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Scanning and transmission electron microscopic study of the tracheal air sac system in a grasshopper Chrotogonus senegalensis Kraus ФOrthopteraAcrididaePyrogomorphinae.

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THE ANATOMICAL RECORD 223:393-405 (1989)
Scanning and Transmission Electron Microscopic
Study of the Tracheal Air Sac System in a
Grasshopper Chrotogonus senegalensis (Kraus)0rt hoptera: Acrididae: Pyrgomorphinae
Department of Veterinary Anatomy, Faculty of Veterinary Medicine, University of Nairobi,
Nairobi Kenya
The morphology of the trachea-air sac system in a species of grasshopper Chrotogonus senegalensis has been studied by using scanning and transmission electron microscopes. Capacious air sacs were formed as dilatations along the
primary tracheal trunks. Narrower secondary trachea arose either directly from the
primary trachea that bypassed the air sacs or from the air sacs themselves. At or
close to the organ or tissue supplied with air, the secondary trachea gave rise to the
notably smaller tertiary trachea that penetrated the tissue, giving rise terminally
to the extremely small tracheoles that indent some cells. The trachea and the air
sacs were basically made up of an inner cuticular lining, helical taenidial rings, and
an overlying epithelial cell cover. The air sacs may be important in efficient ventilation of the respiratory system. The supply of air directly to the tissue cells was
viewed as an exemplary efficient design when compared to that prevailing in the
nontracheate air-breathing animals, where the vascular system is interposed between the respiratory organ and the target tissue cells. A similarity in the general
morphological design of the insect and avian respiratory systems has been observed,
mainly in respect to the presence of the air sacs and that of the respiratory shunts.
This, together with the reported functional features like the unidirectional mode of
ventilation, has been interpreted as a classic case of structural and functional
convergent evolution leading to the evolution of similar and comparably efficient respiratory systems capable of providing the large amount of oxygen demanded
by flight.
In the animal kingdom, active flight is unique to only
three groups of animals: insects (class Insecta), birds
(class Aves), and bats (order Chiroptera). These animals,
through adaptive radiation, have come to dominate the
living animals in respect to specific diversity (Pringle,
1957; Smith, 1968; Wimsatt, 1970; Callahan, 1972;
Rockstein, 1973; Yalden and Morris, 1975; Eisner and
Wilson, 1977). Grossly, these phylogenetically remarkably different groups of animals have acquired comparable aerodynamic morphological configuration in body
form, mainly that of having the wings which act as
aerofoils in providing and sustaining lift and maneuverability during flight. The energy requirements of flight
are remarkably high and largely beyond the reach of
most terrestrial animals (Tucker, 1969). The insects, for
example, increase their resting metabolic rate by a factor of well over 100 in flight (Krogh and Weis-Fogh,
1951; Weis-Fogh, 1964a) and maintain it entirely aerobically (Miller, 1974). The capacity for flight in some
animals is an outstanding example of behavioral convergent evolution that facilitates the exploitation of the
aerial ecological niche. This has taken place at different
geological times and in response to different selective
01989 ALAN R. LISS, INC.
forces. The insects were the first small animals to colonize the dry land with notable success, having established themselves by the late Devonian Period (345
million years ago) (Callahan, 1972).
The respiratory apparatus is the organ system most
sensitive to changes in energetic demands such as entailed in flight and has to be designed to operate optimally at two remarkably different metabolic levelsresting and flying (Weis-Fogh, 1964b).Pulmonary structural and functional adaptations in the bat and the bird
surpassing those of the other air-breathing vertebrates
have been elucidated (Dubach, 1981; Jurgens et al., 1981;
Maina and King, 1982a,b, 1984; Maina et al., 1982;
Maina, 1985; Lechner, 1985). The insects have evolved
the tracheal system, comparable to the vertebrate circulatory system, which delivers oxygen directly to the
tissue cells, a respiratory system which according to
Williams (1977) “embodies the refinement of biological
Received January 25,1988; accepted June 16,1988.
J.N. Maina’s present address is Department of Anatomy, School of
Veterinary Medicine, University of California, Davis, CA 95616. Address reprint requests there.
