Entomology 3rd edition - C.Gillott - Chapter 15 pptx

Introduction In all organisms gas exchange, the supply of oxygen to and removal of carbon dioxide from cells, depends ultimately on the rate at which these gases diffuse in the dissolved

Gas Exchange

1 Introduction

In all organisms gas exchange, the supply of oxygen to and removal of carbon dioxide from cells, depends ultimately on the rate at which these gases diffuse in the dissolved state The diffusion rate is proportional to (1) the surface area over which diffusion is occurring and (2) the diffusion gradient (concentration difference of the diffusing material between the two points under consideration divided by the distance between the two points) Diffusion alone, therefore, as a means of obtaining oxygen or excreting carbon dioxide can be employed only by small organisms whose surface area/volume ratio is high (i.e., where all cells are relatively close to the surface of the body) and organisms whose metabolic rate is low Organisms that are larger and/or have a high metabolic rate must increase the rate at which gases move between the environment and the body tissues by improving (1) and/or (2) above In other words, specialized respiratory structures with large surface areas and/or transport systems that bring large quantities of the gas closer to the site of use or disposal (thereby improving the diffusion gradient) have been developed For most terrestrial animals prevention of desiccation is another important problem, and this has had a major influence

on the development of their respiratory surfaces through which considerable loss of water might occur Typically, respiratory surfaces of terrestrial animals are formed as invaginated structures within the body so that evaporative water loss is greatly reduced

In insects the tracheal system, a series of gas-filled tubes derived from the integument, has evolved to cope with gas exchange Terminally the tubes are much branched, forming tracheoles that provide an enormous surface area over which diffusion can occur Further-more, tracheoles are so numerous that gaseous oxygen readily reaches most parts of the body, and, equally, carbon dioxide easily diffuses out of the tissues Thus, in most insects,

in contrast to many other animals, the circulatory system is unimportant in gas transport Because they are in the gaseous state within the tracheal system, oxygen and carbon dioxide diffuse rapidly between the tissues and site of uptake or release, respectively, on the body surface Oxygen, for example, diffuses 3 million times faster in air than in water (Mill, 1972) Again, because the system is gas-filled, much larger quantities of oxygen can reach the tissues in a given time (Air has about 25 times more oxygen per unit volume than water.) The eminent suitability of the tracheal system for gas exchange is illustrated by the fact that, for most small insects and many large insects at rest, simple diffusion of gases in/out

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invaginations of the integument Up to 12 (3 thoracic and 9 abdominal) pairs of spiracles may be seen in embryos, though this number is always reduced prior to hatching, and further reduction may occur in endopterygotes during metamorphosis Various terms are used to describe the number of pairs of functional spiracles, for example, holopneustic (10 pairs, located on the mesothorax and metathorax and 8 abdominal segments), amphipneustic (2 pairs, on the mesothorax and at the tip of the abdomen), and apneustic (no functional spiracles) The last condition is common in aquatic larvae, which are said, therefore, to have

a closed tracheal system (Section 4.1)

The proportion of the body filled by the tracheal system varies widely, both among species and within the same individual throughout a stadium In active insects whose tracheal system includes air sacs (see below) the tracheal system occupies a greater fraction of the body than in less active species Further, in the former, the volume of the tracheal system

may decrease dramatically during a stadium (e.g., in Locusta from 48% to 3%) as the

air sacs become occluded by the increased hemolymph pressure that results from tissue growth After ecdysis, when body volume has increased (Chapter 11, Section 3.2), the tracheal system expands because of the lowered hemolymph pressure

2.1 Tracheae and Tracheoles

In apterygotes other than lepismatid Zygentoma, the tracheae that run from each spiracle

do not anastomose either with those from adjacent segments or with those derived from the spiracle on the opposite side In the Lepismatidae and Pterygota both longitudinal and transverse anastomoses occur, and, though minor variations can be seen, the resultant pattern

of the tracheal system is often characteristic for a particular order or family Generally, a pair

of large-diameter, longitudinal tracheae (the lateral trunks) run along the length of an insect just internal to the spiracles Other longitudinal trunks are associated with the heart, gut, and ventral nerve cord Interconnecting the longitudinal tracheae are transverse commissures, usually one dorsal and another ventral, in each segment (Figure 15.1) Parts of the tracheal system, for example, that of the pterothorax, may be effectively isolated from the rest of the system by reduction of the diameter or occlusion of certain longitudinal trunks This arrangement is associated with the use of autoventilation as a means of improving the supply

of oxygen to wing muscles during flight (Section 3.3) Also, tracheae are often dilated to form large thin-walled air sacs that have an important role in ventilation (Section 3.3) and other functions

