15
G
as Exchan
g
e
1
. Intr
oduc
t
ion
I
n all or
g
anisms
g
as exchan
g
e, the suppl
y
of ox
yg
en to and removal of carbon dioxide fro
m
cells, depends ultimatel
y
on the rate at which these
g
ases diffuse in the dissolved state. Th
e
d
iffusion rate is proportional to (1) the surface area over which diffusion is occurrin

g
and (2
)
th
e
diff
us
i
on gra
di
ent (concentrat
i
on
diff
erence o
f
t
h
e
diff
us
i
ng mater
i
a
lb
etween t
h
etw
o

po
i
nts un
d
er cons
id
erat
i
on
di
v
id
e
db
yt
h
e
di
stance
b
etween t
h
etwopo
i
nts). D
iff
us
i
on a
l

one,
th
ere
f
ore, as a means o
f
o
b
ta
i
n
i
n
g
ox
yg
en or excret
i
n
g
car
b
on
di
ox
id
e can
b
e emp
l

o
y
e
d
onl
y
b
y
small or
g
anisms whose surface area/volume ratio is hi
g
h (i.e., where all cells ar
e
relativel
y
close to the surface of the bod
y
) and or
g
anisms whose metabolic rate is low
.
Organ
i
sms t
h
at are
l
arger an
d

/or
h
ave a
hi
g
h
meta
b
o
li
c rate must
i
ncrease t
h
e rate at w
hi
c
h
gases move
b
etween t
h
eenv
i
ronment an
d
t
h
e
b

o
d
yt
i
ssues
b
y
i
mprov
i
ng (1) an
d
/or (2
)
a
b
ove.Inot
h
er wor
d
s, spec
i
a
li
ze
d
resp
i
rator
y

structures w
i
t
hl
ar
g
e sur
f
ace areas an
d
/or
t
ransport s
y
stems that brin
g
lar
g
e quantities of the
g
as closer to the site of use or disposa
l
(thereb
y
improvin
g
the diffusion
g
radient) have been developed. For most terrestrial animals
prevent

i
on o
fd
es
i
ccat
i
on
i
s anot
h
er
i
mportant pro
bl
em, an
d
t
hi
s
h
as
h
a
d
ama
j
or
i
n

fl
uenc
e
on t
h
e
d
eve
l
opment o
f
t
h
e
i
r resp
i
ratory sur
f
aces t
h
roug
h
w
hi
c
h
cons
id
era

bl
e
l
oss o
f
wate
r
m
igh
t occur. T
y
p
i
ca
lly
, resp
i
rator
y
sur
f
aces o
f
terrestr
i
a
l
an
i
ma

l
s are
f
orme
d
as
i
nva
gi
nate
d
structures within the bod
y
so that evaporative water loss is
g
reatl
y
reduced.
I
n insects the tracheal s
y
stem, a series of
g
as-filled tubes derived from the inte
g
ument
,
h
as evo
l

ve
d
to cope w
i
t
h
gas exc
h
ange. Term
i
na
ll
yt
h
etu
b
es are muc
hb
ranc
h
e
d
,
f
orm
i
n
g
t
rac

h
eo
l
es t
h
at prov
id
e an enormous sur
f
ace area over w
hi
c
h diff
us
i
on can occur. Furt
h
er-
more, trac
h
eo
l
es are so numerous t
h
at
g
aseous ox
yg
en rea
dily

reac
h
es most parts o
f
t
he
b
od
y
, and, equall
y
, carbon dioxide easil
y
diffuses out of the tissues. Thus, in most insects,
in contrast to man
y
other animals, the circulator
y
s
y
stem is unimportant in
g
as transport
.
B
ecause they are in the gaseous state within the tracheal system, oxygen and carbon dioxid
e
diff
use rap
idl

y
b
etween t
h
et
i
ssues an
d
s
i
te o
f
upta
k
eorre
l
ease, respect
i
ve
l
y, on t
h
e
b
o
d
y
sur
f
ace. Oxygen,

f
or examp
l
e,
diff
uses 3 m
illi
on t
i
mes
f
aster
i
na
i
rt
h
an
i
n water (M
ill
,
1972). A
g
ain, because the s
y
stem is
g
as-filled, much lar
g

er quantities of ox
yg
en can reac
h
t
he tissues in a
g
iven time. (Air has about 25 times more ox
yg
en per unit volume than water.)
The eminent suitability of the tracheal system for gas exchange is illustrated by the fac
t
th
at,
f
or most sma
ll i
nsects an
d
many
l
arge
i
nsects at rest, s
i
mp
l
e
diff
us

