrane is likely to be ten times greater in the rodent than in the reptile! The explanation for the high gas- exchange surface area in the lungs of a mammal or bird is that the lungs of these animals are extraordinarily densely filled with branching and rebranching airways, as we will see in this chapter. In nonavian reptiles and amphibians, in contrast, the lungs typi- cally have parts that are simply like balloons—little more than a sheet of tissue surrounding an open central cavity—and even the parts that are subdivided are much less elaborately subdivided than mammalian or avian lungs. Thus, whereas the lungs are large in a reptile compared with a rodent, they provide the reptile with a comparatively small area of gas-exchange membrane.

The thickness of the barrier between the blood and the envi-

ronmental medium also shows significant evolutionary trends in

the major vertebrate groups. In most fish, the sheet of gill tissue

between blood and water is roughly 5–10 μm thick. Vertebrate

lungs uniformly have a much reduced barrier between blood and

air (FiguRE 23.8B). Mammals tend to have a thinner sheet of tissue

Brown trout

Salmo trutta

Goldfish

Carassius carassius

Flatfish

Pleuronectes platessa

European eel

Anguilla anguilla

Mudpuppy

Necturus maculosus

Bullfrog (larva)

Rana catesbeiana

Bullfrog (adult)

Rana catesbeiana

Lungless salamander

Ensatina eschscholtzii

Boa constrictor

Constrictor constrictor

Southern musk turtle

Sternotherus minor

Red-eared turtle

Trachemys scripta

Green lizard

Lacerta viridis

Chuckwalla lizard

Sauromalus obesus

Big brown bat

Eptesicus fucus

Human

hom*o sapiens

beHtilwl eAenimbaloloPhdyasinodlogayir4tEhanlizards,crocodilians,orothernonavian Sinauer Associates

reptiles. To a dramatic extent, the tissue in birds is thinner yet,

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roughly 0.2 μm. Tunas, which are highly specialized for O2 uptake Figure 23.08 12-09-15

compared with most fish, have a blood–water barrier in their gills that is similar in thickness to the blood–air barrier in mammals.

0 10 20 30 40 50 60 70 80 90 100 Gas exchange through skin (%)

The skin varies widely in its role as a gas-exchange site in ver- tebrates (FiguRE 23.9). Some fish and most reptiles have evolved skinsthatpermitlittleO orCO exchange.Incontrast,theskin

FiguRE 23.9 The percentage of O2 and CO2 exchange that occurs across the skin in vertebrates The exact extent of skin breathing within a species often depends on environmental condi- tions (e.g., temperature). Some authorities place the bullfrog in the genus Lithobates. (After Feder and Burggren 1985.)

22
can be responsible for 25% or more of gas exchange in other fish, in

certain snakes and turtles, and in many amphibians; in the lungless salamanders, which not only lack lungs but have an epidermis that

500 1000

KEY

500 1000

Yellowfin tuna

Birds

Mammals

Dogfish

Reptiles other than birds

Amphibians Rainbow trout

Ray Toadfish

Dogfish

Rainbow trout

Lacerta

Toadfish

Croco

Yellowfin tuna

dile

lizard

Turtle

Monitor lizard

Mammals
Teju lizard

Birds

Snake

Area (cm2) on log scale

Thickness (μm) on log scale

Mammals Amphibians Birds Fish

Reptiles other than birds

O2 CO2

In the intact preparation, rhythmic motor impulses were detected in all the nerves studied.

(A) Intact

However, after the prepara- External Respiration 607 tion was severed into two
parts, the nerves posterior
to the cut went silent. FiguRE 23.10 A central pattern generator

(B) Severed

in the brainstem originates motor-neuron impulses that produce the breathing rhythm An isolated portion of the central nervous system of a neonatal rat, cut free from all connections with the rest of the animal, was used for this study. It included the brainstem and spinal cord. Recording electrodes were attached to two cranial nerves (hypoglossal and glossopharyngeal) and the ventral roots of three spinal nerves: C4 and C5 (C = cervical) and T6 (T = thoracic). Records show electrical activity as a function of time. (From Feldman et al. 1988.)

stops instantly, because the neuronal outputs from the brainstem are unable to travel to the breathing muscles by way of spinal nerves. Experiments that illustrate these vital points

Brainstem

When the preparation was severed into two parts, the cut was made here (equivalent to a high neck fracture).

Ventral roots of spinal nerves

Hypoglossal cranial nerve

Glossopharyngeal cranial nerve

C4 C5 T6

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5 sec

is vascularized (highly unusual), 100% of gas exchange occurs across the skin. Most mammals and birds resemble humans (see Figure 23.9) in relying almost entirely on their lungs. Among terrestrial vertebrates, the role of the skin in breathing is related to the skin’s desiccation resistance. Groups of terrestrial vertebrates that are well defended against water loss through their skin, such as mammals and birds, tend to exhibit little exchange of O2 or CO2 through their skin, whereas groups, such as frogs and salamanders, that are poorly defended against cutaneous water loss tend to engage in significant cutaneous breathing. Modifications that render the skin poorly permeable to water (see page 771) also make it poorly

have been carried out on the type of preparation shown at the left in FiguRE 23.10, consisting of the brainstem and spinal cord of a young rodent, isolated from the rest of the body. The medulla of the brain, isolated in this preparation from any sensory neuronal input, endogenously generates rhythmic bursts of ventilation-driving motor-neuron impulses that are detectable in multiple cranial and spinal nerves (see Figure 23.10A). However, if the spinal cord is severed (see Figure 23.10B), the spinal nerves posterior to the injury go silent, paralyzing the ventilatory muscles they service.5

Humans and most other mammals exhibit continuous breath- ing, meaning that each breath is followed promptly by another breath in a regular, uninterrupted rhythm. Birds and most fish also usually display continuous breathing. Lizards, snakes, turtles, crocodilians, amphibians, and air-breathing fish, in contrast, usually exhibit intermittent breathing, or periodic breathing, defined to be breathing in which breaths or sets of breaths are regularly interrupted by extended periods of apnea—that is, periods of no breathing. During intermittent breathing in these vertebrates, each period of apnea follows an inspiration. The lungs, therefore, are inflated during apnea. The glottis—the opening of the airways into the buccal cavity—is closed during apnea in the groups of vertebrates that display intermittent breathing. Because of this glottal closure, the inspiratory muscles can relax during the apnea without causing air to be expelled from the lungs.

Hill Animpael Prmhyesiaoblolgeyt4oEO2 and CO2. Sinauer Associates

The control of the active ventilation of the gills or lungs is the

final subject that deserves mention in introducing vertebrate breath-

Figure 23.10 12-09-15

ing. Of central importance is the control of the rhythmic muscle contractions that produce breathing movements, such as our own inhalation and exhalation movements. The muscles responsible for breathing movements in all vertebrates are skeletal muscles. They therefore require stimulation by motor neurons for each and every contraction they undergo. The breathing rhythm originates in sets of neurons that form central pattern generators (see Chapter 19); in a process called rhythmogenesis, these sets of neurons initiate rhythmic outputs of nerve impulses (action potentials) that travel to the breathing muscles and stimulate them into rhythmic pat- terns of contraction. The central pattern generators for breathing in all vertebrates are believed to be located in the brainstem: in the medulla, and sometimes other associated parts, of the brain. Although outside influences routinely play roles in controlling breathing, these central pattern generators are absolutely essential for creating the breathing rhythm. Accordingly, if a vertebrate’s spinal cord is severed just posterior to the brainstem, breathing

5 More information on rhythmogenesis is presented later in this chapter in the discussion of mammals.

608 Chapter 23 FiguRE 23.11 The branchial

breathing system in teleost (bony) fish (A) The lateral view shows the orientation of the gill arches under the operculum. (B and C) Consecutive enlargements show the structure of the gill array. (D) An enlarged view of a filament and three of the secondary lamel- lae on its upper surface (those

on the lower surface not shown), showing that blood flow within the secondary lamellae is counter- current to water flow across them. Blood flows in a sheet through each secondary lamella, as seen in the section of the foremost one. (After Hill and Wyse 1989.)

(A)

Operculum (covers gills)

(B)

Buccal cavity

Efferent filament vessel

Afferent filament vessel

Gill arch

Arch skeleton

Secondary lamellae

Gill arch

Lateral view

Gill arch Gill filament

Gill slit

Mouth

Horizontal section through head

Opercular cavity

Water flow

Buccal cavity

Opercular cavity

Operculum

Gill filaments

KEY

(C)

Gill arch

Water flow Blood flow

Efferent filament vessel

Afferent filament vessel

Secondary lamellae

Breathing by Fish

Gill filaments

Many fish start life as tiny larvae that breathe only by diffusion of gases across their general body surfaces (see Box 22.1). Because fish larvae lack specialized breathing organs, it can be easy to disregard these early stages in the study of breathing. However, gas-exchange insufficiencies are sometimes responsible for mass deaths of larvae. Thus the physiology of early diffusion–respiration stages can be of great importance ecologically and evolutionarily. As a young fish grows, its body becomes too thick for diffusion to suffice (see Box 22.1). At the same time, its gills develop and mature—as does its circulatory system, which is required for O2 from the gills to reach the rest of its body.

For our study of gill breathing, we focus here on teleosts, the

principal group of bony fish. The buccal cavity of a teleost com-

municates with the environment not only by way of the mouth

but also by way of lateral pharyngeal openings, the gill slits. The

gills are arrayed across these lateral openings, and a protective

external flap, the operculum, covers the set of gills on each side

of the head. Looking in detail at the structure of the gill apparatus,

there are four gill arches that run dorsoventrally between the gill

(D)

Secondary lamella

Water flow

Buccal cavity

Opercular cavity

Lamella opened to show blood flow inside

Afferent filament vessel

Blood flows through the secondary lamellae in the opposite direction.

Water flow

Water flows through the spaces between secondary lamellae from the buccal side to the opercular side.

Efferent filament vessel

slits on each side of the head (FiguRE 23.11A); the arches, which

collectively, the rows of filaments form a continuous array shaped like a series of Vs (VVVV) separating the buccal cavity on the inside from the opercular cavity on the outside. Each gill filament bears a series of folds, called secondary lamellae, on its upper and lower surfaces (FiguRE 23.11C); the lamellae run perpendicular to the long axis of the filament and number 10–40 per millimeter of filament length on each side. The secondary lamellae—which are richly perfused with blood and are thin-walled—are the principal sitesofgasexchange.

Hill Animal Physiology 4E
are reinforced with skeletal elements, provide strong supports for

the gills proper. Each gill arch bears two rows of gill filaments Morales Studio

splayedoutlaterallyinaV-shapedFaigrurraen2g3e.1m1en1t2-(0F9ig-1u5RE23.11B);

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Water flows along the surfaces of the secondary lamellae from the buccal side to the opercular side. Conversely, blood within the secondary lamellae flows in the opposite direction, as seen in FiguRE 23.11D. Countercurrent gas exchange, therefore, can occur along the gas-exchange membranes. The percentage of O2 extracted from ventilated water by resting teleosts has been reported to range from very high values of 80%–85% down to 30% or less; the latter values raise questions about the exact nature of gas exchange in the fish involved, because the values are lower than would be expected from effective countercurrent exchange.

gill ventilation is usually driven by buccal– opercular pumping

In general, water flow across the gills of a teleost fish is maintained almost without interruption by the synchronization of two pumps: a buccal pressure pump, which develops positive pressure in the buccal cavity and thus forces water from the buccal cavity through the gill array into the opercular cavity, and an opercular suction pump, which develops negative pressure in the opercular cavity and thus sucks water from the buccal cavity into the opercular cav- ity. The relative dominance of the two pumps varies from species to species; here we take a generalized view. We look first at the action of each pump separately and then at the integration of the pumps over the breathing cycle. It will be important to remember throughout that water flows from regions of relatively high pres- sure to ones of relatively low pressure.

THE BuCCAL PREssuRE PumP The stage is set for the buccal pressure pump to operate when a fish fills its buccal cavity with water by depressing the floor of the cavity while holding its mouth open. The lowering of the buccal floor increases the volume of the buccal cavity, thereby decreasing buccal pressure below ambient pressure and causing an influx of water. The mouth is then closed, and the buccal pump enters its positive-pressure phase. The fish raises the floor of the buccal cavity during this phase. This action increases the buccal pressure above ambient pressure and drives water from the buccal cavity through the gills into the opercular cavities. Thin flaps of tissue, which act as passive valves, project across the inside of the mouth opening from the upper and lower jaws. During the refilling phase of the buccal cycle, when buccal pressure is below ambient, these flap valves are pushed inward and open by the influx of water through the mouth. During the positive-pressure phase, however, the flap valves are forced against the mouth opening on the inside and help to prevent water from exiting the buccal cavity through the mouth.