Numerous smaller tracheae branch off the main tracts and undergo progressive subdi-vision until at a diameter of about 2–5µm they form a number of fine branches each 1µµ µmµµ

or less across known as tracheoles Tracheoles are intracellular, being enclosed within a very thin layer of cytoplasm from the tracheoblast (tracheal end cell) (Figure 15.2), and ramify throughout most tissues of the body They are especially abundant in metabolically active tissues Thus, in flight muscles, fat body, and testes, for example, tracheoles indent

GAS EXCHANGE

FIGURE 15.1. (A) Dorsal tracheal system of abdomen of locust; and (B) diagrammatic transverse section

through abdomen of a hypothetical insect to illustrate main tracheal branches [A, from F O Albrecht, 1953, The

Anatomy of the Migratory Locust By permission of Athlone Press B, from R E Snodgrass, Principles of Insect

Morphology Copyright 1935 by McGraw-Hill, Inc Used with permission of McGraw-Hill Book Company.]

individual cells, so that gaseous oxygen is brought into extremely close proximity with the

energy-producing mitochondria

In Calpodes ethlius caterpillars not all tracheae end in tracheoles within or on tissues.

In particular, some tracheae originating from the spiracles of the eighth abdominal segment

FIGURE 15.2. Structure of (A) large; and (B) small tracheae (C) Origin of tracheole [After V B Wigglesworth,

1965, The Principles of Insect Physiology, 6th ed., Methuen and Co By permission of the author.]

form large, greatly branched tufts that are suspended within the hemolymph (Figure 15.3) The tracheolar tips of these tufts are connected to heart and other muscles so that the tufts are constantly moved within the hemolymph (Locke, 1998) The observation that hemocytes were abundant within the tufts led Locke to speculate that the tufts are sites of gas exchange for the blood cells, analogous to the lungs of vertebrates Though similar tracheal tufts are found in caterpillars from other lepidopteran families, their existence and function(s) among other insect groups has not been examined

As derivatives of the integument, tracheae comprise cuticular components, epidermis, and basal lamina (Figure 15.2) Adjacent to the spiracle, the tracheal cuticle includes, the cuticulin envelope, epicuticle and procuticle; in smaller tracheae and most tracheoles only the cuticulin envelope and epicuticle are present Providing the system with strength yet flexibility, tracheal cuticle has internal ridges that may be either separate (annuli) or form

a continuous helical fold (taenidium) In large tracheae the ridges include some procuticle, but this is absent from those of tracheoles Taenidia are absent from, or poorly developed

in, air sacs The epicuticle of tracheae comprises the same layers as that of the integument

GAS EXCHANGE

FIGURE 15.3. Tufts of tracheae in the eighth abdominal segment of Calpodes ethlius that perhaps serve to aerate

hemocytes Arrows indicate direction of hemolymph flow [From M Locke, 1998, Caterpillars have evolved lungs

for hemocyte gas exchange, J Insect Physiol 44:1–20 With permission from Elsevier.]

In the smallest tracheoles, however, only the cuticulin envelope is present and, furthermore,

this contains fine pores These two features may be associated with movement of liquid into

and out of tracheoles in connection with gas exchange (Section 3.1) (Locke, 1966)