i
on o
f
gases
i
n/ou
t
4
6
9
4
7
0
CHAPTER
15
o
f the tracheal s
y
stem entirel
y
satisfies their requirements (but see Section 3.3). In lar
g
e,
active insects the
g
radient over which diffusion occurs is increased b
y
means of ventilation;
that is, air is activel
y

pumped throu
g
h the tracheal s
y
stem.
2
. Organization and Structure of the Tracheal Syste
m
A tracheal s
y
stem is present in all Insecta and in other hexapods with the exception of
t
h
e Protura an
d
many Co
ll
em
b
o
l
a. It ar
i
ses
d
ur
i
ng em
b
ryogenes

i
sasaser
i
es o
f
segmenta
l
i
nvag
i
nat
i
ons o
f
t
h
e
i
ntegument. Up to 12 (3 t
h
orac
i
can
d
9a
bd
om
i
na
l

)pa
i
rs o
f
sp
i
rac
l
es
m
a
y
be seen in embr
y
os, thou
g
h this number is alwa
y
s reduced prior to hatchin
g
, and furthe
r
reduction ma
y
occur in endopter
yg
otes durin
g
metamorphosis. Various terms are used to
describe the number of

p
airs of functional s
p
iracles, for exam
p
le, holo
p
neustic (10
p
airs
,
l
ocate
d
on t
h
e mesot
h
orax an
d
metat
h
orax an
d
8a
bd
om
i
na
l

segments), amp
hi
pneust
i
c
(
2pa
i
rs, on t
h
e mesot
h
orax an
d
at t
h
et
i
po
f
t
h
ea
bd
omen), an
d
apneust
i
c (no
f

unct
i
ona
l
sp
i
rac
l
es). T
h
e
l
ast con
di
t
i
on
i
s common
i
n aquat
i
c
l
arvae, w
hi
c
h
are sa
id

,t
h
ere
f
ore, to
h
ave
a closed tracheal s
y
stem (Section 4.1)
.
T
he proportion of the bod
y
filled b
y
the tracheal s
y
stem varies widel
y
, both amon
g
spec
i
es an
d
w
i
t
hi

nt
h
e same
i
n
di
v
id
ua
l
t
h
roug
h
out a sta
di
um. In act
i
ve
i
nsects w
h
ose trac
h
ea
l
system
i
nc
l

u
d
es a
i
r sacs (see
b
e
l
ow) t
h
e trac
h
ea
l
system occup
i
es a greater
f
ract
i
on o
f
t
h
e
b
o
dy
t
h

an
i
n
l
ess act
i
ve spec
i
es. Furt
h
er,
i
nt
h
e
f
ormer, t
h
evo
l
ume o
f
t
h
e trac
h
ea
l
s
y

stem
m
a
y
decrease dramaticall
y
durin
g
a stadium (e.
g
., i
n
L
ocusta from 48% to 3%
)
as th
e
air sacs become occluded b
y
the increased hemol
y
mph pressure that results from tissu
e
growt
h
.A
f
ter ec
d
ys

i
s, w
h
en
b
o
d
yvo
l
ume
h
as
i
ncrease
d
(C
h
apter 11, Sect
i
on 3.2), t
he
trac
h
ea
l
system expan
d
s
b
ecause o

f
t
h
e
l
owere
dh
emo
l
ymp
h
pressure.
2
.
1
.Tr
ac
h
eae a
n
d
Tr
ac
h
eo
l
es
In apterygotes otherthanlepismatid Zygentoma, thetracheae that run fromeach spiracle
d
o not anastomose e

i
t
h
er w
i
t
h
t
h
ose
f
rom a
dj
acent segments or w
i
t
h
t
h
ose
d
er
i
ve
df
ro
m
t
h
esp

i
rac
l
eont
h
e oppos
i
te s
id
e. In t
h
e Lep
i
smat
id
ae an
d
Pterygota
b
ot
hl
ong
i
tu
di
na
l
an
d
transverse anastomoses occur, and, thou

g
h minor variations can be seen, the resultant patter
n
o
f the tracheal s
y
stem is often characteristic for a particular order or famil
y
. Generall
y
, a pai
r
o
f large-diameter, longitudinal tracheae (the lateral trunks) run along the length of an insect
j
ust
i
nterna
l
to t
h
esp
i
rac
l
es. Ot
h
er
l
ong