THE OPERCuLAR suCTiOn PumP A teleost fish is able to ex- pand and contract its opercular cavities by lateral movements of its opercular flaps and other muscular actions. Running around the rim of each operculum is a thin sheet of tissue that acts as a passive valve, capable of sealing the slitlike opening between the opercu- lar cavity on the inside and the ambient water on the outside. The negative-pressure phase—suction phase—of the opercular pump occurs when the opercular cavity is expanded. At this time, the pressure in the cavity falls below the pressures in the buccal cav- ity and the ambient water. The negative pressure in the opercular cavity sucks water from the buccal cavity into the opercular cav-

Buccal cavity Oral valve

4

1

Gill array

Opercular cavity Opercular valve

Suction pump

2

External Respiration 609

– –––

–+

Pressure pump

FiguRE 23.12 The breathing cycle in teleost fish
minus (–) symbols indicate pressures relative to ambient pressure.The buccal and opercular pumps are represented by pistons. Blue arrows represent water flow. Arrows through the gill array indicate water flow over the gills. Stages ➋ and ➍ are transitional and short in duration. (After Hughes 1961, Moyle 1993.)

ity through the gill array. Water would also be sucked in from the environment were it not for the action of the opercular rim valve, which is pushed medially against the fish’s body wall by the higher ambient pressure, sealing the opercular opening and preventing influx of ambient water. After its sucking phase, the opercular pump enters its discharge phase. The cavity is contracted, raising the pressure inside to be higher than ambient pressure; this pres- sure difference forces the rim valve open and discharges water through the opercular opening.

Hill Animal Physiology 4E
inTEgRATiOn OF THE TwO PumPs PRODuCEs nEARLy COn-

TinuOus, uniDiRECTiOnAL FLOw The temporal integration Morales Studio

oFfigtuhre2b3u.1c2ca1l2a-n09d-1o5percular pumps is diagrammed in FiguRE 23.12. In stage ➊, the buccal cavity is being refilled. Expansion of the buccal cavity produces a pressure below ambient; therefore, if the buccal pump were the only pump, flow of water through the gills from the buccal side would not occur at this time, and in fact, there would be backflow through the gills into the buccal cavity because of the lowered buccal pressure. It is during stage ➊, how- ever, that the opercular pump is in its sucking phase. The pressure

3

+–

+++ +

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Plus (+) and

610 Chapter 23

in the opercular cavity is reduced to a level far below buccal pres- sure, and water is drawn through the gills from the buccal cavity. Stage ➋ is a short transition period in which the opercular pump is completing its sucking phase and the buccal pump is beginning its pressure phase. In stage ➌, the opercular pump is in its dis- charge phase, and the pressure in the opercular cavity is elevated. However, because the buccal pump is simultaneously in its pres- sure phase, the buccal pressure exceeds opercular pressure, and water again flows through the gills from the buccal cavity. Only in stage ➍, which occupies just a short part of the breathing cycle, is the pressure gradient in the direction favoring backflow of water through the gills. In all, therefore, the two pumps are beautifully integrated to produce almost continuous, unidirectional flow across the gills: The opercular pump sucks while the buccal pump is being refilled, and the buccal pump develops positive pressure while the opercular pump is being emptied.

many fish use ram ventilation on occasion, and some use it all the time

When a swimming fish attains a speed of 50–80 cm/s or greater, its motion through the water, if it holds its mouth open, can itself elevate the buccal pressure sufficiently to ventilate the gills at a rate adequate to meet O2 requirements. Many fast-swimming fish, in fact, cease buccal–opercular pumping when they reach such speeds and employ ram ventilation, which in theory lowers the metabolic cost of ventilation (because ventilation is achieved simply as a by-product of swimming). As mentioned at the start of this chapter, in ram ventilation the gills are ventilated by a swim- ming fish’s forward motion, and ventilation is therefore powered by the swimming muscles.

Tunas, mackerel, dolphinfish, bonitos, billfish (e.g., marlins), and lamnid sharks swim continuously and use ram ventilation all the time. In the tunas, at least, ram ventilation is obligatory, as already mentioned, because the buccal–opercular pumping mechanisms have become incapable of producing a sufficiently vigorous ventilatory stream.

Fish physiologists have long wondered whether the delicate structures of the gills might be thrown into disarray by the forces of high-speed water movement over the gills when powerful swim- mers such as tunas employ ram ventilation. Recently progress has been made in better understanding gill structure in these fish. The gills of tunas and some other powerful swimmers, it turns out, have evolved structural reinforcements (FiguRE 23.13). These structural specializations are believed to stabilize the geometry of the filaments and secondary lamellae when the gills are subjected to high-velocity water flow.

(A) Ordinary structure

and exercise are the major

Decreased O
stimuli for increased ventilation in fish

2

Fish are capable of as much as 30-fold changes in their rates of gill ventilation by buccal–opercular pumping. One potent stimulus to increase the rate of ventilation is a decrease in the partial pressure of O2 in the environment or blood, detected by chemoreceptor cells in the gills. Exercise also is a potent stimulus of ventilation in fish. Carbon dioxide, however, tends to be a relatively weak ventilatory stimulus in fish—in sharp contrast to mammals, in which ventilation is extremely sensitive to elevated CO2. The

(B) Specialized, structurally reinforced structure seen in tunas

Specialized tissue stabilizes the geometry of the secondary lamellae: the gas-exchange surfaces.

200 μm

FiguRE 23.13 specialized gill reinforcements in tunas Each part shows a longitudinal section through three vertically adjacent gill filaments on a single gill arch. For orientation, compare with Figure 23.11C. (A) The ordinary structure of the gills in teleost fish. (B) The specialized structure seen in parts of the gills of many species of tunas, in which tissue not only connects the outer ends of all the sec- ondary lamellae on each filament but also bridges the lamellae on one filament to those on the next adjacent filament. (After Wegner et al. 2013.)

question arises as to why CO2 plays such different roles in the two groups. The answer probably lies in the high solubility of CO2 in water (see Box 23.1 for a more rigorous treatment). Put loosely, for a water breather, although O2 can be difficult to acquire, CO2

Hill Animal Physiology 4E
is easy to excrete. As discussed earlier, water breathers never in-

Changes in the rate of ventilation are not the only means em- ployed by fish to adjust gill O2 exchange. Some fish, for example, exhibit lamellar recruitment, by which they adjust the proportion of the secondary lamellae that are actively perfused with blood. Whereas only about 60% of lamellae may be perfused at rest, 100% may be perfused during exercise or exposure to reduced O2.

several hundred species of bony fish are able to breathe air

Many species of bony fish have evolved mechanisms for tapping the rich O2 resources of the air. Nearly 400 species of air-breathing fish are known, especially in freshwater. Most retain functional gills and

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crease the CO partial pressure by much in the water passing over Morales Studio 2

tFhigeuireg2i3l.l1s3; the01re-2f1o-r1e6 CO2 is unlikely to be a sensitive indicator of their ventilatory status.

Secondary lamellae Gill filament Secondary lamellae

Water between two filaments

are dual breathers, acquiring O2 from both water and air. The extent to which these fish rely on the atmosphere depends on several factors. They typically increase their use of air as the level of dissolved O2 in their aquatic habitat falls. They also tend to resort increasingly to air breathing as the temperature rises, because high temperatures elevate their O2 needs. Notably, air-breathing fish typically void most of their CO2 into the water—across their gills or skin—even when relying on the atmosphere for most of their O2. What is the adaptive value of air breathing? The usual hypothesis is that air breathing arose in groups of fish that were living over evolutionary scales of time in O2-poor waters (see page 23), as a means of solving the problem of O2 shortage in the water (see also page 687).

Some air-breathing fish lack marked anatomical specializations for exploiting the air. American eels (Anguilla rostrata) are examples. They sometimes come out onto land in moist situations, and they then meet about 60% of their O2 requirement by uptake across their skin and 40% by buccal air gulping. Their gills, which are quite ordinary, are probably the primary site of O2 uptake from the air they gulp.

In most air-breathing fish, some part or branch of the alimen- tary canal has become specialized as an air-breathing organ. The specialized region varies greatly among species—reflecting the fact that air breathing has evolved independently more than 20 times. The specialized region is always highly vascularized, and its walls may be thrown into extensive patterns of evagin*tion or invagin*tion. In some species the buccal cavity is specialized for air breathing—as is true in electric eels (Electrophorus electricus), which have vast numbers of vascularized papillae on the walls of their buccal cavity and pharynx. The opercular cavities form air- breathing organs in some species; mudskippers (Periophthalmus), for example, breathe air using expanded gill chambers lined with vascularized, folded membranes. Many air-breathing species employ suprabranchial chambers, situated in the dorsal head above the gills. Quite a few air-breathing fish employ vascularized por- tions of the stomach to breathe. Others, notably species of armored catfish (family Callichthyidae), employ the intestine; in these, half or more of the intestinal length is highly vascularized and devoted to breathing from air that is swallowed and later expelled via the anus. The swim bladder (gas bladder) is used as an air-breathing organ by many fish. The “tinkering” aspect of evolution (see page 10) is nowhere better illustrated than in the fantastic diversity of body parts that fish have diverted from old functions to the task of getting O2 from the atmosphere.

The air-breathing organs of fish are most often inflated by buc- cal pumping. A fish takes air into its buccal cavity, then closes its mouth and compresses the buccal cavity. In this way, air is driven into its stomach, swim bladder, or other air-breathing structure.

A potential problem for air-breathing fish is that O2 taken up from the atmosphere may be lost to O2-poor water across their gills! This possibility probably helps explain why the gills of these animals are often reduced in comparison with those of other fish. In extreme cases, the gills are so atrophied that air breathing is obligatory—as is true of electric eels, which drown if they cannot obtain air. Many air-breathing fish have also evolved specialized circulatory shunts by which oxygenated blood can bypass the gas-exchange surfaces of their gills, thereby limiting O2 loss across the gills.

Of all air-breathing fish, the six species of lungfish (dipnoans) (FiguRE 23.14A) have received the most attention because they

External Respiration 611 (A) An African lungfish in the genus Protopterus

(B) The inner wall of a lungfish lung

FiguRE 23.14 Lungfish and their lungs
African lungfish (genus Protopterus); two other genera of lungfish occur in South America and Australia. (A) Protopterus dolloi. (B) The inner wall of part of a lung of Protopterus aethiopicus.The respiratory surface area of the lung is greatly enhanced by a complex pattern of vascularized folds.The side compartments in the wall of the lung open to a central cavity that runs the length of the lung.The cavity communicates anteriorly with a short pulmonary canal leading to the esophagus. (B from Poll 1962.)

are believed to be the modern fish that most closely resemble the

ancestral fish that gave rise to terrestrial vertebrates. The walls of

the lungs of lungfish (FiguRE 23.14B) are thrown into complex

arHraillysAonfiminatlePrchoysnionloegcyte4dEfolds—withthefoldsarrangedroughlyin Sinauer Associates

tiers from low folds to high folds—resembling the walls of many

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amphibian lungs. Why are the air-breathing organs of lungfish

Figure 23.14 12-09-15

called lungs, and why are the fish themselves named lungfish? These names arose decades ago because the air-breathing organs were viewed as being “particularly hom*ologous” to the lungs of terrestrial vertebrates. Many morphologists now conclude, however, that swim bladders could just as justifiably be called lungs by this standard. To a physiologist, all invagin*ted breathing organs are lungs (see Figure 23.2), and thus all of the air-breathing organs of fish are lungs.

This figure features

612 Chapter 23

(A) Salamander larva with gills

Gills

(B) Frog lungs

Glottis Larynx

Bronchus

Lungs

Partitions on inner wall of lung

Breathing by Amphibians

Amphibians, of all the vertebrate groups, mix water and air breath- ing to the greatest extent. Many move from an aquatic environment to a terrestrial one during their individual development, and many are dual breathers as adults.

The gills of aquatic amphibian larvae (tadpoles) are of differ- ent origin and structure than the gills of adult fish. They develop as outgrowths of the integument of the pharyngeal region and project into the water from the body wall (FiguRE 23.15A). The gills are external in all young amphibian larvae; in salamander larvae they remain so, but in the larvae of frogs and toads (an- urans), an outgrowth of the integument, termed the operculum (different from the bony operculum of a fish), soon encloses the gills in a chamber that opens to the outside posteriorly. Ventila- tion of the gills enclosed in the opercular cavity is accomplished by buccal pumping. The gills of amphibians are generally lost at metamorphosis, but external gills remain throughout life in certain aquatic salamanders, such as mudpuppies (Necturus). Mudpuppies ventilate their gills by waving them back and forth in the water and increase the frequency of these movements in response to decreased O2 or increased temperature.