Figs. 1-4
engineering almost past belief.” The development,
structure, and function of the tracheal system has been
extensively investigated and reviewed (see Wigglesworth, 1931, 1953, 1954, 1959, 1972; Maloeuf, 1938;
Richards and Anderson, 1942a,b; Whitten, 1955, 1956,
1957, 1962, 1972; Edwards et al., 1958; Buck, 1962;
Shafiq, 1963; Weis-Fogh, 1964a,b; Uvarov, 1966; Peterson and Buck, 1968; Peterson, 1970; Miller, 1974; Wigglesworth and Lee, 1982). In spite of the numerous
studies, among others, Richards and Korda (19501, WeisFogh (1964a), Uvarov (1966), Whitten (19721, Miller
(1974), and Wigglesworth and Lee (1982) have pointed
out the diversity of organization of insect tissues. Such
immense detailed structural differences are undoubtedly a measure of the remarkable adaptive radiation the
insects have undergone. The prevailing incompleteness
of the structural and functional information, notably on
the respiratory system, was pointed out by Uvarov
(1966), who observed that “the knowledge of the insect
respiratory mechanisms is still inadequate,” and echoed
more recently by Tenney (1979) and Pringle (19831, who,
respectively, noted that “the kinds of structural data
that are required to deduce states of tissue oxygenation
under physiological conditions are simply not in hand”
and that “we still have a great deal to learn from them
[insects] for a better understanding of biological processes and of the design of efficient machinery.” Recently, Smith (1984) noted that “little is known about
the organization of air sacs” and further that “no detailed comparative survey of insect muscle tracheation
is available.”
The main objective of this study was t o examine, by
using scanning and transmission electron microscopes,
the topographic anatomy and the structure of the air
sacs and trachea in a species of grasshopper as an attempt to illustrate the pertinent structural features of
the insect respiratory system which are important in
gas exchange. Such studies are apparently lacking in
this species. Some similarity in the organization of the
insect and the avian respiratory systems was observed
and a possible explanation for this conformity is given.
Mature specimens of the grasshopper Chrotogonus s e
negalensis (Kraus, 1877) were kindly donated by the
Department of Zoology, University of Nairobi. They were
killed in an air-tight glass jar with chloroform soaked in
cotton wool after 2 days of examination for the mode
and frequency of respiration. The abdomen and the
thorax were opened under a dissecting microscope with
the specimens stuck on a board in a supine position, The
air sacs and the tracheal system particularly in the
flight muscles and the gastrointestinal system were
carefully studied. Tissue samples were taken and fixed
by immersion in 2.3% glutaraldehyde buffered in potassium phosphate (pH 7.4 and osmolarity 420 mOsm).
They were then dehydrated in five changes of absolute
alcohol after which they were trimmed to an appropriate
size, critical point dried in liquid carbon dioxide, stuck
on metal chucks, and sputtered with gold-palladium
complex before viewing on a Philips PSEM 275 scanning
electron microscope. The remaining tissues were diced
into small pieces (about 1 mm3) which were processed
for transmission electron microscopy by postfixation in
2% osmium tetroxide for 2 hours, en bloc stained in
uranyl acetate with maleic acid, and dehydrated in
graded concentrations of ethanol starting at 50%
through absolute and acetone before infiltration and
embedding in TAAB resin. Blocks were picked; ultrathin sections were cut, mounted on 200-mesh wire grids,
and subsequently stained with lead citrate before viewing on a Corinth AEI 275 electron microscope.
Respiration in C. senegalensis was observed to be aided
by abdominal pumping which during rest occurred at a
rate of 20 times per minute. The first eight cranial
abdominal segments were associated with paired left
and right air sacs which lay interposed between the gut
and the body wall (Figs. 1-3). These air sacs (Fig. 5),
which occurred singly, in pairs, or in groups of three,
were embedded in fat tissue. The single air sacs were
generally larger than the individual ones that composed
the doublets and the triplets. The air sacs were connected directly t o the spiracles and occasionally to the
adjacent spiracles by a longitudinal anastomic (intersegmental) tracheal chain (Figs. 3, 4). In this species, the
Fig. 1. A longitudinal view of the air sacs (As) and the main tracheal
trunks, the dorsal intersegmental trunk (Ds), the ventral tracheal air sacs in general decreased in size cranial-caudally.
trunk (Vt), and the lateral intersegmental trunk (St) in Chrotogonus Smaller air sacs (Figs. 2, 4, 10 inset) were observed
senegalensis. Sp, spiracle (others shown with arrows).