i
tu
di
na
l
trun
k
s are assoc
i
ate
d
w
i
t
h
t
h
e
h
eart, gut, an
d
v
entra
l
nerve cor
d
. Interconnect
i
ng t
h

e
l
ong
i
tu
di
na
l
trac
h
eae are transverse comm
i
ssures,
usuall
y
one dorsal and another ventral, in each se
g
ment (Fi
g
ure 1
5
.1). Parts of the tracheal
s
y
stem, for example, that of the pterothorax, ma
y
be effectivel
y
isolated from the rest of
the s

y
stem b
y
reduction of the diameter or occlusion of certain lon
g
itudinal trunks. This
arrangement
i
s assoc
i
ate
d
w
i
t
h
t
h
e use o
f
autovent
il
at
i
on as a means o
fi
mprov
i
ng t
h

e supp
l
y
of
oxygen to w
i
ng musc
l
es
d
ur
i
ng
fli
g
h
t (Sect
i
on 3.3). A
l
so, trac
h
eae are o
f
ten
dil
ate
d
t
o

f
orm
l
ar
g
et
hi
n-wa
ll
e
d
a
i
r sacs t
h
at
h
ave an
i
mportant ro
l
e
i
n vent
il
at
i
on (Sect
i
on 3.3) an

d
o
ther functions
.
N
umerous smaller tracheae branch off the main tracts and under
g
o pro
g
ressive subdi
-
v
ision until at a diameter of about 2–
5
µ
m they form a number of fine branches each 1
µµ
µ
m
µ
µ
o
r
l
ess across
k
nown as trac
h
eo
l

es. Trac
h
eo
l
es are
i
ntrace
ll
u
l
ar,
b
e
i
ng enc
l
ose
d
w
i
t
hi
n
a
v
er
y
thin la
y
er of c

y
toplasm from the tracheoblast (tracheal end cell) (Fi
g
ure 1
5
.2), and
ramif
y
throu
g
hout most tissues of the bod
y
. The
y
are especiall
y
abundant in metabolicall
y
active tissues. Thus, in fli
g
ht muscles, fat bod
y
, and testes, for example, tracheoles indent
4
7
1
GAS
EX
C
H

A
N
G
E
F
I
GU
RE 15.1.
(
A) Dorsal tracheal system of abdomen of locust; and (B) diagrammatic transverse sectio
n
t
hrough abdomen of a hypothetical insect to illustrate main tracheal branches. [A, from F. O. Albrecht, 1953, T
h
e
Anatomy o
f
t
h
e Migratory Locust
.
By
perm
i
ss
i
on o
f
At
hl

one Press. B,
f
rom R. E. Sno
dg
rass,
P
rincip
l
es o
f
Insec
t
Morpholo
gy.
Copyright 1935 by McGraw-Hill, Inc. Used with permission of McGraw-Hill Book Company.]
i
n
di
v
id
ua
l
ce
ll
s, so t
h
at gaseous oxygen
i
s
b

roug
h
t
i
nto extreme
l
yc
l
ose prox
i
m
i
ty w
i
t
h
t
he
ener
gy
-pro
d
uc
i
n
g
m
i
toc
h

on
d
r
i
a.
I
n Cal
p
odes ethlius cater
p
illars not all tracheae end in tracheoles within or on tissues.
I
n particular, some tracheae ori
g
inatin
g
from the spiracles of the ei
g
hth abdominal se
g
men
t
4
7
2
CHAPTER
15
F
I
GU

RE 15.2. Structure of (A) large; and (B) small tracheae. (C) Origin of tracheole. [After V. B. Wigglesworth,
1
965, T
h
e Princip
l
es of Insect P
h
ysio
l
og
y
,6
th ed., Methuen and Co. By permission of the author.]
f
orm large, greatly branched tufts that are suspended within the hemolymph (Figure 15.3).
T
h
e trac
h
eo
l
ar t
i
ps o
f
t
h
ese tu
f

ts are connecte
d
to
h
eart an
d
ot
h
er musc
l
es so t
h
at t
h
etu
f
ts are
c
onstant
l
y move
d
w
i
t
hi
nt
h
e
h

emo
l
ymp
h
(Loc
k
e, 1998). T
h
eo
b
servat
i
on t
h
at
h
emocytes
w
ere abundant within the tufts led Locke to speculate that the tufts are sites of
g
as exchan
ge
f
or the blood cells, analo
g
ous to the lun
g
s of vertebrates. Thou
g
h similar tracheal tufts