In most amphibians, paired lungs develop from the ventral wall of the pharynx near the time of metamorphosis. Each lung is classified as unicameral (uni, “one”; cameral, “chamber”) because it is a single sac with an open, undivided central cavity that provides access to any side compartments that may be formed by the fold- ing of the walls. The lungs of many adult amphibians are simple, well-vascularized sacs; their internal surface area is increased little, if at all, by folding, and in this respect they are less well developed than the lungs of lungfish. The inner walls of the lungs of frogs and toads are often more elaborate; they may be thrown into complex

patterns differing in detail have been reported, the essentials

FiguRE 23.15 Breathing organs of amphibians
nal gills of a 3-week-old salamander larva (Ambystoma maculatum). (B) The lungs of a frog (Rana temporaria).The dorsal half of one lung has been cut off to reveal the compartmentalization of the inner wall by interconnected folds in multiple tiers. Modern amphibians lack a trachea; their lungs connect almost directly to the pharynx. (B after Poll 1962.)

patterns of interconnected folds in multiple tiers, giving them a honeycombed appearance (FiguRE 23.15B).

Lunged amphibians fill their lungs by buccopharyngeal pres-

sure. This basic mechanism is presumably carried over from their

piscine ancestors and, as mentioned earlier, is often employed by

amphibian larvae to ventilate their gills. In frogs, although several

Hill Animal Physiology 4E
of the buccopharyngeal pressure pump are uniform. Air is taken

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into the buccal cavity through the nares or mouth when the pressure

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inFtighuerec2a3v.i1t5y is12re-0d9u-1c5ed by lowering its floor. Then, when the floor

of the buccal cavity is raised with the mouth closed and the nares at least partially sealed by valves, the increase in pressure forces air into the lungs. The inflation of the lungs elevates the air pressure within them. Thus the lungs would discharge upon opening of the mouth or nares were it not for the glottis (see Figure 23.15B), which is closed by muscular contraction after inhalation. A period of apnea (no breathing), with the lungs inflated, then follows (i.e., breathing is intermittent). The nares are opened during the apneic period, and a frog often pumps air in and out of its buccal cavity through its nares at that time by raising and lowering the floor of the buccal cavity, termed buccopharyngeal pumping. Then the glottis is opened, and air from the lungs is exhaled.

Exhalation in a frog results in part from elastic recoil of the expanded lungs and may also be promoted by contraction of muscles in the walls of the lungs and body wall. Exhalation is described as having both passive and active components. In the study of the forces that drive lung volume changes, passive means “not involving contraction of muscles” and refers to forces developed by simple elastic rebound. Active, by contrast, refers to forces developed by muscular contraction.

(A) The exter-

CO2 excretion (%) O2 uptake (%)

Naris

Glottis

External Respiration 613

12
3

Lung

In tadpoles, gills and skin each account for about half of O2

FiguRE 23.16 The three major steps in the ventilatory cycle of an adult bullfrog (Rana catesbeiana) Some authorities name this species Lithobates catesbeianus. (After Gans 1970.)

The bullfrog (Rana catesbeiana) provides a well-studied specific example of the pulmonary breathing cycle. A bullfrog fills its buccal cavity in preparation for inflation of its lungs before it empties its lungs; to do so, with its glottis closed, it inhales air, which mostly comes to lie in a posterior depression of the buccal floor (step ➊, FiguRE 23.16). Next (step ➋), the glottis is opened, and pulmonary exhalant air passes in a coherent stream across the dorsal part of the buccopharyngeal cavity to exit through the nares. The fresh air in the depression of the buccal floor is then driven into the lungs when the buccal floor is raised with the nares closed (step ➌). An important effect of the buccopharyngeal pumping between breaths is that it washes residual pulmonary exhalant air out of the buccal cavity, so that when the next pulmonary ventilatory cycle begins, the buccal cavity is filled with a relatively fresh mixture.
Hill Animal Physiology 4E

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gMoilrlasle,sluStnudgios, and skin are used in various combinations to achieve gas exchange Figure 23.16 12-09-15

A central question in amphibian respiratory physiology is how the total gas exchange of an individual is partitioned among the available gas-exchange sites: the gills, lungs, and skin. Bullfrogs, to continue with them as an example, start their lives without lungs, and when they are living at 20°C as aquatic tadpoles, their gills and skin each account for about half of their O2 and CO2 exchange (Fig- uRE 23.17). As bullfrog tadpoles mature and their lungs become functional, their lungs gradually assume primary responsibility for their O2 uptake. In adulthood, the lungs take up most O2. The lungs, however, do not play a large role in CO2 exchange at any age; instead, when the gills are lost at metamorphosis, the skin increases its role in eliminating CO2 (see Figure 23.17). The pattern seen in adult bullfrogs at 20°C—that the lungs are primarily responsible for O2 uptake, whereas the skin eliminates most CO2—is common in amphibian adults at such temperatures.

Some species of frogs in temperate regions of the world hibernate at the bottoms of ponds and lakes during winter. All their O2 and CO2 exchange is then across their skin. One reason the skin can suffice under these circ*mstances is that the hibernating animals have very low needs for O2 and CO2 exchange because of their low body temperatures and seasonal metabolic depression. The relatively high permeability of the skin is also important: Whereas it increases rates of dehydration on land, it makes underwater breathing by adults possible.

100 80 60 40 20

100

80

60

40

20

In adult frogs, the lungs take up most O2...

...but the skin eliminates most CO2.

Postmetamorphic
Adults froglets
Gills resorbed,
lungs well
developed, tail
being resorbed

Aquatic tadpoles
Air-breathing Gills well
tadpoles developed, lungs
Gills well developing but
developed, lungs nonfunctional
developed and used, hindlimbs emerging

FiguRE 23.17 The development of external respiration in the bullfrog (Rana catesbeiana) Shown are the percentages of O2 uptake and CO2 excretion that occur across the gills, lungs, and skin of bullfrogs as they develop from tadpoles to adults.The animals were studied at 20°C and had free access to well-aerated water and air. Some authorities name this species Lithobates catesbeianus. (Af- ter Burggren and West 1982.)

Breathing by Reptiles Other than Birds

When we consider the lizards, snakes, turtles, and crocodilians, an

important first point to make is that in most of them, the lungs take

up essentially all O2 and eliminate essentially all CO2. The skin

of reptiles is generally much less permeable than amphibian skin,

meaning that it protects far better against evaporative dehydration, Hill Animal Physiology 4E
but it does not readily allow the respiratory gases to pass through. Sinauer Associates
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The simplest type of reptilian lung—seen in most lizards and sFnigaurkee2s3—.1i7su1n2i-c0a9m-1e5ral(single-chambered);itisasaclikestructure with an open central cavity. Unicameral lungs are sometimes

well perfused with blood throughout, but sometimes they are well perfused only at the anterior end and are balloonlike at the posterior end (FiguRE 23.18A). In the well-perfused parts where O2 and CO2 are principally exchanged with the blood, the walls are thrown into a honeycomb-like pattern of vascularized folds, increasing their surface area (FiguRE 23.18B,C). Air flows in and out of the central cavity during breathing, but gas exchange between the central cavity and the depths of the honeycomb-like cells on the walls is probably largely by diffusion.

A major evolutionary advance observed in several groups of nonavian reptiles is that, in each lung, the main lung cavity has become subdivided by major septa into numerous smaller parts, forming a multicameral—multiple-chambered—lung, as seen in FiguRE 23.18D. A multicameral lung can provide a great deal more

614 Chapter 23
(A) Unicameral lungs of a plated lizard

Some unicameral lungs are perfused with blood principally at just the cranial (anterior) end.

(B) A unicameral lung in a lacertid lizard

(C) Scanning electron micrograph of the wall of a tegu lizard lung

(D) The elaborate, multicameral lung of a monitor lizard

A bronchus allows air to flow to the multiple cham- bers of this type of lung.

surface area of gas-exchange membrane per unit of lung volume than

a unicameral lung because the septa between lung chambers, not just

the outer walls, can develop elaborate, highly folded gas-exchange

surfaces. The multicameral type of lung occurs in monitor lizards (see

Hill Animal Physiology 4E
Figure 23.18D), reptiles noted for their dramatically active ways of life

FiguRE 23.18 Lizard lungs (A) Freshly dissected unicameral lungs from an African plated lizard (Gerrhosaurus sp.). Blood trapped within the tissue is responsible for the red color.The highly localized presence of blood at the cranial (anterior) ends of the lungs re- flects the fact that virtually all perfusion takes place within the cranial portions of the lungs in some species with unicameral lungs. (B) A drawing of the gross internal structure of the unicameral lung of another type of lizard, the green lizard (Lacerta viridis). (C) Scanning electron micrograph of the lung wall of a tegu lizard (Tupinambis nigropunctatus), showing the honeycomb-like pattern of vascularized partitions. Magnification: 25×. (D) Gross internal structure of the highly developed multicameral lung of a monitor lizard (Varanus exanthe- maticus). (A courtesy of Tobias Wang; B and D courtesy of Hans-Rainer Duncker, reprinted from Duncker 1978; C courtesy of Daniel Luchtel and Michael Hlastala.)

and turtles. These groups all resemble each other in their septation, in that—when viewed in three dimensions—each lung is divided into three rows of chambers, with four or more chambers in each row. A noteworthy evolutionary development in the multicameral lung is the appearance of a cartilage-reinforced tube (bronchus) that runs lengthwise through the lung (see Figure 23.18D). This tube allows air to flow to all of the multiple chambers in the lung.

During ventilation the lungs in nonavian reptiles are filled principally or exclusively by suction (also termed aspiration) rather than by buccal pressure: Air is drawn into the lungs by an expan- sion of the lung volume, which creates a subatmospheric pressure within the lung chambers. This mode of ventilation represents a major evolutionary transition from the earlier buccal-pressure–filled lungs of air-breathing fish and amphibians. It is a transition that is carried forward to the mammals and birds, which also employ suction to fill their lungs. Because suction is created by the action of thoracic and abdominal muscles, not by buccal muscles, the evolution of suction ventilation liberated the buccal cavity from one of its ancient functions, allowing it to evolve in new directions without ventilatory constraints.

Suction is developed in the lungs of reptiles in two different ways. In one sort of breathing cycle, seen in at least some snakes, thoracic and abdominal expiratory muscles compress the lungs to a volume smaller than their passive relaxation volume during the exhalation of air; suction for inhalation is then developed when the lungs later rebound elastically to larger size. In the other sort of breathing cycle, seen in lizards and some crocodilians, inspiratory muscles actively create suction in the lungs during inhalation by expanding the lungs to a size larger than their passive relaxation volume; then, when the muscular activity stops, the lungs rebound elastically, becoming smaller, and the elastic rebound contributes to exhalation.

Lizards provide an instructive example to study in more detail. Unlike modern amphibians, lizards have well-developed ribs. Running over and between the ribs on each side of the body are intercostal muscles (costa, “rib”) that—by means of their contrac- tions—can expand or contract the volume enclosed by the rib cage. When a resting lizard inhales, certain of its intercostal muscles are activated and expand the rib cage, a mechanism sometimes called the costal suction pump. After the inflation of the lungs has oc- curred, the glottis is closed and the inspiratory muscles relax. The inhaled air is then held in the lungs for several seconds to several minutes of apnea, while often the buccal cavity is ventilated by buccopharyngeal pumping, thought generally to aid olfaction. Exhalation then occurs, followed quickly by another inhalation.

Recent research has demonstrated that when lizards are walk- ing or running, some of their intercostal muscles help produce the back-and-forth flexions of the body that are so characteristic of lizard

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and relatively high aerobic competence. It is also found in crocodilians

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Figure 23.18 12-09-15

locomotion. This involvement of the intercostals in locomotion can interfere with their ability to develop ventilation forces. Some, but not all, species of lizards overcome this problem by using buccal pressure to help fill their lungs while they are walking or running.

Sea turtles and some crocodilians exhibit the most structurally elaborate lungs seen in the nonavian reptiles.

Breathing by mammals

Mammals and birds possess the most elaborate lungs of all animals. Their lungs are independently evolved and built on very different principles. The extreme intricacy of mammalian lungs is illustrated by the plastic cast of a person’s airways shown in FiguRE 23.19.

The lung system of an adult human consists of 23 levels of airway branching. The trachea first branches to form two major airways, the primary bronchi (singular bronchus), which enter the two lungs (see Figure 23.19). Each primary bronchus then branches and rebranches dendritically (as a tree branches) within the lung, giving rise to secondary and higher-order bronchi of smaller and smaller diameter, and then to ever-smaller fine tubes known as bronchioles. At the outer limits of this branching tree of airways, 23 branches away from the trachea, the final bronchioles end

External Respiration 615 (A) The finest airways of the mammalian lung, ending in alveoli

The terminal bronchioles, with diameters of 0.5 mm or less in humans, are the final branches of the conducting (nonrespiratory) airway system.