dorsal lateral to the gastrointestinal tract on the proximal segments. Conspicuously large air sacs (about 4 mm
Fig. 2. A close-up of the abdominal air sacs (As), the smaller dorsal
lateral air sacs, and the main tracheal trunks, these being the dorsal in diameter), which were bilaterally interposed between
intersegmental trunk (Ds), the ventral intersegmental trunk (Vt),and the flight muscles, were observed in this species of grassthe lateral intersegmental trunk (St). The arrows show the spiracles. hopper. Like the abdominal air sacs, the thoracic air
Gt, outline of the gastrointestinal tract.
sacs were buried in fat tissue. The air sacs were made
Fig. 3. A gross photograph of the abdomen showing the air sacs up of an epithelial cell cover, spiral taenidia, and an
(asterisks) lying next to the gastrointestinal tract (Gt) and the major inner cuticular lining (Figs. 5 inset, 10 inset).
tracheal trunks the lateral intersegmental (anastomotic) trunk (Ls)
The trachea, like the air sacs, consisted of an inner
and the primary trachea (Pt).Sp, spiracle. x 2 . Note that the air sacs cuticular lining underlain by an epicuticle thickened at
have been dissected out on one side of the gut to expose the primary
intervals to form regularly spaced circular threads, the
taenidia, and to the outside, an epithelial cell cover
Fig. 4. A transverse view of the abdomen of Chrotogonus senegalen- (Figs. 6, 8). The size and the frequency of the taenidia
sis showing thc main tracheal trunks. Sp, spiracle; Gt, gut; Dt, dorsal and the epithelial cell cover appeared to change as the
segmental trachea; Vt, ventral segmental trachea; Ls, lateral interseg- trachea decreased in size, the taenidia and the epithelial
mental trunk; Ds, dorsal intersegmental trunk; Dc, dorsal commissure;
Vc, ventral commissure. The dashed lines show the outlines of the cell cover being less prominent in the finer passages (cf.
Figs. 12, 13).
larger air sacs and the much smaller lateral ones relative to the gut.
Figs. 5 and 6
The tracheal supply to the flight muscles (Figs. 7, 8)
and to the gastrointestinal system (Figs. 9, 10) was notably profuse. In general terms, the tracheal system
could be divided into a primary set which consisted of
relatively large trachea with such trachea in the abdomen dividing to give rise to ventral, dorsal, and the
horizontal segmental branches (Fig. 4). The ventral and
dorsal branches united through the dorsal intersegmental trachea to form the respective longitudinal trunks.
The lateral intersegmental tracheal trunk constituted
the lateral longitudinal anastomotic chain. The primary
trachea either ran directly to give rise to the smaller
secondary trachea near the organ supplied with air or
emptied into the air sacs from where the secondary
trachea arose (Fig. 5). The secondary trachea divided
dichotomously, giving rise t o finer branches-the tertiary trachea-which invaded the tissues (Figs. 7-10),
where they gave way to the extremely small tracheoles
that interacted and, in some cases, as terminal tracheoles, entered the individual tissue cells (Figs. 11,15).In
some instances the elaborate division of the secondary
tracheal trunk on the surface of the flight muscle was
reminiscent of a motor nerve ending (Fig. 7).
The terminal tracheoles (Figs. 11, 13) had a mean
diameter of about 0.20 pm and on average lay as close
as 0.050 pm to the nearest mitochondrion in the flight
muscles of this species of grasshopper. In the intracytoplasmic invaginations of the terminal tracheoles in the
gut cells (Figs. 14, 15), some of the nearest mitochondria
were as close as 0.014 pm to a tracheole. The mitochondria were seen in such instances to aggregate around
the terminal tracheoles, a feature which appears to be
an attempt to decrease the diffusional pathway from the
tracheole; this relationship was termed by Edwards et
al. (1958) the tracheole-mitochondria continuum. The
tracheoles, both extracytoplasmic and intracytoplasmic,
were invested by tracheoblasts (Figs. 14,151.The intima
of the terminal tracheoles was surrounded by three concentric membranes: lying next to the tracheolar cuticle
was the intratracheal membrane (Fig. 15). Intracytoplasmically, this innermost layer was separated from
the peripheral plasma membrane by a very narrow space
of cytoplasm (about 0.03 pm) in width. The outermost
layer is separated from the tracheole by a relatively
wider space (0.04 pm) which is the invaginated circumtracheolar plasma membrane of the cell (Fig. 15). The
Fig. 5. Lateral abdominal air sacs (as) of the grasshopper Chrote
gonus senegalensis. The primary trachea (pt) run from the spiracle to
the air sac but in some areas run directly to the tissue, decreasing in
size to give rise t o the secondary trachea. The inset is an enlargement
of the boxed area to show secondary trachea (st) arising from the air
sac (as). te, tracheal epithelium; tn, taenidial rings. Figure 5 x33.