are found in cater
p
illars from other le
p
ido
p
teran families, their existence and function(s
)
among ot
h
er
i
nsect groups
h
as not
b
een exam
i
ne
d
.
As
d
er
i
vat
i
ves o
f
t

h
e
i
ntegument, trac
h
eae compr
i
se cut
i
cu
l
ar components, ep
id
erm
i
s,
and basal lamina (Fi
g
ure 1
5
.2). Ad
j
acent to the spiracle, the tracheal cuticle includes, the
c
uticulin envelope, epicuticle and procuticle; in smaller tracheae and most tracheoles onl
y
the cuticulin envelope and epicuticle are present. Providin
g
the s
y

stem with stren
g
th
y
e
t
fl
ex
ibili
ty, trac
h
ea
l
cut
i
c
l
e
h
as
i
nterna
l
r
id
ges t
h
at may
b
ee

i
t
h
er separate (annu
li
)or
f
or
m
a cont
i
nuous
h
e
li
ca
lf
o
ld
(taen
idi
um). In
l
arge trac
h
eae t
h
er
id
ges

i
nc
l
u
d
e some procut
i
c
l
e
,
b
u
t
t
hi
s
i
sa
b
sent
f
rom t
h
ose o
f
trac
h
eo
l

es. Taen
idi
a are a
b
sent
f
rom, or poor
ly d
eve
l
ope
d
i
n, air sacs. The epicuticle of tracheae comprises the same la
y
ers as that of the inte
g
ument.
4
7
3
GAS
EX
C
H
A
N
G
E
F

I
GU
RE 15.3
.
Tu
f
ts o
f
trac
h
eae
i
nt
h
ee
igh
t
h
a
bd
om
i
na
l
se
g
ment o
f
Ca
l

po
d
es et
hl
ius
th
at
p
er
h
a
p
s serve to aerat
e
h
emocytes. Arrows indicate direction of hemolymph flow. [From M. Locke, 1998, Caterpillars have evolved lungs
f
or
h
emocyte gas exc
h
ange
,
J.
Insect P
h
ysio
l.
44
:1–20. W

i
t
h
perm
i
ss
i
on
f
rom E
l
sev
i
er.]
I
n the smallest tracheoles, however, onl
y
the cuticulin envelope is present and, furthermore
,
t
his contains fine pores. These two features ma
y
be associated with movement of liquid into
and out of tracheoles in connection with gas exchange (Section 3.1) (Locke, 1966)
.
2
.2. Spiracles
Onl
y
in some apter

yg
otes do tracheae ori
g
inate at the bod
y
surface. Normall
y
, the
y
arise sli
g
htl
y
below the bod
y
surface from which the
y
are separated b
y
a small cavit
y
,
t
he atrium (Fi
g
ure 15.4A). In this arran
g
ment, the term “spiracle”
g
enerall

y
includes bot
h
th
e atr
i
um an
d
t
h
es
pi
rac
l
e
s
en
s
u
s
tr
i
ct
o
,
t
h
at
i
s, t

h
e trac
h
ea
lp
ore. Exce
p
t
f
or t
h
ose o
fa
f
ew
i
nsects t
h
at
li
ve
i
n
h
um
id
m
i
croc
li

mates, sp
i
rac
l
es may
b
e covere
d
,
f
or examp
l
e,
by
th
ee
ly
tra or w
i
n
g
s
i
n Hem
i
ptera an
d
Co
l
eoptera, or are equ

i
ppe
d
w
i
t
h
var
i
ous va
l
ves
f
o
r
prevention of water loss. The valves ma
y
take the form of one or more cuticular plates that
can be pulled over a spiracle b
y
means of a closer muscle (Fi
g
ure l5.4B–D). Openin
g
of th
e
va
l
ve(s)
i

se
ff
ecte
d
e
i
t
h
er
b
yt
h
e natura
l
e
l
ast
i
c
i
ty o
f
t
h
e surroun
di
ng cut
i
c
l

eor
b
y an opene
r
musc
l
e. A
l
ternat
i
ve
l
y, t
h
eva
l
ve may
b
e a cut
i
cu
l
ar
l
ever w
hi
c
hb
y musc
l

e act
i
on constr
i
cts
t
he trachea ad
j
acent to the atrium (Fi
g
ure l
5
.4E,F). In lieu of, or in addition to, the valves
,
t
here ma
y
be hairs linin
g
the atrium or a sieve plate (a cuticular pad penetrated b
y
man
y
fi
ne pores) coverin
g
the atrial pore. It is commonl
y
assumed that an important function o
f