Terminal bronchiole

Respiratory bronchioles

Alveoli first appear along the respiratory bronchioles and form a continuous lining along the alveolar ducts and sacs.

Alveolar duct

(B) Scanning electron micrograph of an alveolar region in a human lung

Alveolus

Alveolar sac

The walls of the alveoli are richly invested with blood capillaries.

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The trachea divides here to give rise to two major airways, the primary bronchi, that enter the two lungs.

A

D

The lung on the left shows only the

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Pulmonary artery

Pulmonary vein

100 μm

FiguRE 23.19 Human lungs
airways, whereas the lung on the right shows the airways and blood vessels. Note the large sizes of the major blood vessels, reflecting the high rates at which blood must flow through the lungs.To visualize the airways, the lung passages were injected with a yellow plastic. Similarly, the arteries and veins were injected with red and blue plas- tic, respectively. After the plastic hardened, the tissue was removed, leaving just the plastic to mark the airways and blood vessels. Only the airways and vessels of relatively large diameter are preserved with this technique:The airway system and the arterial and venous systems branch far more finely than seen here. Note that the arteries and veins tend to branch in parallel with the airways. (Courtesy of Ewald R. Weibel, Institute of Anatomy, University of Berne, Switzerland.)

FiguRE 23.20 Respiratory airways of the mammalian lung (A) Longitudinal section of the final branches of the airways in a mammalian lung, showing respiratory bronchioles, alveolar ducts, alveolar sacs, and alveoli. (B) Scanning electron micrograph of a 0.4-mm2 area of a human lung, showing alveolar ducts (D) and alveoli (A). (A after Hildebrandt and Young 1960; B courtesy of Ewald Weibel.)

blindly in alveolar ducts and alveolar sacs, the walls of which are composed of numerous semispherical outpocketings, each called an alveolus (alveolus, “hollow cavity”) and collectively termed alveoli (FiguRE 23.20). The structure is so elaborate that describing it quantitatively is a great challenge, and estimates still undergo revision. According to the latest values, as summarized

Hill Animal Physiology 4E
by Ewald Weibel, there are almost 500 million alveoli in the two

The trachea and bronchi and all but the last few branches of bronchioles in a mammal’s lungs are not much involved in gas exchange; they are thus known as the conducting airways and are said to constitute the anatomical dead space of the lungs.

lungs (taken together) of a human adult; they vary in size but

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average about 0.25 mm in diameter. The alveoli make up a total Figure 23.20 12-09-15 2

area of gas-exchange membrane averaging about 130 m ! The floor of an 80-student classroom is likely to have a similar area. Thus, by virtue of elaborate branching, a highly vascularized interface between air and blood that is the size of a large classroom floor is fit within the compact volume occupied by our lungs.

616 Chapter 23

They are lined with a relatively thick epithelium and do not receive a particularly rich vascular supply. Gas exchange between air and blood occurs in the respiratory airways of the lungs (see Figure 23.20A), which consist of respiratory bronchioles (the last two or three branches of bronchioles), alveolar ducts (through-passages lined with alveoli), and alveolar sacs (end sacs lined with alveoli). The pulmonary walls of the respiratory airways are composed of a single layer of thin, highly flattened epithelial cells and are richly supplied with blood capillaries. The alveoli constitute most of the gas-exchange surface. In them, blood and air are separated by just two thin epithelia (the pulmonary alveolar epithelium and the capillary epithelium) and a basem*nt membrane in between. The total average diffusive thickness of these structures is only 0.3–0.6 μm. Recent research indicates that type IV collagen in the basem*nt membrane is critical for imparting mechanical strength to these very thin structures: strength adequate to prevent them from rupturing, despite the fact that they are exposed to consider- able physical stresses during breathing.

The total lung volume is employed in different ways in different sorts of breathing

When mammals breathe at rest, they do not come close to inflating their lungs fully when they inhale, and they do not come close to deflating their lungs fully when they exhale. Thus a wide margin exists for increasing the use of total lung volume. The tidal vol- ume is the volume of air inhaled and exhaled per breath. In rest- ing young men, the volume of the lungs at the end of inhalation is about 2900 mL, whereas that at the end of exhalation is about 2400 mL. Thus the resting tidal volume is about 500 mL (FiguRE 23.21). The maximum volume of air that an individual can expel

beyond the resting expiratory level is termed the resting expira- tory reserve volume. In healthy young men, it is about 1200 mL; that is, of the 2400 mL of air left in the lungs at the end of a resting exhalation, 1200 mL can be exhaled by maximum expiratory ef- fort, but 1200 mL (termed the residual volume) cannot be exhaled at all (see Figure 23.21). The maximum volume of air that can be inhaled beyond the resting inspiratory level is the resting inspira- tory reserve volume. In healthy young men, it is about 3100 mL; thus the total lung volume at the end of a maximum inspiratory effort is about 6000 mL (see Figure 23.21). Using the terminology developed here, when mammals increase their tidal volume above the resting level, they do so by using parts of their inspiratory and expiratory reserve volumes. The maximum possible tidal volume, sometimes termed vital capacity, is attained by fully using both reserves and thus is the sum of the resting tidal volume and the resting inspiratory and expiratory reserve volumes: about 4800 mL in young men. The vital capacity of humans tends to be increased by physical training, but advancing age and some diseases tend to decrease it.

The gas in the final airways differs from atmospheric air in composition and
is motionless

The gas in the alveoli, which is the gas that undergoes exchange with the blood, differs dramatically in composition from atmo- spheric air in all mammals. The most fundamental reason is that the alveolar sacs form the blind ends of tidally ventilated airways that are never fully emptied. To see the implications of this ana- tomical fact, consider a resting person. At the end of a resting exhalation, the lungs contain 2400 mL of stale air, about 170 mL of which is in the anatomical dead space (the conducting airways). When the person then inhales, the stale air in the anatomical dead space moves deeper into the lungs, into the respiratory airways, meaning that the entire 2400 mL of stale air is in the respiratory airways after inhalation. Of the 500 mL of fresh atmospheric air inhaled during a resting breath, about 330 mL passes through the anatomical dead space and enters the respiratory airways; the other 170 mL—the last of the air to be inhaled—simply fills the anatomical dead space and is later exhaled, unused. All things considered, at the end of a resting inhalation, the gas in the respiratory airways consists of a mix of 2400 mL of stale air and 330 mL of fresh atmospheric air. Accordingly, the O2 partial pressure in the alveoli is bound to be far below the atmospheric O2 partial pressure, and the CO2 partial pressure in the alveoli is far above the atmospheric partial pressure. Another significant property that arises from these quantitative realities is that the gas partial pressures in the alveoli do not change much between inhalation and exhalation. Using the values for resting humans, only about 12% of the air in the respiratory airways at the end of an inhalation is fresh, whereas 88% is carried over from previous breaths. The large carry-over from breath to breath helps impart stability to the gas composition deep in the lungs.

The exact partial pressures of gases that prevail in the alveoli depend dynamically on the rate at which fresh air is brought into the depths of the lungs and the rate of gas exchange with the blood. Ventilatory control systems (to be discussed later) ordinarily adjust the rate of ventilation relative to the rate of gas exchange with the

Vital capacity (4800 mL)

6 5 4 3 2

1

0 Volume (L)

Volume attained by maximum inspiratory
effort (6000 mL)

Volume at the end of resting inspiration (2900 mL)

Volume at the end of resting expiration (2400 mL)

Volume attained by maximum expiratory effort (1200 mL)

Inspiratory reserve volume (3100 mL)

Resting tidal volume (500 mL) Expiratory reserve volume

(1200 mL)

Residual volume (1200 mL)

FiguRE 23.21 Dynamic lung volumes in healthy young adult men The lung volumes shown include the anatomical dead space as well as the respiratory airways.The inspiratory and expiratory re- serve volumes shown are the reserves available during resting breath- ing.The residual volume is the volume remaining in the lungs after maximum expiratory effort.Values shown are averages for 70-kg men.

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Alveolus

FiguRE 23.22 mechanisms of gas transport in the final branches of mammalian lungs during inhalation Although gases are drawn by convection (bulk flow) into the finest bronchioles, the gases in the alveolar sacs and alveoli are motionless.Therefore O2 must travel by diffusion across the final, very short distance it must cover to reach the gas-exchange membrane, and CO2 must diffuse in the opposite direction. (After Weibel 1984.)

blood so that certain set-point partial pressures of O2 and CO2 are maintained in the alveolar gas. In humans near sea level, the partial pressure of O2 in alveolar gas is nearly always about 13.3 kPa (100 mm Hg), and that of CO2 is about 5.3 kPa (40 mm Hg).6

The gas occupying the final respiratory airways of a mammal is

essentially motionless (FiguRE 23.22). This unexpected property

is still another consequence of the anatomical fact that the alveolar

sacs are the blind ends of a tidally ventilated airway system. Dur-

ing inhalation, convective air movement carries air rapidly down

the trachea and through the various bronchi. As the air flows ever

deeper into the lungs, however, it slows, because the collective

volume of the airways rapidly increases as the airways branch into

Hill Animal Physiology 4E
greater and greater numbers. Convective airflow ceases before the

air reaches the alveolar sacs.

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FiguBrec2a3u.2s2e t1h2e-0g9a-s15in the blind ends of the airways is motionless,

O2 and CO2 transport through that gas must occur by diffusion (see Figure 23.22). The layer of motionless gas is very thin (recall, for instance, that human alveoli average only 0.25 mm in diameter). Therefore diffusion across the motionless layer of gas can readily occur fast enough for rates of O2 and CO2 exchange between the lung air and the blood to be adequate (see Table 5.1). This happy situation is contingent, however, on the alveoli being filled with gas, not water. If the alveoli become filled with body fluid, rates of diffusion sharply plummet. That is why any disease that causes even a minute chronic accumulation of body fluid within the airways is a mortal threat.

6 There are some data that indicate that these values vary with body size among species of mammals, and a partial explanation for this pattern would be the regular relation between breathing rate and body size. Small- bodied mammals take many more breaths per minute than large-bodied ones (see Chapter 7). Correlated with this potentially greater influx of fresh air relative to lung volume, mammals smaller than humans may have consistently higher values for the alveolar partial pressure of O2 than humans (e.g., 14.5 kPa measured in rats). Conversely, mammals larger than humans may have lower values than humans (e.g., 10 kPa in horses).

KEY

Convection (bulk flow)

Diffusion through motionless air

External Respiration 617

Terminal bronchiole

The forces for ventilation are developed by the diaphragm and the intercostal and abdominal muscles

Unlike other vertebrates, mammals have a true diaphragm: a sheet of muscular and connective tissue that completely separates the thoracic and abdominal cavities (see Figure 1.18). The diaphragm is dome-shaped, projecting farther into the thorax at its center than at its edges. Contraction of the diaphragm tends to flatten it, pulling the center away from the thorax toward the abdomen. This movement increases the volume of the thoracic cavity, resulting in expansion of the lungs and inflow of air by suction.

The external and internal intercostal muscles that run obliquely between each pair of adjacent ribs are also important in ventilation. Contraction of the external intercostals rotates the ribs anteriorly and outward, expanding the thoracic cavity. The contractile filaments of the internal intercostals run (roughly speaking) per- pendicular to those of the externals, and in general their contraction rotates the ribs posteriorly and inward, decreasing the volume of the thoracic cavity. You can easily demonstrate the action of these muscles on yourself by consciously expanding and contracting your rib cage while monitoring your ribs with your fingers.

To fully understand ventilation, it is essential to recognize that the lungs and thoracic wall together form an elastic system. Much like a hollow rubber ball with a hole on one side, they assume a certain equilibrium volume, known as their relaxation volume, if they are free of any external forces. For the volume of the lungs to deviate from the relaxation volume, muscular effort must be exerted. In adult human males, the relaxation volume of the lungs, measured as the volume of gas they hold at relaxation, is about 2400 mL. This volume is the same as that of the lungs after a resting exhalation (see Figure 23.21): The lungs and thorax are in their relaxed state after a resting exhalation.

Inhalation in humans at rest is active (meaning that it entails muscular effort). During inhalation, the lungs are expanded to greater than their relaxation volume by contraction of the diaphragm, external intercostal muscles, and anterior internal intercostals. Mammals do not close the glottis during ordinary breathing. Thus inhalation continues only as long as the inspiratory muscles contract. Exhalation in resting humans is largely or completely passive (meaning that it does not entail muscular effort). When the inspiratory muscles cease to contract at the end of inhalation, lung volume returns elastically to its passive equilibrium state: the relaxation volume.