Inset, ~ 2 3 6 .
Fig. 6.Primary trachea (pt) running from the spiracles. The primary
trachea are joined by a n anastomotic chain (at). The primary trunks
give rise to dorsal and ventral branches which unite with their fellows
on the opposite side to constitute the dorsal and ventral tracheal
trunks. The anastornotic chain is seen to give rise to smaller trachea
(arrows)which supply air to the gastrointestinal system. mt, malpighian tubules. The inset is an enlargement of the boxed area. It shows
the taenidial rings that maintain the trachea patent. The epithelial
cell cover is shown with the arrow. st, secondary trachea. Figure 6,
x30. Inset, x 140.
tracheoblasts contained electron-dense granules and mitochondria (Figs. 14, 15). In the flight muscles, the mitochondria, with profuse cristae, virtually run from one Zline to another, contributing about 25% of the volume of
the muscle tissue. Haemolymphatic vessels could be discerned notably in the flight muscles (Fig. 11).In some of
these vessels haemocytes with large, centrally placed
nuclei and numerous cytoplasmic electron dense granules could be discerned (Fig. 11).
The insect tracheal respiratory system delivers oxygen directly to the mitochondria and takes away carbon
dioxide from the individual tissue cells (Snodgrass,1935;
Weis-Fogh, 1964a,b; Smith, 1968; Bursell, 1970; Wigglesworth, 1972; Miller, 1974; Bridges et al., 1980). In
mechanical terms the tracheal system efficiently acts
both as a compressor and as an exhaust pipe (Nachtigall,
1974). It is now well accepted that the tracheal system
develops as an invagination of the surface cuticle at the
spiracles (Wigglesworth, 1931, 1972; Snodgrass, 1935;
Locke, 1957, 1958a,b, 1974; Whitten, 1972; Smith, 1968;
Miller, 1974), accounting for the similarity and the reversal of the layers constituting the trachea. The main
tracheal trunks from the spiracles branch dichotomously, diminishing in size, ultimately giving rise to
the minute tubules-the tracheoles-which are intimately associated with the tissue cells. The doubts expressed by Snodgrass (1935) on the possibility of
intracellular penetration by the terminal tracheoles
have now been resolved by Edwards et al. (19581, Tahmisian and Devine (19571, and Wigglesworth and Lee
(1982)and in this study. The tracheolar cuticular intima
is ensheathed in a tracheoblast which is presumed to be
involved in its formation (Keister, 1948; Wigglesworth,
1954; Edwards et al., 1958;Locke, 1958a,b;Shafiq, 1963;
Whitten, 1972; Rockstein, 1973).The nature and degree
of tracheolization appear to depend on the metabolic
demands of a tissue (Buck, 1962; Whitten, 1972; Wigglesworth and Lee, 1982). The tracheoles, besides the
obvious difference in their smaller size, are said to differ
from trachea in that they are contained in single tracheal cells (Wigglesworth, 19541, have a smooth papillate intima (Edwards et al., 1958;Locke, 1958a)(features
both observed here in the grasshopper), in general do
not appear to be shed during molting (Keister, 1948;
Wigglesworth, 1954), lack taenidial ridges, and are usually less than 1 pm in diameter (Snodgrass, 1935; Wigglesworth and Lee, 1982). The growth of the tracheal
system appears to be coordinated such that the crosssectional area of the trachea and the tracheoles largely
remains constant (Bursell, 1970; Locke, 1958b),presumably maintaining a uniform or even reducing tracheal
air-flow resistance (Weis-Fogh,1964a,b, 1967) until the
tracheolar diameter may reach the mean free path of
the diffusing oxygen molecules when further reduction
in diameter would become a limiting factor to oxygen
diffusion (Pickard, 1974).