2.2 Spiracles

Only in some apterygotes do tracheae originate at the body surface Normally, they

arise slightly below the body surface from which they are separated by a small cavity,

the atrium (Figure 15.4A) In this arrangment, the term “spiracle” generally includes both

the atrium and the spiracle sensu stricto, that is, the tracheal pore Except for those of a

few insects that live in humid microclimates, spiracles may be covered, for example, by

the elytra or wings in Hemiptera and Coleoptera, or are equipped with various valves for

prevention of water loss The valves may take the form of one or more cuticular plates that

can be pulled over a spiracle by means of a closer muscle (Figure l5.4B–D) Opening of the

valve(s) is effected either by the natural elasticity of the surrounding cuticle or by an opener

muscle Alternatively, the valve may be a cuticular lever which by muscle action constricts

the trachea adjacent to the atrium (Figure l5.4E,F) In lieu of, or in addition to, the valves,

there may be hairs lining the atrium or a sieve plate (a cuticular pad penetrated by many

fine pores) covering the atrial pore It is commonly assumed that an important function of

these hairs and sieve plates is to prevent dust entry However, as Miller (1974) noted, sieve

plates are not better developed on inspiratory than on expiratory spiracles and several other

functions can be suggested: (1) they may prevent waterlogging of the tracheal system in

terrestrial species during rain, in aquatic insects, and in species that live in moist soil, rotting

FIGURE 15.4. Spiracular structure (A) Section through spiracle to show general arrangement; (B, C) outer and inner views of second thoracic spiracle of grasshopper; (D) diagrammatic section through spiracle to show mechanism of closure The valve is opened by movement of the mesepimeron, closed by contraction of the muscle; (E) closing mechanism on flea trachea; and (F) section through flea trachea at level of closing mechanism.

[A–C, from R E Snodgrass, Principles of Insect Morphology Copyright 1935 by McGraw-Hill, Inc Used with

permission of McGraw-Hill Book Company D, after P L Miller, 1960, Respiration in the desert locust II The

control of the spiracles, J Exp Biol 37:237–263 By permission of Cambridge University Press E F, after V B.

Wigglesworth, 1965, The Principles of Insect Physiology, 6th ed., Methuen and Co By permission of the author.]

vegetation, etc.; (2) they may prevent entry of parasites, especially mites, into the tracheal system; and (3) they may reduce bulk flow of gases through the system caused by body movements, thereby reducing evaporative water loss This would be disadvantageous in insects that ventilate the tracheal system, and it is of interest, therefore, that those spiracles important in ventilation commonly lack a sieve plate or have a plate that is divided down the middle so that it may be opened during ventilation

3 Movement of Gases within the Tracheal System

Gas exchange between tissues and the tracheal system occurs almost exclusively across the walls of tracheoles, for it is only their walls that are sufficiently thin as to permit a satis-factory rate of diffusion It is necessary, therefore, to ensure that a sufficient concentration of

GAS EXCHANGE

oxygen is maintained in tracheoles to supply tissue requirements and, at the same time, that

carbon dioxide produced in metabolism is removed quickly, preventing its buildup to toxic

levels In small insects and inactive stages of larger insects, diffusion of gases between the

spiracle and tracheoles is sufficiently rapid that these requirements are met However, if the

spiracles are kept permanently open, the amount of water lost via the tracheal system may

become important Thus, many insects utilize discontinuous gas exchange as a means of

reducing this loss The needs of large, active insects can be satisfied only by shortening the

distance over which diffusion must occur This is achieved by active ventilation movements

3.1 Diffusion

The absence of obvious breathing movements led many 19th century scientists to

assume that insects obtained oxygen by simple diffusion It was not, however, until 1920

that Krogh (cited in Miller, 1974) calculated, on the basis of (1) measurements of the

average tracheal length and diameter, (2) measurements of oxygen consumption, and (3)

the permeability constant for oxygen, that for Tenebrio and Cossus (goat moth) larvae at

rest with the spiracles open, the oxygen concentration difference between the spiracles and

tissues is only about 2% and easily maintainable by diffusion

Even in large active insects that ventilate (Section 3.3), diffusion is a significant process,

because the ventilation movements serve only to move the air in the larger tracheae For

example, in the dragonfly Aeshna, oxygen reaches the flight muscles by diffusion between

the primary (ventilated) air tubes and tracheoles, a distance of up to 1 mm Even in flight,

when the oxygen consumption of the muscle reaches 1.8 m1/g/min and the difference in

oxygen concentration between the primary tube and tracheoles is 5–13%, diffusion is quite

adequate (Weis-Fogh, 1964)