When mammals exercise, they typically increase not only their tidal volume but also their breathing frequency. Additional muscular activity is required, therefore, both to amplify changes in lung volume during each breath and to hasten the inspiratory and expiratory processes. In people, the external intercostal muscles assume a greater role in inhalation during exercise than they do during rest; whereas expansion of the rib cage by these muscles during quiet breathing is of relatively minor importance compared with the action of the diaphragm, expansion of the rib cage by the external intercostals during heavy exertion accounts for about half of the inspiratory increase in lung volume. Active forces also contribute to exhalation in people during exercise. The most im- portant muscles in exhalation are the internal intercostals, which actively contract the rib cage, plus the muscles of the abdominal wall, which contract the abdominal cavity, forcing the diaphragm

618 Chapter 23

upward into the thoracic cavity. These muscles hasten exhalation during exercise and may also compress the lungs beyond their relaxation volume, thereby enhancing tidal volume by use of some of the expiratory reserve volume.

Although all mammals tend to use the same basic groups of muscles for ventilation, the relative importance of the muscle groups varies. In large quadrupeds, for example, movements of the rib cage tend to be constrained, and the diaphragm bears especially great responsibility for ventilation.

The control of ventilation

We can think of ventilation as consisting of a rhythm—inhalation alternating with exhalation—that is modulated from time to time to meet changing demands for O2 and CO2 exchange.

A kEy siTE OF ORigin OF THE VEnTiLATORy RHyTHm is THE PRE-BöTzingER COmPLEx The location of the specific neu- rons that are most important for rhythmogenesis—generation of the breathing rhythm—is now well established. These neurons are found in a bilaterally arrayed pair of neuron clusters, called the pre-Bötzinger complex, within the ventrolateral medulla of the brainstem. Thin medullary tissue slices containing the pre- Bötzinger complex—slices that are entirely isolated from the rest of the body—endogenously produce neural outputs that control the routine breathing rhythm and that evidently also play roles in con- trolling sighs (FiguRE 23.23). A question that remains is whether the central pattern generator in the pre-Bötzinger complex can, in itself, produce the fully formed rhythmogensis observed in intact animals. Current evidence indicates it must interact with one or more additional, nearby central pattern generators to achieve this.

VEnTiLATiOn is mODuLATED By CHEmOsEnsATiOn OF CO2, H+, AnD O2 As briefly mentioned earlier, the partial pressures of

O2 and CO2 in alveolar gas are ordinarily held at set-point levels under a wide range of functional states. In humans at rest, for ex- ample, the alveolar O2 partial pressure is 13.3 kPa (100 mm Hg), and the CO2 partial pressure is 5.3 kPa (40 mm Hg). These partial pressures remain the same during light to moderately intense exercise. Only during heavy exertion do the gas partial pressures in the alveoli deviate more than slightly from the resting values. To explain the stability of alveolar gas composition, ventilatory controls based on chemosensation of CO2, H+, and O2 are critical, although they are not the only important controls of ventilation.

Controls based on sensation of CO2 and H+ are the most potent chemosensory controls of ventilation in mammals. When the concen- tration of CO2 in the blood or other body fluids rises, the concentration of H+ typically increases in parallel, and vice versa (see page 659).7 Thus the blood concentrations of CO2 and H+ vary together. The blood concentrations of both CO2 and H+ are independently sensed by chemosensitive neural zones near the ventral surface of the medulla (the retrotrapezoid nucleus being of particular importance). A deviation of either concentration from its normal level potently influences breathing, and because both concentrations tend to vary together, they often exert synergistic effects. Ventilation increases or decreases so as to bring the concentrations of CO2 and H+ back toward normal—a negative feedback system. For example, if the CO2 concentration of the blood is elevated, ventilation is increased, resulting in a greater rate of CO2 exhalation. The potency of these effects is illustrated by the fact that an increase of just 0.5 kPa (4 mm Hg) in a person’s arterial partial pressure of CO2—from 5.3 to 5.8 kPa (40 to 44 mm Hg)—will cause the volume of air ventilated per minute to approximately double. During high-intensity exercise, as discussed in Chapter 8, production of lactic acid by anaerobic glycolysis

7 CO2 has been aptly termed a “gaseous acid” because it reacts with H2O to form carbonic acid (H2CO3), which then dissociates to form H+ and HCO3–. The changes in H+ concentration are sometimes expressed as changes in pH. When H+ concentration increases, pH decreases, and vice versa.

FiguRE 23.23 The likely fountainhead of breathing A 1-mm-thick slice of the medulla of the brain of a nestling mouse produces electrical signals that, judging from their patterns, control the rhythm of ordinary breathing and sighs. Each heavy black line is a recording of electrical activity as a function of time.The recordings pre- sented here have been integrated to remove random noise, explaining why they are smoother than those in Figure 23.10. (After Lieske et al. 2000.)

The breathing rhythm is relayed to the hypoglossal nucleus from the pre-Bötzinger complex.

The pre-Bötzinger complex originates signals that control both normal breathing and, it is postulated, sighs.

Dorsal motor nucleus of vagus

Hypoglossal nucleus

Pre-Bötzinger complex

Slice of medulla

Electrical output controlling normal breathing

Electrical output for a sigh

Time

Simultaneous recordings from hypoglossal nucleus (above) and pre-Bötzinger complex (below)

2s

Recording from pre-Bötzinger complex

2s

Voltage

often increases the H+ concentration of the blood, in addition to the effects of CO2 on H+. Ventilatory drive caused by this acidification sometimes is so potent that it gives athletes a sense of profound discomfort because of the intensity of their breathing.

Let’s now turn to the role of O2. Blood hypoxia in mammals is detected principally by chemoreceptive bodies outside the central nervous system: the carotid bodies and aortic bodies. There are two carotid bodies (each measuring about 0.5 cm in humans), positioned along the two common carotid arteries, near where each branches to form internal and external carotids. The carotid bodies receive blood flow from the carotid arteries and relay sensory information on the blood O2 partial pressure to the brainstem via the glossopharyngeal nerves. Although humans have only O2-sensing carotid bodies, dogs, cats, and many other mammals also have O2-sensing aortic bodies, located along the aortic arch.

Both the carotid and aortic bodies are richly perfused with blood from major arteries, and because of this they are in excellent posi- tions to monitor arterial O2 partial pressure. Ordinarily the arterial O2 partial pressure must fall far below normal before ventilation is reliably stimulated. Sensation of CO2 and H+ by the medulla of the brain is therefore paramount in regulating ventilation under usual resting conditions. In humans, if the arterial O2 partial pressure falls below 7–8 kPa (50–60 mm Hg) (as compared with a normal arterial value of ~12.7 kPa [~95 mm Hg]), marked stimulation of ventilation occurs. Such a large drop in arterial O2 partial pressure is unusual. Thus sensation of O2 partial pressure is of key importance in ventilatory regulation only under specialized circ*mstances. One of these is exposure to high altitude (BOx 23.2). The carotid and aortic bodies become more sensitive to lowered O2 when the blood concentration of CO2 or H+ is elevated.

External Respiration 619

620 Chapter 23

ventilation is also modulated by conscious con- trol, lung mechanosensors, and direct effects of exercise The most obvious type of modulation of ventilation in humans is conscious control. We can temporarily stop breathing by choosing to stop. There are, in addition, other types of control besides the chemosensory ones.

One well-understood set of controls is based on mechanore- ceptors in the lungs, which sense stretch or tension in the airways. Information from these receptors is relayed via sensory neurons to the brainstem, where signals for inhalation tend to be inhibited by lung expansion and excited by lung compression. Certain of these mechanosensory responses are known as the Hering-Breuer reflexes.

It is now well established that during exercise there are controls operating in addition to chemosensory ones. Whereas these other controls are important, they are not well understood. As already stressed, the arterial partial pressures of O2 and CO2 remain little changed from resting values during light to moderate exercise. This stability results because of adjustments in the ventilation rate, which is increased in tandem with the metabolic rate. However, arterial gas partial pressures are far too stable during light to moderate exercise to account for observed increases in ventilation on the basis of the simple chemosensory negative feedback systems we have discussed up to here; for example, whereas an increase of about 0.5 kPa (4 mm Hg) in the arterial CO2 partial pressure is required to bring about a doubling of ventilation rate, the measured CO2 partial pressure during exercise may not be elevated to that extent even when ventilation has reached 10–15 times the resting rate! In addition to the controls mediated by gas partial pressures, there is increasing evidence for the existence of controls that are initiated in direct association with the muscular movements of exercise. These controls are postulated to take two forms: First, parts of the brain that initiate motor signals to the exercising muscles might simultane- ously initiate stimulatory signals to the breathing centers. Second, sensors of movement or pressure in the limbs might stimulate the breathing centers based on the vigor of the limb activity they detect. One persuasive piece of evidence for these sorts of controls is that when people suddenly begin to exercise at a moderate level, their ventilation rate undergoes a marked increase within just one or two breaths; this response is far too rapid to be mediated by changes in the chemical composition of the body fluids. Another piece of evidence is that in many species of mammals, breathing movements and limb movements are synchronized during running.

both tidal volume and breathing frequency are modulated by control systems The overall rate of lung ventilation depends on two properties: the tidal volume, VT , and the frequency of breaths, f, usually expressed as the number of breaths per minute. The product of these is the respiratory minute volume:

Respiratory minute volume = VT × f (23.2) (mL/min) (mL/breath) (breaths/min)

To illustrate, resting humans have a tidal volume of about 500 mL and breathe about 12 times per minute. Thus their respiratory minute volume is about 6 L/min.

Both tidal volume and breathing frequency are increased during exercise and during other states that increase the rate of metabolism. Humans and other mammals, however, cannot maximize both of

these variables simultaneously because the time needed for one breathing cycle tends to increase as the tidal volume increases. Nonetheless, during vigorous exercise, trained athletes are able to maintain a tidal volume of at least 3 L while breathing at least 30 times per minute. In this way, their respiratory minute volume can reach greater than 100 L/min—more than 15 times the resting value.

The alveolar ventilation rate, typically expressed as the alveolar minute volume, is defined to be the rate at which new air is brought into the alveoli and other respiratory airways. This rate is important because the air that reaches the respiratory airways is the air that can undergo gas exchange with the blood. The alveolar minute volume is calculated by subtracting the volume of the anatomical dead space, VD, from the tidal volume and multiplying by the breathing frequency:

Alveolar minute volume = (VT – VD) × f (23.3)

Another property of importance relating to the respiratory airways is the fraction of all inhaled air that reaches them. This fraction— calculated by dividing the alveolar minute volume (Equation 23.3) by the total minute volume (Equation 23.2)—is (VT – VD)/VT.

From the expression just described, you can see that—with VD assumed to be constant—the fraction of air reaching the respiratory airways increases as the tidal volume increases. This fact helps resolve a paradox. When the overall ventilation rate is increased, the oxygen utilization coefficient increases. Although humans, for example, use about 20% of the O2 in the air they breathe when their tidal volume is 500 mL, they use about 30% when their tidal volume is 2000 mL. How is this possible if, as we have often emphasized, the control systems typically keep the alveolar O2 partial pressure constant? The paradox is resolved by recognizing two aspects of gas exchange. First, air that reaches the respiratory airways always gives up about the same fraction of its O2 (accounting for the constancy of alveolar O2 partial pressure). Second, however, a greater proportion of all the air that is breathed actually enters the respiratory airways as the tidal volume increases.

in species of different sizes, lung volume tends to be a constant proportion of body size, but breathing frequency varies allometrically

If we look at the full range of mammals, ranging in size from shrews to whales, there is a strong inverse (and allometric) relation between breathing frequency and body size. Humans breathe about 12 times per minute at rest. A mouse breathes 100 times per minute! This dramatic effect is a logical consequence of several facts. First, lung volume tends, on average, to be a relatively constant fraction of total body volume: Lung volume in liters averages about 6% of body weight in kilograms. Second, resting tidal volume tends 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 are at rest, the amount of O2 they obtain per breath is approximately a constant proportion of their body weight. However, as emphasized in Chapter 7, the resting weight-specific rate at which mammals metabolically consume O2 increases allometrically as body size decreases. If the O2 demand per unit of body weight in a small mammal is greater than that in a large mammal, and yet the small animal obtains about the same amount of O2 per breath per unit of weight, then the small animal must breathe more frequently.

External Respiration 621

622 Chapter 23
Pulmonary surfactant keeps the alveoli

from collapsing

The alveoli may be thought of as aqueous bubbles because their gas-exchange surfaces are coated with an exceedingly thin water layer. If the alveoli were composed only of water, they would fol- low the physical laws of simple aqueous bubbles. One such law is 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 radius of an alveolus decreases, the alveolus might collapse shut by emptying entirely into the airways of the lung. This possibility may sound like a remote conjecture from a physics book. In fact, however, until this application of physics to biology was appreci- ated, thousands of human babies died every year because of bubble physics, as we discuss soon.