A notable variation apparently exists in the way that
the tracheoles interact with the tissue cells (Day, 1951;
Hodge, 1955; Edwards et al., 1958; Smith, 1968; Miller,
1974). In the order Odonata the flight muscles of the
dragonflies and the damselflies are devoid of intracellular tracheolar invaginations though the dragonflies are
considered to be strong fliers (Smith, 1966;Azuma et al.,
Figs. 7 and 8
1985).The lack of the tracheolar intracytoplasmic arborizations in this group of insects could be attributed to
the rather more primitive synchronous mode of contraction exhibited by their flight muscles, which are structurally similar to those of the vertebrates (Smith, 1966;
Pringle, 1983). In the mosquito, tracheal invaginations
are lacking in some organs like fat body, papillae, and
testes (Edwards et al., 1958) while in the cicadas the
invagination was not observed in the tymphal muscle
(Smith, 1968).A close relationship between the terminal
tracheoles and the mitochondria should increase the
tracheolar diffusing capacity. Weis-Fogh (196413) contended that without tracheolar indentation of the tissue
cell, oxygen supply would be inadequate in the insect’s
flight muscles. Weight for weight, the insect flight muscle is the most energetically active tissue known (WeisFogh, 1964b; Smith, 1977).This is reflected in the high
density of mitochondria in flight muscle, constituting up
to 3040% of this tissue (Edwards and Ruska, 1955;
Pringle, 1957,1983;Smith, 1961a,b, 1962;Wigglesworth
and Lee, 19821, values as high as 50% having been
reported by Ready (1983) in cricket flight muscle. Haemolymph in the majority of insects is not directly involved in gas transport as it largely lacks the oxygencarrying pigments (Florkin and Jeuniaux, 1974); the
insects have successfully thus dissociated the dependence of the respiratory and circulatory system that
typifies the vertebrates.
The air sacs constitute an integral part of the insect
respiratory system. Their structure and development
seem to differ from species to species, being absent in
the subclass Apterygota and well developed in the Diptera and Hymenoptera (Snodgrass, 1935). In the cicada
Fidicina monnifera the air sacs together with the tracheal system constitute 45% of the body volume (Bartholomew and Barnhart, 1984). In the honeybee, where the
air sacs are very well developed (Bets, 1923, 1933),the
air sacs have no taenidia; such air sacs may respond to
a greater extent to the increase and decrease in abdominal pressure and are more important in the ventilation
of the tracheal system (Snodgrass, 1935).The functional
anatomy of the air sacs in the insect respiratory system
has been subject to a lot of discussion and even speculation: they were considered to be inadequately studied by
Uvarov (1966), and functional analogy of the insect air
Fig. 7. Tracheal supply to the flight muscle (m). The secondary
trachea (st) give rise to the tertiary trachea (arrows) that invade the
muscle bundles, a pattern reminiscent of a motor nerve ending. The
figure is an enlargement of the enclosed area in the inset. The inset
shows secondary (st) and tertiary (tt)trachea invading the muscle im).
The flight muscles were particularly well supplied with air and had
an independent supply of air from paired thoracic air sacs. The arrow
in the inset shows a n uncoiled taenidium. Figure 7, ~1,044.Inset,
Fig. 8. A close-up of a tertiary tracheal (tt)penetrating into the flight
muscle (m). The tertiary trachea give rise to the tracheoles, which in
some tissues indent the cells as the terminal tracheoles. These minute
tubules could not clearly be viewed here, not only because of their
small size, but also because only the surface features are technically
examined with the SEM. The inset shows the taenidia (arrows)covered
by the glistening epithelial cell. The epithelial cell cover becomes less
pronounced in the smaller trachea (cf. with the tertiary trachea in the
same figure). Figure 8, x 420. Inset, X623.
sacs has even been drawn to the avian air sacs (WeisFogh, 1964a).The diverse functions of the air sacs in the
insect have been summarized by Wigglesworth (1963,
1972). Further, they are thought to act as bellows in
ventilating the tracheal system (Bets, 1933),to guarantee an intensive ventilation of the trachea during
breathing (Demoll, 19271, to act as sound resonators
(Pringle, 1957; Church, 19601, to act as heat insulators
(Weis-Fogh, 1964a1, to assist in egg laying and molting
(Clarke, 19571, and to permit the build-up of sufficient
pressure to supply air to smaller tracheae (McCutcheon,
1940). In Hymenoptera, there is a good correlation between the development of the air sacs and the size and
activity of the various species of insect (Tonapi, 1958).