th
ese
h
a
i
rs an
d
s
i
eve p
l
ates
i
s to prevent
d
ust entry. However, as M
ill
er (1974) note
d
,s
i
eve
p
l
ates are not
b
etter
d
eve
l

ope
d
on
i
nsp
i
ratory t
h
an on exp
i
ratory sp
i
rac
l
es an
d
severa
l
ot
h
e
r
f
unct
i
ons can
b
e suggeste
d
: (1) t

h
ey may prevent water
l
ogg
i
ng o
f
t
h
e trac
h
ea
l
system
i
n
t
errestrial species durin
g
rain, in aquatic insects, and in species that live in moist soil, rottin
g
4
7
4
CHAPTER
15
F
IGURE 15.4.
S
p

i
racu
l
ar structure. (A) Sect
i
on t
h
roug
h
sp
i
rac
l
etos
h
ow genera
l
arrangement; (B, C) oute
r
an
di
nner v
i
ews o
f
secon
d
t
h
orac

i
csp
i
rac
l
eo
fg
rass
h
opper; (D)
di
a
g
rammat
i
c sect
i
on t
h
rou
gh
sp
i
rac
l
etos
h
ow
m
echanism of closure. The valve is opened by movement of the mesepimeron, closed by contraction of the

m
usc
l
e; (E) c
l
os
i
ng mec
h
an
i
sm on
fl
ea trac
h
ea; an
d
(F) sect
i
on t
h
roug
hfl
ea trac
h
ea at
l
eve
l
o

f
c
l
os
i
ng mec
h
an
i
sm.
[A–C,
f
rom R. E. Sno
dg
rass
,
Princip
l
es of Insect Morp
h
o
l
ogy . Cop
y
ri
g
ht 193
5
b
y

McGraw-Hill, Inc. Used wit
h
permission of McGraw-Hill Book Company. D, after P. L. Miller, 1960, Respiration in the desert locust. II. The
c
ontro
l
o
f
t
h
esp
i
rac
l
es
,
J. Exp. Bio
l
.
3
7:237–2
6
3. By permission of Cambridge University Press. E. F, after V. B.
Wi
gg
lesworth, 196
5
, T
h
e Princip

l
es of Insect P
h
ysio
l
og
y
,6
th ed., Methuen and Co. B
y
permission of the author.
]
ve
getat
i
on, etc.; (2) t
h
ey may prevent entry o
f
paras
i
tes, espec
i
a
ll
ym
i
tes,
i
nto t

h
e trac
h
ea
l
s
y
stem; and (3) the
y
ma
y
reduce bulk flow of
g
ases throu
g
h the s
y
stem caused b
y
bod
y
m
ovements, thereb
y
reducin
g
evaporative water loss. This would be disadvanta
g
eous in
i

nsects that ventilate the tracheal system, and it is of interest, therefore, that those spiracle
s
i
mportant
i
n vent
il
at
i
on common
l
y
l
ac
k
as
i
eve p
l
ate or
h
aveap
l
ate t
h
at
i
s
di
v

id
e
dd
own
t
h
em
iddl
esot
h
at
i
t may
b
e opene
dd
ur
i
ng vent
il
at
i
on
.
3. Movement of Gases within the Tracheal
S
ystem
Gas exc
h
an

g
e
b
etween t
i
ssues an
d
t
h
e trac
h
ea
l
s
y
stem occurs a
l
most exc
l
us
i
ve
ly
across
the walls of tracheoles, for it is onl
y
their walls that are sufficientl
y
thin as to permit a satis-
f

actor
y
rate of diffusion. It is necessar
y
, therefore, to ensure that a sufficient concentration of
4
7
5
GAS
EX
C
H
A
N
G
E
ox
yg
en is maintained in tracheoles to suppl
y
tissue requirements and, at the same time, tha
t
carbon dioxide produced in metabolism is removed quickl
y
, preventin
g
its buildup to toxic
levels. In small insects and inactive sta
g
es of lar

g
er insects, diffusion of
g
ases between th
e
sp
i
rac
l
ean
d
trac
h
eo
l
es
i
ssu
ffi
c
i
ent
l
y rap
id
t
h
at t
h
ese requ

i
rements are met. However,
if
t
h
e
sp
i
rac
l
es are
k
ept permanent
l
y open, t
h
e amount o
f
water
l
ost v
i
at
h
e trac
h
ea
l
system ma
y