The alveoli in normal lungs do not behave as simple aqueous bubbles because of the presence of a complex mixture of metabolically produced lipids and proteins called pulmonary surfactant (surfactant, “surface active agent”). About 90% of pulmonary surfactant is lipids, mostly phospholipids (amphipathic molecules, as seen in Chapter 2). Pulmonary surfactant is synthesized by specialized pulmonary epithelial cells, which secrete the lipoprotein complex as vesicles. After secretion, phospholipids from the vesicles associate with the surface of the thin water layer that lines each alveolus, where they radically alter the surface-tension properties of the water. Their overall effect is to reduce the surface tension below that of pure water. This effect in itself helps prevent alveoli from collapsing shut because the tendency of bubbles to collapse decreases as their surface tension decreases (explaining why soap bubbles linger longer than bubbles of pure water). The most profound effect of pulmonary surfactant, however, is that it gives the alveoli a dynamically variable surface tension. With surfactant present, as an alveolus enlarges, its surface tension increases, an effect that impedes further enlargement and helps prevent the alveolus from expanding without limit. Conversely, as an alveolus decreases in size, its surface tension decreases, helping to prevent any further decrease in size. Surfactant, therefore, helps keep all alveoli similar in size.

Infants born prematurely sometimes lack adequate amounts of pulmonary surfactant. Their alveoli therefore lack the protections of surfactant, and many alveoli collapse shut during each exhala- tion. An affected infant then must inhale with sufficient force to reopen the alveoli. The process is tiring and damages the alveoli. Death rates were very high until therapies based on knowledge of pulmonary surfactant were introduced.

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 because it plays indispensable roles in controlling the distribution of surfactant lipids.

Pulmonary surfactants that share basic chemical similarities have been reported from the lungs of all groups of terrestrial vertebrates, lungfish, and some other air-breathing fish. Thus the pulmonary surfactants have a long evolutionary history, dating back at least

8 This is an implication of Laplace’s Law, which—applied to bubbles— states that ΔP = 2T/r, where r is the radius of a bubble, ΔP is the pressure difference between the inside and outside of the bubble, and T is the 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 seen to increase as the radius r decreases.

to the origins of vertebrate air breathing. The roles of pulmonary surfactants in animals other than mammals are incompletely known but are gradually being better understood.

Breathing by Birds

The lungs of birds, although they are logical derivatives of the types of lungs thought to exist in the common ancestors of birds and mammals, differ in fundamental structural features from the lungs of mammals and all other modern vertebrates except certain crocodilian reptiles. The structural difference between avian and mammalian lungs inevitably invites comparison. Are avian lungs functionally superior to mammalian lungs? Some authorities conclude that the designs of the lungs in birds and mammals are “different but equal”—that is, equal in their gas-exchange ability. Other authorities conclude that the lungs of birds are in fact superior organs of gas exchange. As evidence, they point to the fact that bird

(A) Anatomy

Anterior secondary bronchi

Anterior air sacs

Primary bronchus

Parabronchi

Mesobronchus

Neopulmonal parabronchi

External Respiration 623

FiguRE 23.24 Airflow in the lungs and air sacs of birds (A) Basic anatomy of the avian lung and its connec- tions with the air sacs. In this presentation, the anterior and posterior groups of secondary bronchi are each represent- ed as a single passageway.The tubes labeled parabronchi are those of the dominant paleopulmonal system. (B, C) Airflow during (B) inhalation (when the air sacs undergo expansion) and (C) exhalation (when the air sacs undergo compression).

Air flows through the parabronchi from posterior to anterior.

The posterior air sacs expand and fill with fresh air coming directly from the environment.

As during inhalation, air flows through the parabronchi from posterior to anterior.

The posterior air sacs are compressed.
The fresh air in them is directed primarily into the posterior secondary bronchi.

KEY

Posterior secondary bronchi

Posterior air sacs

(B) Inhalation

The anterior air sacs expand and fill with gas that has passed across the respiratory exchange surfaces.

(C) Exhalation

The anterior
air sacs are compressed, discharging stale gas stored in them.

The gas that is exhaled has passed across the respiratory exchange surfaces even if temporarily held in the anterior air sacs.

Outflow to the environment along the length of the mesobronchus is minimal, according to available evidence.

lungs have relatively large surface areas for gas exchange and thin gas-exchange membranes (see Figure 23.8). They also point to the fact that some birds, such as certain geese, cranes, and vultures, can fly—not just mope around and survive—near or above the altitude of Mt. Everest. The design of the bird lung, in comparison with the mammalian lung, may be an advantage at high altitude, in part because (as we will see) cross-current gas exchange pre- vails in the bird lung instead of tidal exchange. High-flying birds are discussed in Box 23.2.

they are formally termed the medioventral and mediodorsal groups, respectively. Also for simplicity, each group is represented as just a single passageway in FiguRE 23.24A.

The anterior and posterior secondary bronchi are connected by a great many small tubes, 0.5–2.0 mm in internal diameter, termed tertiary bronchi or parabronchi (four are shown in Fig- ure 23.24A). As depicted in FiguRE 23.25, the central lumen of each parabronchus gives off radially along its length an immense number of finely branching air capillaries. The air capillaries are profusely surrounded by blood capillaries and are the sites of gas exchange. They are only 3–14 μm in diameter (large birds tending to have diameters greater than those of small birds), and collectively they form an enormous gas-exchange surface amounting to 200–300 mm2/mm3 of tissue in the parabronchial walls. Air flows through the central lumen of each parabronchus, but exchange between the central lumen and the surfaces of its air capillaries is probably largely by diffusion. The parabronchi, air capillaries, and associated vasculature constitute the bulk of the lung tissue of a bird.

A bird’s trachea bifurcates to give rise to two primary bronchi,

Hill Animal Physiology 4E
which enter the lungs. Here the similarity to mammals ends. The

Sinauer Associates
pMriomraalersySbturdoionchus that enters each lung passes through the lung,

Figure 23.24 12-09-15

being known as the mesobronchus within the lung. Two groups of branching secondary bronchi arise from the mesobronchus. One group, which arises at the anterior end of the mesobronchus, spreads over the ventral surface of the lung. The other group origi- nates toward the posterior end of the mesobronchus and spreads over the dorsolateral lung surface. For simplicity, we call these the anterior and posterior groups of secondary bronchi, although

Fresh air

Stale gas (i.e., depleted in O2, enriched in CO2)

624 Chapter 23
(A) Scanning electron micrograph of parabronchi in longitudinal section

Openings such as these lead to air capillaries.

(B) Scanning electron micrograph of a parabronchus in cross section

This tissue consists of intermingled air capillaries and blood capillaries.

(C) A parabronchus and associated vasculature

Air capillaries

Parenchyma (intermingled air capillaries and blood capillaries)

Parabronchus 0.5 mm

Efferent blood vessel

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- bronchi. (Each mesobronchus terminates at its connection with an abdominal air sac.) The air sacs are thin-walled, poorly vascularized structures that play little role in gas exchange between the air and 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.

Cervical sac

Trachea Syrinx

Primary bronchis

Anterior secondary bronchi

Posterior secondary bronchi

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.)

Air flow

Blood flow

Afferent blood vessel

These lung structures are collectively termed the paleopulmonal Hill Animal Physiology 4E

Abdominal sac

system, or simply paleopulmo. Most birds, in addition, have a Sinauer Associates

more or less extensively developed system of respiratory para-

Morales Studio
brFoignucreh 2i a3l.2t5ub1e2s-—09t-e1r5med t he n e o p u l m o n a l s y s t e m — r u n n i ng directly between the posterior air sacs and the posterior parts of the mesobronchi and posterior secondary bronchi (see Figure 23.24A). The neopulmonal system is especially well developed in songbirds. The paleopulmonal system, nonetheless, is always dominant.

Ventilation is by bellows action

Avian lungs are compact, rigid structures. Unlike mammalian lungs, they undergo little change in volume over the course of

Anterior thoracic sac

Posterior thoracic sac

Interclavicular sac

FiguRE 23.26 The air sacs of a goose and their connections to the lungs Air sacs are blue, lungs are light orange. All the air sacs are paired, except the single interclavicular sac. (After Bracken- bury 1981.)

Mesobronchus

External Respiration 625

each breathing cycle. The air sacs, by contrast, expand and contract substantially and, like bellows, suck and push gases through the relatively rigid airways of the lungs. To a dramatic extent relative to mammalian ventilation, this avian process is an energetically inexpensive way to move air.

The part of the rib cage surrounding the lungs themselves is relatively rigid. During inhalation, other parts of the rib cage (es- pecially those posterior to the lungs) are expanded by contraction of internal intercostal muscles and certain other thoracic muscles, and the sternum swings downward and forward. These movements enlarge all the air sacs by expanding the thoracoabdominal cavity. Some of the external intercostals and abdominal muscles compress the thoracoabdominal cavity and air sacs during exhalation. Rest- ing birds typically breathe at only about one-half or one-third the frequency of resting mammals of equivalent body size, but the birds have greater tidal volumes.

Air flows unidirectionally through the parabronchi

Air flows unidirectionally through the parabronchi of the paleo- pulmonal system. To see how this occurs, we must describe the movement of air during both inhalation and exhalation. During inhalation, both the anterior and posterior sets of air sacs expand. Suction, therefore, is developed in both sets of air sacs, and both receive gas. As depicted in FiguRE 23.24B, air inhaled from the atmosphere flows through the mesobronchus of each lung to enter the posterior air sacs and posterior secondary bronchi. Simultane- ously, the air entering the posterior secondary bronchi is drawn anteriorly through the parabronchi by suction developed in the expanding anterior air sacs. Three aspects of the events during inhalation deserve emphasis. First, the posterior air sacs are filled with relatively fresh air coming directly from the environment. Second, the anterior air sacs are filled for the most part with stale gas that has passed across the respiratory exchange surfaces in the parabronchi. Finally, the direction of ventilation of the parabronchi in the paleopulmonal system is from posterior to anterior.

During exhalation, both sets of air sacs are compressed and discharge gas. As shown in FiguRE 23.24C, air exiting the poste- 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 the environment during inhalation. Gas exiting the parabronchi anteriorly, combined with gas exiting the anterior air sacs, is directed into the mesobronchus via the anterior secondary bronchi and exhaled. Recall that the anterior air sacs were filled with stale gas from the parabronchi during inhalation. Thus the exhaled gas is mostly gas that has passed across the respiratory exchange surfaces. Three aspects of the expiratory events deserve emphasis: First, the relatively fresh air of the posterior air sacs is directed mostly to the parabronchi. Second, most of the gas that is exhaled from the lungs has passed across the respiratory exchange surfaces. Finally, air flows through the parabronchi of the paleopulmonal system from posterior to anterior, just as it does during inhalation.

One of the greatest remaining questions in the study of avian lungs is how air is directed along its elaborate (and in some ways counterintuitive) paths through the paleopulmonal system and air sacs. Passive, flaplike valves appear to be entirely absent. Active,

muscular valves could be present, but evidence for their existence is at best circ*mstantial. Most present evidence suggests that the complex architecture of the lung passages creates aerodynamic conditions that direct air along the inspiratory and expiratory paths without need of either passive or active valves.

Ventilation of the neopulmonal system is incompletely under- stood. Probably, however, airflow through many of the neopulmonal parabronchi is bidirectional (see Figure 23.24B,C).

As discussed in BOx 23.3, birds face unique challenges at hatching because of their lungs, which at that point must take over full responsibility for gas exchange.

The gas-exchange system is cross-current

When the unidirectional flow of air through the paleopulmonal parabronchi in the lungs of birds was first discovered, countercur- rent exchange between the blood and air was quickly hypothesized. Soon, however, this hypothesis was disproved by clever experi-

626 Chapter 23

ments, which showed that the efficiency of gas exchange between air and blood is not diminished if the direction of airflow in the parabronchi is artificially reversed. Morphological and functional studies have now shown convincingly that blood flow in the respi- ratory exchange vessels of the circulatory system occurs in a cross- current pattern relative to the flow of air through the parabronchi (see Figures 23.5 and 23.25C).

internal gills (see Figure 23.2). Certain of the aquatic snails provide a straightforward example. In them (FiguRE 23.28A), a series of modest-sized gill leaflets hangs in the mantle cavity and is venti- lated unidirectionally by ciliary currents. Blood flow through the leaflets, in at least some cases, is opposite to the direction of water flow. Thus countercurrent gas exchange occurs.