The insects inspire a volume of air equal to two-thirds
the total volume of the tracheal system (Krogh, 1920b,
1941). This value was estimated at 5% at rest and at
20% in hyperventilation, with twice as high values expected in gravid females (Weis-Fogh,1967; Miller, 1974).
As much as 70% of the total tracheal volume may be
ventilated in a respiratory cycle in some insects (Bursell,
The pattern of the flow of the air in the tracheal
system has been debated for a long time. This could be
attributed to the notable interspecific differences in the
mode of air flow. While Snodgrass (1935) asserted that
“there is no law governing inhalation and exhalation of
the spiracles” and that “the respiratory currents may
alternate even in the same individual,” studies by Krogh
(1920a1, Lee (1925), McArthur (19291, McGoaan (1931),
Fraenkel (19321, Bailey (19541, and Weis-Fogh (1967)
have indicated what appears to be a definite pattern of
air flow which may change in respect to the prevailing
energetic demands. In the desert locust Schistocerca gregaria, during flight the air flows unidirectionally
through the thoracic spiracles, supplying the head and
the central nervous system and out through the abdominal spiracles, while at rest 50% of the total volume of
air ventilated by the abdomen passes unidirectionally
(Weis-Fogh,1967).In the honeybee, the tracheal air flow
has a strongly unidirectional component during flight
(Bailey, 1954). In Sphodromantis (Miller, 19741, 95% of
the inhaled air passes unidirectionally while only 5%
passes tidally when stimulated. Miller (1974) observed
that the synchronized spiracle movements that typify a
large number of orders of insects suggest that unidirectional air flow may be a universal feature in the larger
insects. The unidirectional mode of ventilation in the
respiratory organs is exhibited by diverse groups of animals such as some crustaceans, molluscs, and fish
(Miller, 1974), but among the terrestrial species, this is
only encountered in birds and insects. A plausible explanation for this similarity will be risked.
The avian pulmonary system consists of compact inexpansile lung which is ventilated by the concerted action
of the cranial and caudal groups of air sacs (for review
of anatomy see King, 1966; and Duncker, 1971). The
capacious air sacs can replenish the intrapulmonary air
in a single respiratory cycle. The flow of the air in the
parabronchial lumen (paleopulmo)is unidirectional and
continuous during the two phases of respiration (see
Scheid, 1979; Fedde, 1980; Burger, 1980; and Brackenbury, 1981, for recent reviews). In birds the air flow in
the parabronchial lumen is by bulk flow and is entirely
by diffusion in the exchange tissue. This compares with
Figs. 9 and 10
Figs. 11-13
Figs. 14 and t5
the nature of air flow in the tracheal system of the
larger insects, where the movement of the air is by bulk
flow in the trachea and by diffusion in the tracheoles.
The spatial relationship between the bulk parabronchial
air flow and the centripetal blood flow in the exchange
tissue of the bird lung is cross-current(Scheid and Piiper,
1972). This type of gas exchange design is apparently
the most efficient respiratory system to have evolved
among the air-breathing vertebrates, since for an equivalent degree of ventilation the avian lung extracts more
oxygen than the lungs of the other air-breathing vertebrates and the partial pressure of oxygen in the arterial
blood may exceed that in the end-expired air (Piiper and
Scheid, 1972). The pattern of gas exchange in insect
tissue at the tracheolar level, whether these gas exchange tubules are intra- or extracytoplasmic, would
appear to be a uniform pool (Piiper and Scheid, 1972)
and structurally similar to that of the nonavian airbreathing vertebrates (amphibians, reptiles, and mammals) at the faveolar/alveolar level. This is particularly
so as the terminal tracheoles appear to come to a dead
end and presumably do not anastomose with each other
(Wigglesworth and Lee, 1982). The tracheal system
should, however, be highly effkient, as the oxygen is
delivered directly to the mitochondria. Weis-Fogh
(1964a1, on functional grounds, first drew attention to
the similarity between the avian lung and the tracheal
system of the insect on the basis of the unidirectional
and continuous mode of ventilation. In birds the inhaled
air bypasses the gas-exchange part of the lung via the
intrapulmonary part of the primary bronchus to the
caudal air sacs (King, 1966; Duncker, 1971). In the locust, Weis-Fogh (1964a) observed tracheal shunts bypassing the immediate flight muscles to supply oxygen
to parts of the muscle farthest away from the spiracle.