Diffusion is also important in moving gases between the tracheoles and mitochondria

of the tissue cells Because diffusion of dissolved gases is relatively slow, the distance over

which it can function satisfactorily (in structural terms, half the distance between adjacent

tracheoles) is directly related to the metabolic activity of the tissue In highly active flight

muscles of Diptera and Hymenoptera, for example, it has been calculated that the maximum

theoretical distance between tracheoles is 6–8µm In practice, tracheoles, which indent theµµ

muscle cells, are within 2–3µm ofµµ each other, allowing a significant “safety margin”

(Weis-Fogh, 1964)

In many insects, distal parts of tracheoles are not filled with air but liquid under normal

resting conditions During activity, however, the tracheoles become completely air-filled;

that is, fluid is withdrawn from them only to return when activity ceases Wigglesworth

(1953) suggested that the level of fluid in tracheoles depends on the relative strengths of the

capillary force drawing fluid along the tube and the osmotic pressure of the hemolymph

During metabolic activity, the osmotic pressure increases as organic respiratory substrates

are degraded to smaller metabolites, causing fluid to be withdrawn from the tracheoles

(perhaps via the pores mentioned earlier) and, therefore, bringing gaseous oxygen closer to

the tissue cells (Figure 15.5) As the metabolites are fully oxidized and removed, the osmotic

pressure will fall, and once again the capillary force will draw fluid along the tracheoles

Though carbon dioxide is more soluble, and has a greater permeability constant, than

oxygen in water and could conceivably move by diffusion through the hemolymph to leave

the body via the integument, this route does not normally eliminate a significant quantity

of the gas (e.g., 2–10% of the total in some dipteran larvae with thin cuticles) The great

majority of carbon dioxide leaves by gaseous diffusion via the tracheal system

FIGURE 15.5. Changes in level of tracheolar fluid as a result of muscular activity (A) Resting muscle; and (B)

active muscle [After V B Wigglesworth, 1965, The Principles of Insect Physiology, 6th ed., Methuen and Co.

By permission of the author.]

3.2 Discontinuous Gas Exchange

Originally discovered in diapausing pupae of Hyalophora cecropia and other

lep-idopterans, the discontinuous gas exchange cycle (DGC) [formerly known as passive (suction) ventilation] is now known to occur in all ants, many bees, some wasps, sev-eral different families of beetles, cockroaches, grasshoppers and locusts (Lighton 1996, 1998) The DGC, which makes use of the high solubility of carbon dioxide in water, com-prises three phases (Figure 15.6): constricted- or closed-spiracle phase, fluttering-spiracle phase, and open-spiracle phase In the constricted-spiracle phase the spiracular valves are kept almost closed As oxygen is used in metabolism, the carbon dioxide so produced is stored, largely as bicarbonate in the hemolymph and tissues but partially also in the gaseous state in the tracheal system Thus, a slight vacuum is created within the tracheal system that sucks in more air Eventually, the tracheal oxygen concentration falls to about 3.5% and the carbon dioxide concentration rises to about 4% At this point, the low oxygen concentration induces “fluttering” (rapid opening and closing of the valves), the effect of which is to allow some outward diffusion of nitrogen and more air to flow into the tracheal system However, carbon dioxide cannot escape and its concentration increases to about 6.5%, at which point the valves are opened and remain open between 15 and 30 minutes During this period there is rapid diffusion of carbon dioxide out of the tracheal system and massive release

of carbon dioxide from the hemolymph When the concentration of carbon dioxide in the tracheal system falls to 3.0%, the valves reclose Experiments in which gases of different composition are perfused through the tracheal system or over the segmental ganglia have shown that there is dual control over the opening of the valves Hypercapnia (above normal carbon dioxide concentration) directly stimulates relaxation of the valve closer muscle (the valve opens as a result of cuticular elasticity), whereas hypoxia (insufficient oxygen) acts at the level of the central nervous system (probably the metathoracic ganglion) In diapausing

Hyalophora pupae the periods between bursts of carbon dioxide release may be as long as

7 hours

For diapausing pupae and certain other postembryonic stages of insects, the slight net inflow of air during the constricted-spiracle phase of the DGC may serve as a means of conserving moisture that would otherwise be lost as a result of gas exchange However, there are many insects that show DGC but do not normally experience water-loss problems Conversely, there are many desert insects in which DGC does not occur This has led to the proposal that DGC evolved primarily to facilitate gas exchange in hypoxic and hypercapnic

GAS EXCHANGE

FIGURE 15.6. Discontinuous release of carbon dioxide in pupa of Hyalophora cecropia in relation to spiracular

valve opening and closing [After R I Levy and H A Schneiderman, 1966, Discontinuous respiration in insects.