One major modification of the gills in molluscs is the evolution of extensive sheetlike gills in the clams, mussels, oysters, and other lamellibranch (“sheet-gilled”) groups. In these groups, four gill sheets, or lamellae, composed of fused or semifused filaments, hang within the mantle cavity (FiguRE 23.28B). Cilia on the gill sheets drive incoming water through pores on the gill surfaces into water channels that run within the gill sheets; the water channels then convey the water to exhalant passages. The direction of water flow within the water channels is opposite to the direction of blood flow in the major gill blood vessels, meaning that countercurrent gas exchange can again occur. The specialized sheetlike gills of these molluscs represent, in part, an adaptation for feeding: As the abundant flow of incoming water passes through the arrays of pores leading to the interior water channels of the gill sheets, food particles suspended in the water are captured for delivery to 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 body surfaces suffices to meet metabolic needs. Thus the “gills” have become primarily feeding organs.

In the cephalopod molluscs—the squids, cuttlefish, and oc- topuses—it is not so much the gills that are specialized, but the mechanism of ventilation. The gills are feathery structures that follow the usual molluscan plan of being positioned in the mantle cavity (FiguRE 23.28C). They are ventilated, however, by muscular contraction rather than beating of cilia. Cephalopods swim by using muscular contractions of the mantle; they alternately suck water into the mantle cavity via incurrent openings and then drive it forcibly outward through a ventral funnel by mantle contraction, producing a jet-propulsive force. The gills are ventilated (in countercurrent fashion) by the vigorous flow of water used for propulsion. Some species move so much water for propulsion that they use only a small fraction of the O2 in the water: 5%–10%.

A final specialization worthy of note in molluscs is the evolution of the mantle cavity into a lung in the dominant group of snails and slugs that live on land, a group known aptly as the pulmonates (FiguRE 23.28D). In the terrestrial pulmonates, gills have disap- peared, and the walls of the mantle cavity have become highly vascularized and well suited for gas exchange. Some species are thought to employ the mantle cavity as a diffusion lung, but others ventilate it by raising and lowering the floor of the cavity.

Decapod crustaceans include many important water breathers and some air breathers

In the decapod crustaceans—which include many ecologically and commercially important crabs, shrimps, lobsters, and cray- fish—the head and thorax are covered with a continuous sheet of exoskeleton, the carapace, that overhangs the thorax laterally, fitting more or less closely around the bases of the thoracic legs. The carapace encloses two lateral external body cavities—the branchial chambers—in which the gills lie (FiguRE 23.29A).

Breathing by Aquatic invertebrates and Allied groups

Many small aquatic invertebrates, and some large ones, have no specialized breathing organs. They exchange gases across general body surfaces, which sometimes are ventilated by swimming mo- tions or by cilia- or flagella-generated water currents. Many larvae and some adults also lack a circulatory system. Thus gases move within their bodies by diffusion or by the squishing of body fluids from place to place. To the human eye, these sorts of gas-exchange systems are confining. They suffice only if the animals are tiny (see Box 22.1) or have specialized body plans, such as those of flatworms and jellyfish. Most cells of a flatworm are near a body surface be- cause the worm’s body is so thin. Most cells of a jellyfish are near a body surface because a jellyfish’s body is organized with its active tissues on the outside and primarily low-metabolism, gelatinous tissue deep within.

Adults of the relatively advanced phyla of aquatic invertebrates typically have gills of some sort. The gills of the various major phyletic groups are often independently evolved. Thus, whereas they all are evagin*ted and project into the water (meeting the definition of gills), they vary widely in their structures and in how they are ventilated (FiguRE 23.27).

molluscs exemplify an exceptional diversity of breathing organs built on a common plan

The phylum Mollusca nicely illustrates that within a phyletic group, a single basic sort of breathing apparatus can undergo wide diversi- fication. In molluscs, outfolding of the dorsal body wall produces a sheet of tissue, the mantle (responsible for secreting the shell), that overhangs or surrounds all or part of the rest of the body, thereby enclosing an external body cavity, the mantle cavity. The gills of molluscs typically are suspended in the mantle cavity and thus are

(A) Polychaete annelid with gill tufts

Gills

External Respiration 627

(B) Polychaete annelid with tentacular fan

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

Water ring

Sea star showing major internal parts of water vascular system

KEY

Digestive cecum

Gonad

...and the tube feet function partly as gills.

Gill sheets

Gill plates

Radial canal of water vascular system

The branchial papulae are gills...

Perivisceral coelom filled with coelomic fluid

Branchial papulae

FiguRE 23.27 A diversity of gills in aquatic invertebrates
(A) This terebellid worm (Amphitrite), a type of marine annelid, lives inside a tube it constructs and can pump water in and out of the tube. (B) This fanworm, another type of marine annelid, also lives in a tube, but when undisturbed, it projects its well-developed array of pinnately divided tentacles into the ambient water.The tentacles are used for both feeding and respiratory gas exchange; they are ventilated by the actioHnillof cAinliamaolnPhthyesiotelongtya4cEles. (C) Sea stars bear many thin-walled,

gases pass between the coelomic fluid and ambient water by diffusion through the walls of the papulae. Similarly, gases diffuse between the coelomic fluid and ambient water through the tube feet and associat- ed parts of the water vascular system. Cilia accelerate these processes by circulating fluids over the inner and outer surfaces of the papulae and tube feet.(D) Horseshoe crabs (Limulus) have unique book gills, consisting of many thin gill sheets arranged like pages of a book.The book gills are protected under thick gill plates, which undergo rhythmic flapping motions that ventilate the gills. (D after a drawing by Ralph Russell, Jr.)

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fingerlike projections from their coelomic cavity, termed branchial Morales Studio

papulae (“gill processes”), on their upper body surfaces; respiratory Figure 23.27 12-10-15

Oral side

Convection Diffusion

628 Chapter 23 (A) Aquatic snail

(A) A transverse section through the thorax of a crayfish

The carapace—a sheet of exo- skeleton—overhangs the body. It thus...

...encloses a branchial chamber on each side. The gills are in the branchial chambers.

Gills

Lateral carapace

Gut

Heart

Pericardial sinus

Mantle cavity

Foot

Shell

Gills

Gill leaflets hanging in the mantle cavity are ventilated by water currents generated by ciliary action.

Branchial chamber

Muscle

Base of leg

KEY

Water for gill ventilation is drawn into and expelled from the mantle cavity through openings called siphons.

Exhalant siphon

Inhalant siphon

Cilia on the sheetlike gills drive water through pores into internal water channels, which convey the water to the exhalant siphon.

Ventral nerve cord

(B) Clam (a lamellibranch mollusc)

(B) A lateral view showing the gills under the carapace

Gill

Carapace

Shell Foot

Mantle cavity

Visceral mass Gill lamella

(D) Pulmonate land snail

Lung (mantle cavity)

Ventilation is unidirectional, and countercurrent exchange may occur. Some crabs and crayfish have invaded the land, especially in the tropics. All the semiterrestrial and terrestrial species retain gills, which are supported to some degree by their cuticular covering. One trend observed in semiterrestrial and terrestrial crabs is that the gills tend to be reduced in size and number by comparison with aquatic crabs. 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

Shell

Mantle cavity

Foot

The scaphognathite beats, driving water out of the branchial chamber. Because of the suction thus produced in the chamber, water enters at multiple places.

(C) Squid (a cephalopod)

Funnel (formed from mantle)

Mantle cavity

Gills

Squid gills are ventilated by muscle power. They are positioned in the muscle-driven water stream the animal uses to swim by jet propulsion.

A pulmonate land snail lacks gills, but has a lung derived from the
mantle cavity.

hell

an anterior exhalant opening. Negative pressure is thus created

Convection

Scaphognathite

Gill lamella with pores and internal channels

FiguRE 23.29 The gills and ventilation in a crayfish

The gills arise from near the bases of the thoracic legs. Each gill consists of a central axis to which are attached many richly vas- cularized lamellar plates, filaments, or dendritically branching tufts. The gill surfaces—like all the external body surfaces of crustaceans—are covered with a chitinous cuticle. The cuticle on 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, under control of nerve impulses from a central pattern generator in theHcilel ntArnailmnael rPvhoyusisolsoygsyte4mE , generally drives water outward through

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within the branchial chamber, drawing water in at various openings.

Figure 23.29 12-10-15

S

FiguRE 23.28 The diversification of the breathing system in molluscs

Hill Animal Physiology 4E Sinauer Associates Morales Studio
Figure 23.28 12-10-15

9 This tissue is called the branchiostegites.

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.

Breathing by insects and Other

Tracheate Arthropods

The insects (FiguRE 23.30) have evolved a remarkable strategy for breathing that is entirely different from that of most meta- bolically active animals. Their breathing system brings the gas- exchange surface itself close to every cell in the body. Thus, with some thought-provoking exceptions, the cells of insects get their O2 directly from the breathing system, and the circulatory system plays little or no role in O2 transport. Insect blood, in fact, usually lacks any O2-transport pigment such as hemoglobin.

The body of an insect is thoroughly invested with a system of gas-filled tubes termed tracheae (FiguRE 23.31A,B). This system opens to the atmosphere by way of pores, termed spiracles, located at the body surface along the lateral body wall. Tracheae penetrate into the body from each spiracle and branch repeatedly, collectively reaching all parts of the animal (only major branches are seen in Figure 23.31). The tracheal trees arising from different spiracles typically join via large longitudinal and transverse connectives to form a fully interconnected tracheal system. The spiracles, which number from 1 to 11 pairs, are segmentally arranged and may occur on the thorax, abdomen, or both (but not the head). Usually they can be closed by spiracular muscles. Although tracheal breathing is best understood in insects, there are other tracheate arthropods: Most notably, certain groups of spiders and ticks have tracheal systems. Some spiders and other arachnids have book lungs, unique breathing

FiguRE 23.30 A praying mantis, one of the largest existing insects To look at a praying mantis, one could imagine it breath- ing through its mouth. Nothing could be further from the truth.

organs that sometimes function in parallel with tracheal systems and sometimes are the sole breathing organs (BOx 23.4).

The tracheae of an insect develop as invagin*tions of the epi- dermis and thus are lined with a thin cuticle. Typically the cuticle is thrown into spiral folds, providing resistance against collapse. The tracheae become finer with increasing distance from the spiracles and finally give rise to very fine, thin-walled end-tubules termed tracheoles, believed to be the principal sites of O2 and CO2 exchange with the tissues. Tracheoles are perhaps 200–350 μm long and are believed to end blindly. They generally taper from a lumen diameter approximating 1 μm at their origin to 0.05–0.20 μm at the end. The walls of the tracheoles and the finest tracheae are about 0.02–0.2 μm thick—exceedingly thin by any standard (see Figure 23.8B).

Although the layout of the tracheal system varies immensely among various species of insects, the usual result is that all tissues are thoroughly invested with fine tracheae and tracheoles. The degree of tracheation of various organs and tissues tends to vary directly with their metabolic requirements. For the most part, the tracheoles run between cells. However, in the flight muscles of many species, the tracheoles penetrate the muscle cells, indenting the cell membranes inward, and run among the individual myofibrils, in close proximity to the arrays of mitochondria. The average distance between adjacent tracheoles within the flight muscles of strong fliers is often only about 3 μm. The nervous system, rectal glands, and other active tissues—including muscles besides the flight muscles—also tend to be richly supplied by the tracheal system, although intracellular penetration is not nearly as common as in flight muscles. In the epidermis of the bug Rhodnius, which has been carefully studied, tracheoles are much less densely distributed than in active flight muscles, but nonetheless, cells are usually within

630 Chapter 23

30 μm of a tracheole. In other words, no cell is separated from a branch of the tracheal system by more than two or three other cells! The terminal ends of the tracheoles are sometimes filled with liquid when insects are at rest. During exercise, or when the insects are exposed to O2-deficient environments, the amount of liquid decreases and gas penetrates farther into the tracheoles. This process facilitates the exchange of O2 and CO2 because of the greater ease

of diffusion in gas than liquid.
Distensible enlargements of the tracheal system called air

sacs are a common feature of insect breathing systems (FiguRE 23.31C) and may occur in the head, thorax, or abdomen. Some air sacs are swellings along tracheae, whereas others form blind endings of tracheae. Air sacs tend to be particularly well developed in active insects, in which they may occupy a considerable fraction of the body volume.

Diffusion is a key mechanism of gas transport through the tracheal system

The traditional dogma has been that the tracheal system of most insects functions as a diffusion lung, meaning that gas transport through the system occurs solely by diffusion. This dogma is pres- ently undergoing profound revision. Diffusion, nonetheless, seems likely to be an important gas-transport mechanism in subparts of the tracheal system in most or all insects and may be the sole transport process in some. Diffusion can occur fast enough to play this role because the tracheae are gas-filled.