Though in the bird lung the primary bronchus is basically a gas conduit, the shunting of the air from the
trachea to the posterior air sacs facilitates the continuous and unidirectional ventilation of the paleopulmonic
parabronchi which compose the bulk of the respiratory
tissue in some birds.
Fig. 9. The tracheal supply to the abdominal muscles (m). The secondary trachea (st) that arise from the primary trachea (see Fig. 6)
branch profusely, giving rise to the tertiary trachea (arrows) that
invade the muscle. The white arrowhead shows the luminal aspect of
the gastrointestinal tract. Like the flight muscles, the abdominal muscles were well supplied with air and mt for osmoregulation. The inset
(slightly enlarged area enclosed in the figure) shows the terminal parts
of the secondary trachea (st) giving rise to the tertiary trachea (arrows)
that penetrate the abdominal muscle (m). mt, malpighian tubules. Fig.
9, x27. Inset, ~ 3 7 .
The design specialization in the respiratory system of
insects and birds indicates the large demands to which
the system is subject because of their unique capacity
for flight. The structural and functional similarity in
insect and avian respiratory systems, in animals so phylogenetically remarkably different, could be viewed as a
classic case of systemic convergent evolution that has
given rise to highly efficient respiratory systems that
have enabled these animals to exploit the aerial ecological niche.
I wish to thank Prof. E.R. Weibel, the director of the
Institute of Anatomy, University of Bern, Switzerland,
in whose laboratory the SEM part of this work was
carried out. I am indebted to Dr. P. Gehr and Mr. K.
Babl for numerous courtesies during this time, without
which this work would not have been possible in the
present form. This study received generous financial
help from the Leverhulme Trust of London, for which I
am grateful.
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Fig. 12. A high-power view of a tertiary trachea (Tt) in the flight
muscle showing the characteristic tacnidia (Tnl overlaid by an epithelial cell (arrows). ~ 6 8 , 3 3 0 .
Fig. 13. A high-power view of a terminal tracheole (Tr)in the flight
muscle. Note the reduced sporadicity of the taenidia and the mitochondria (Mt) lying close to the tracheole. The arrows show the invagination of the sarcoplasmic membrane as the tracheole invades the muscle
tissue. ~ 1 2 6 , 7 0 0 .
Fig. 14. A high-power view of tracheoles (Tr),in the gastrointestinal
tract, contained in a tracheoblast. Note the numerous electron-dense
granules in the tracheoblast. The inset shows a single tracheole contertiary trachea (arrows) that penetrate the intestinal wall giving rise tained in a tracheoblast. These cells are associated with the develop.
to tracheoles (t); mt, the osmoregulatory malpighian tubules that sim- ment of the trachea. ~ 1 7 6 , 2 4 0Inset,
ilarly invade the gut wall (asterisk).The open arrow shows the luminal
Fig. 15. An intracytoplasmic extension of a tracheole (Tr)into a cell
aspect of the gut. The inset shows the smaller single air sacs (as)
located dorsal to the gastrointestinal tract. The arrows show the epi- of the gastrointestinal system. The membranes that surround the
tracheole in this very-high-power view are evident. From the inside
thelial cell cover and mt. Figure 10, x340. Inset, x50.
the tracheole is surrounded by an intratracheal membrane (It), a tracheal membrane (Tm), and the unit membrane (the plasma membrane)
Fig. 11. A transmission electron micrograph of the flight muscle of of the invaginated cell (Pm). Note the mitochondrion (Mt) in the cytoChrotogonus senegalensis showing a haemocyte (Hc) contained in a plasm of the tracheoblast (Tb).The arrows show mitochondria in the
haemolymphatic duct running next to the muscle. The terminal tra- cytoplasm (Ct) of the invaded cell lying in close proximity t o the
chea gives rise to the tracheoles (Tr)that invade the muscle and come terminal tracheole. The inset shows an invading tracheole transected
to lie next to the mitochondria (Mt). Sr, sarcoplasmic reticulum. longitudinally. The plasma membrane of the invaded cell (arrow) can
be seen. ~ 3 2 2 , 4 2 4 Inset,
Fig. 10. A transverse view of the gastrointestinal tract showing the
tracheal air supply. The secondary trachea (st) give rise to the short
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