IV, J Insect Physiol 12:465–492 By permission of Pergamon Press Ltd.]

environments (Lighton 1996, 1998) Certainly, DGC is common in some subterranean

groups, notably ants and beetles that burrow in soil, dung or wood However, there are

exceptions to this generalization, perhaps the major one being termites (Shelton and Appel,

2000, 2001) Further, some species that normally use DGC may abandon it under hypoxic

conditions (Chown and Holter, 2000; Chown, 2002)

3.3 Active Ventilation

By alternately decreasing and increasing the volume of the tracheal system through

compression and expansion of larger air tubes, a fraction of the air in the system is

pe-riodically renewed and the diffusion gradient between tracheae and tissues kept near the

maximum These breathing (ventilation) movements may be continuous as in locusts and

dragonflies, intermittent as in cockroaches, or occur only after activity as is seen in wasps

The volume changes are normally brought about by contraction of abdominal dorsoventral

and/or longitudinal muscles, which increases the hemolymph pressure, thus causing the

regions is induced indirectly, by contraction of mandible and leg muscles When these mus-cles relax, the elasticity in the taenidial rings returns the tracheae to their original shape and volume This discovery may require reconsideration of the proposal that diffusion alone satisfies the gas-exchange requirements of small insects

The diffusion gradient can be further improved by increasing the volume of air in the tracheal system that is renewed during each stroke (the tidal volume) This has been achieved through the development of large, compressible air sacs However, simple tidal flow (pumping of air in to and out of all spiracles) is still somewhat inefficient because a considerable volume of air (the dead air space) remains within the system at each stroke The size of the dead air space is greatly reduced by using unidirectional ventilation in which air is made to flow in one direction (usually anteroposteriorly) through the tracheal system Unidirectional airflow is achieved by synchronizing the opening and closing of spiracular valves with ventilation movements In the resting desert locust, for example, the first, second, and fourth spiracles are inspiratory, while the tenth (most posterior) is expiratory When the insect becomes more active, the first four spiracles become inspiratory, the remainder expiratory The spiracular valves do not form an airtight seal, however, so that a proportion

of the inspired air continues to move tidally rather than unidirectionally (20% in the resting desert locust)

During flight, the oxygen consumption of an insect increases enormously (up to 24 times in the desert locust), almost entirely because of the metabolic activity of the flight muscles To facilitate this activity, a massive exchange of air occurs in the pterothorax, made possible by certain structural features of the pterothoracic tracheal system and by changes

in the body’s normal (resting) ventilation pattern As noted earlier, the tracheal system of the pterothorax is effectively isolated from that of the rest of the body by reduction in the diameter or occlusion of the main longitudinal tracheae Autoventilation of flight muscle tracheae also occurs This is ventilation that results from movements of the nota and pleura during wing beating, and it brings about a considerable flow of air into and out of the thoracic tracheae During autoventilation, normal unidirectional flow, where such occurs, becomes masked by the massive increase in tidal flow in the pterothorax To achieve this tidal flow, in the desert locust, spiracles 2 and 3 remain permanently open Spiracles 1 and 4–10, however, continue to open and close in synchrony with abdominal ventilation so that some unidirectional flow occurs The rate of abdominal ventilation movements also increases during flight to about four times the resting value, but these movements probably serve primarily to increase the rate of flow of hemolymph around the body, bringing fresh supplies of metabolites to the flight musculature However, keeping the central nervous system well supplied with oxygen also appears to be important

Autoventilation is used by many Odonata, Orthoptera, Dictyoptera, Isoptera, Hemiptera, Lepidoptera, and Coleoptera, but is of little importance in Diptera and Hy-menoptera Its significance can be broadly correlated with body size, the type of muscles used in flight (Chapter 14, Section 2.1), and the extent of movements of the thorax during