Because of the importance of diffusion in insect breathing and because diffusion transport tends to be slow when distances are great, physiologists have long wondered whether insect body size is limited by the nature of the insect breathing system. A recent study using a new X-ray technique to visualize the tracheal system (see Figure 23.31B) revealed that in beetles of different body sizes, the volume of the tracheal system is disproportional to body size. In stark contrast to mammals, a greater proportion of body space is devoted to the breathing system in big beetles than in small

ones. This trend could represent an evolutionary compensation for diffusion limitations in large-bodied insects. If so, the trend would suggest that a tracheal breathing system poses obstacles to the evolution of large body size.

When considering an individual insect, a question that arises is how the rate of diffusion can be varied to correspond to the insect’s needs for O2. Although diffusion may sound like a process that is purely physical and therefore independent of animal needs, in fact its rate responds to an insect’s metabolic needs because the animal’s metabolism alters the partial pressures of gases. Suppose that an insect breathing by diffusion has an adequate rate of O2

Hill Animal Physiology 4E
transport when (1) the atmospheric O2 partial pressure is at the

the insect suddenly increases its rate of O2 consumption, its end- tracheal O2 partial pressure will fall because of the increased rate of O2 removal from the tracheae. This decline in the end-tracheal partial pressure will increase the difference in partial pressure between the two ends of the tracheal system and thus acceler- ate O2 diffusion. Suppose that the difference in partial pressure between level ➊ and level ➌ in Figure 23.32A is sufficient for O2 to diffuse fast enough to meet the insect’s new (higher) O2 need. The end-tracheal partial pressure will then fall to level ➌ and stabilize. In this way, the rate of diffusion will automatically increase to meet the insect’s heightened O2 need.

Of course, there are limits to the ability of the process just described to increase the rate of O2 diffusion. The end-tracheal O2 partial pressure must itself remain sufficiently high for O2 to diffuse from the ends of the tracheae to the mitochondria in cells. If an insect’s oxygen cascade follows line ➊-➋-➍ in FiguRE 23.32B when the insect has a low rate of cellular O2 use, it might follow line ➊-➌-➎ when the insect’s rate of O2 use is raised. The mitochondrial O2 partial pressure would then be very low, and a further increase in the rate of O2 diffusion might not be possible while keeping the mitochondrial O2 level adequate.

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level marked ➊ in FiguRE 23.32A and (2) the O2 partial pressure Morales Studio

at the inner end of its tracheal system is at the level marked ➋. If Figure Box 23.04 12-10-15

(A) Major parts of the tracheal system in a flea

(C) Air sacs in the abdomen of a worker honeybee

Air sac

Origins of tracheae

Transverse tracheal connective

External Respiration 631 FiguRE 23.31 insects breathe using a tra-

cheal system of gas-filled tubes that— branching and rebranching—reach all tissues from the body surface (A) The principal tracheae in a flea in the genus Xeno- psylla—an insect that has ten pairs of spiracles (two thoracic pairs and eight abdominal).

(B) The tracheae in a tiny living adult carabid beetle in the genus Notiophilus, visualized by
a cutting-edge technique, synchrotron X-ray phase-contrast imaging. (C) Air sacs and as- sociated tracheae in the abdomen of a worker honeybee (Apis).Additional air sacs occur in the head and thorax. (A after Wigglesworth 1935; B from Socha et al. 2010; image courtesy of Jake Socha.)

Thoracic spiracle 1

Abdominal spiracles 1–7

Abdominal spiracle 8

Tracheae 0.5 mm

A new X-ray method is permitting physiologists to see, for the first time, large parts of the tracheal system in living insects.

Eye (A)

(B) Tracheae in a carabid beetle

Location of a spiracle (note tuft of tracheae originating here)

1 mm

Trachea in head

Trachea in leg

some insects employ conspicuous ventilation

Conspicuous (macroscopic) ventilation of the tracheal system oc-

curs in some large species of insects at rest and is common among

active insects. Grasshoppers and locusts, for example, are easily

seen to pump their abdomens, and abdominal pumping occurs

also in bumblebees, ants, and some other insects. The abdominal

pumping motions alternately expand and compress certain of the

tracheal airways, either causing tidal ventilation or causing air to

be sucked in via certain spiracles and expelled via others, flowing

unidirectionally through parts of the tracheal system in between.

FiguRE 23.32 insect oxygen cascades assuming oxygen transport by diffusion These diagrams outline simplified thought exercises. (A) A drop in the O2 partial pressure at the inner end
of the tracheal system from level ➋ to level ➌ will speed diffusion through the tracheal system by increasing the difference in partial pressure from one end to the other. (B) For the rate of diffusion to the mitochondria to be accelerated, the difference in partial pressure between the inner end of the tracheal system and the mitochondria must be increased—as well as the difference between the ambient air and the inner tracheae. Eventually no further increase in the rate of diffusion will be possible because the mitochondrial partial pres- sure will become too low for mitochondrial function.

AirHsillacsA,nwimhael Pnhpysrieosloegnyt4(Eas they are in grasshoppers and bumble- Sinauer Associates

bees, for example), commonly act as bellows during such muscular

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pumping movements; they may be compressed to only 25%–50%

Figure 23.31 12-10-15

of their full size during each cycle of compression. A mechanism of

(B)

Ambient air

Inner end of tracheal system

Mitochondria in cells

Ambient air

Inner end of tracheal system

O2 partial pressure O2 partial pressure

632 Chapter 23

conspicuous tracheal ventilation that is important in many insects during flight is autoventilation: ventilation of the tracheae sup- plying the flight muscles driven by flight movements.

Physiologists have generally hypothesized that during conspicuous ventilation, air is forced to flow only in major tracheae, with diffusion being the principal mode of gas transport through the rest of the tracheal system. According to this hypothesis, the function of con- spicuous ventilation is essentially to reduce the path length for diffusion by moving air convectively to a certain depth in the tracheal system.

microscopic ventilation is far more common than believed even 15 years ago

A revolution is underway in the understanding of microscopic ventilation: forced airflow that occurs on such fine scales that it is impossible to detect without the use of technology. Probably the most dramatic recent discovery is that when microscopic X-ray videos are made of various insects—such as beetles, crickets, and ants—the major tracheae in the head and thorax are observed to undergo cycles of partial compression and relaxation, a process named rhythmic tracheal compression. These pulsations occur ev- ery 1–2 s and are substantial: Each compression reduces the vol- umes of the tracheae to 50%–70% of their relaxed volumes. These microscopic cycles of tracheal compression probably move gases convectively. They may be particularly important for O2 delivery to the head and brain, recognizing that tracheae to the head con- nect to the atmosphere at thoracic spiracles and thus may be long.

Similar X-ray studies have revealed that in some insects under some conditions, tracheae undergo massive rhythmic collapsing movements during which they completely empty and refill. This is observed, for example, in some moth caterpillars exposed to hypoxia.

One of the first sorts of evidence for microscopic ventilation was the discovery and analysis of discontinuous gas exchange in diapausing pupae10 of moths some decades ago. The hallmark and defining feature of discontinuous gas exchange is that an insect releases CO2 to the atmosphere in dramatic, intermittent bursts, whereas the insect takes up O2 from the atmosphere at a relatively steady rate. The observed pattern of CO2 release arises in large part from spiracular control. In the periods between one burst of CO2 release and the next, the spiracles are closed or partly closed, and CO2 produced by metabolism accumulates in body fluids by dissolving and reacting to form bicarbonate (HCO3–). Because O2 is removed from the tracheal airways by metabolism during these periods, but the CO2 produced by metabolism temporarily accumulates in the body fluids rather than in the airways, a partial vacuum—a negative pressure—can develop in the airways. When such a negative pres- sure develops, it sets the stage for microscopic ventilation because atmospheric air can be sucked into the tracheal airways convectively on an inconspicuous, microscopic scale when the insect partly or fully opens its spiracles. Investigators have directly assessed in several species whether inward suction of air actually occurs, and it does in some (not all) of the species tested. No one knows the depth to which air is drawn, but it travels by convection at least through the spiracles and into the major tracheae. Discontinuous gas exchange is known today to occur widely in quiescent or resting insects, plus certain ticks, mites, and spiders.

10 Diapause is a programmed resting stage in the life cycle.

In addition to the forms of microscopic ventilation we have already discussed, several other types have been reported during the last 25 years. These include processes named miniature ventila- tion pulses in grasshoppers and tiny Prague cycles of CO2 release in beetles.

According to the old dogma, insects that were not conspicu- ously pumping their abdomens or ventilating in other conspicuous ways were breathing entirely by diffusion. The evidence is now overwhelming that convective phenomena are widely employed by visibly motionless insects, but many mysteries remain regarding the exact interplay of convection and diffusion in the tracheal system.

Control of breathing

A vulnerability of the insect respiratory system is that it can per- mit rapid evaporative loss of body water. The gas in the tracheal airways is humid—ordinarily saturated with water vapor—and when the spiracles are open, only a minute distance separates the humid tracheal gas from the atmosphere. Outward diffusion of water vapor can accordingly be rapid. Insects commonly solve this problem by keeping their spiracles partly closed—or by periodi- cally opening and closing them—whenever compatible with their needs for O2 and CO2 exchange. If the spiracles of resting insects are experimentally forced to remain fully open all the time, the rate of evaporative water loss increases 2- to 12-fold, demonstrating the importance of keeping them partly closed.

In insects using diffusion transport, it is common for the spiracles to be opened more fully or frequently as the insects become more active. The greater opening of the spiracles facilitates O2 transport to the tissues, although it also tends to increase evaporative water loss. Insects that ventilate their tracheal systems by abdominal pumping or other conspicuous mechanisms are well known to increase their rates of ventilation as they become more active.

What is the chemosensory basis for spiracular control? The most potent stimulus for opening of the spiracles in insects is an increase in the CO2 partial pressure and/or H+ concentration of the body fluids. A decrease in the O2 partial pressure in the body fluids may also stimulate spiracular opening but typically offers far less potent stimulation. In these respects, the control of the spiracles in insects resembles the control of pulmonary ventilation in mammals.

Aquatic insects breathe sometimes from the water, sometimes from the atmosphere, and sometimes from both

Many insect species live underwater in streams, rivers, and ponds during parts of their life cycles. The aquatic life stages of some of these species lack functional spiracular openings and obtain O2 by taking up dissolved O2 from the water using superficial arrays of fine tracheae. These insects often have dense proliferations of fine tracheae under their general integument. Many have tracheal gills: evagin*tions of the body surface that are densely supplied with tracheae and covered with just a thin cuticle—a remarkable parallel with the evolution of ordinary gills in numerous other groups of aquatic animals. Tracheal gills may be positioned on the outer body surface or in the rectum. In aquatic insects that breathe with tracheal gills or other superficial tracheae, the tracheal system remains gas-filled. Oxygen diffuses into the tracheal airways from the water across the gills or other superficial tracheae. Thereafter

the gas-filled tracheal system serves as the path of least resistance for the O2 to move throughout the body.

Other aquatic insects retain functional spiracles and have evolved alternative ways of interfacing their tracheal breathing systems with the ambient water or air. The aquatic insects with functional spiracles breathe from external gas spaces. There are three distinctive ways in which they do so. The simplest to understand is the system used by insects such as mosquito larvae, which hang at the water’s surface and have their functional spiracles localized to the body region that contacts the atmosphere. Such insects breathe from the atmosphere, much in the way that terrestrial insects do.

A second strategy employed by aquatic insects with functional

spiracles is to carry a conspicuous bubble of gas captured from the

atmosphere. Many water beetles, for example, carry a conspicuous

bubble either under their wings or at the tip of their abdomen (see

opening photo of Chapter 22). Their functional spiracles open into

the bubble and exchange O2 and CO2 with the gas in the bubble.

As explained previously (see Figure 22.3), a remarkable attribute

water diffuses into the bubble. Thus the insect is able to remove much more O2 from the bubble than simply the amount captured from the atmosphere. A conspicuous bubble gradually shrinks, a process that decreases its surface area and impairs O2 diffusion into the bubble because the rate of diffusion depends on bubble surface area. A bubble of this sort must therefore be periodically renewed with air from the atmosphere.

The third strategy employed by aquatic insects with functional spiracles is certainly the most unexpected. It is also a type of bubble breathing, but a very different type. In some aquatic insects, parts of the body surface are covered extremely densely with fine water- repelling hairs; the bug Aphelocheirus aestivalis, for example, has 2–2.5 million of these hairs per square millimeter! Such densely distributed water-repelling hairs on the body surface trap among themselves a thin, almost invisible film of gas that cannot be dis- placed. This film of gas, known as a plastron, is incompressible and permanent. Thus its surface area remains constant, and it can serve as a gill (an air space into which O2 diffuses from the water) for an indefinite period. Some plastron-breathing aquatic insects remain submerged continuously for months!