b
ecome
i
mportant. T
h
us, man
yi
nsects ut
ili
ze
di
scont
i
nuous
g
as exc
h
an
g
e as a means o
f
reducin
g
this loss. The needs of lar
g
e, active insects can be satisfied onl
y
b
y
shortenin

g
the
d
istance over which diffusion must occur. This is achieved b
y
active ventilation movements.
3.1. D
iff
us
i
o
n
The absence of obvious breathin
g
movements led man
y
19th centur
y
scientists to
assume that insects obtained ox
yg
en b
y
simple diffusion. It was not, however, until 1920
t
hat Krogh (cited in Miller, 1974) calculated, on the basis of (1) measurements of the
a
v
erage trac
h

ea
ll
engt
h
an
ddi
ameter, (2) measurements o
f
oxygen consumpt
i
on, an
d
(3)
th
e permea
bili
ty constant
f
or oxygen, t
h
at
f
or Tene
b
ri
o
an
d
C
ossus (goat mot

h
)
l
arvae a
t
rest with the spiracles open, the ox
yg
en concentration difference between the spiracles and
t
issues is onl
y
about 2% and easil
y
maintainable b
y
diffusion
.
Even in large active insects that ventilate (Section 3.3), diffusion is a significant process,
b
ecause t
h
e vent
il
at
i
on movements serve on
l
ytomovet
h
ea

i
r
i
nt
h
e
l
arger trac
h
eae. Fo
r
examp
l
e,
i
nt
h
e
d
ragon
fl
y
A
e
sh
na
,
oxygen reac
h
es t

h
e
fli
g
h
t musc
l
es
b
y
diff
us
i
on
b
etween
th
epr
i
mar
y
(vent
il
ate
d
)a
i
rtu
b
es an

d
trac
h
eo
l
es, a
di
stance o
f
up to 1 mm. Even
i
n
fligh
t
,
w
hen the ox
yg
en consumption of the muscle reaches 1.8 m1/
g
/min and the difference in
ox
yg
en concentration between the primar
y
tube and tracheoles is 5–13%, diffusion is quit
e
adequate (Weis-Fogh, 1964).
D
iff

us
i
on
i
sa
l
so
i
mportant
i
nmov
i
ng gases
b
etween t
h
e trac
h
eo
l
es an
d
m
i
toc
h
on
d
r
ia

o
f
t
h
et
i
ssue ce
ll
s. Because
diff
us
i
on o
fdi
sso
l
ve
dg
ases
i
sre
l
at
i
ve
ly
s
l
ow , t
h

e
di
stance ove
r
w
hich it can function satisfactoril
y
(in structural terms, half the distance between ad
j
acen
t
t
racheoles) is directl
y
related to the metabolic activit
y
of the tissue. In hi
g
hl
y
active fli
g
h
t
muscles of Diptera and Hymenoptera, for example, it has been calculated that the maximum
t
heoretical distance bet
w
een tracheoles is
6

–
8
µ
m. In practice, tracheoles, which indent the
µ
µ
musc
l
ece
ll
s
,
are w
i
t
hi
n 2–3
µ
mof
µ
µ
e
ac
h
ot
h
er, a
ll
ow
i

ngas
i
gn
ifi
cant “sa
f
ety marg
i
n” (We
i
s-
F
o
g
h, 19
6
4)
.
I
n man
y
insects, distal parts of tracheoles are not filled with air but liquid under norma
l
resting conditions. During activity, however, the tracheoles become completely air-filled;
th
at
i
s,
fl
u

id i
sw
i
t
hd
rawn
f
rom t
h
em on
l
y to return w
h
en act
i
v
i
ty ceases. W
i
gg
l
eswort
h
(19
5
3) suggested that the level of fluid in tracheoles depends on the relative strengths of the
capillar
y
force drawin
g

fluid alon
g
the tube and the osmotic pressure of the hemol
y
mph.
Durin
g
metabolic activit
y
, the osmotic pressure increases as or
g
anic respirator
y
substrate
s
are de
g
raded to smaller metabolites, causin
g
fluid to be withdrawn from the tracheole
s
(per
h
aps v
i
at
h
e pores ment
i
one

d
ear
li
er) an
d
,t
h
ere
f
ore,
b
r
i
ng
i
ng gaseous oxygen c
l
oser t
o
t
he tissue cells (Figure 1
5
.
5
). As the metabolites are fully oxidized and removed, the osmoti
c
pressure w
ill f
a
ll

,an
d
once a
g
a
i
nt
h
e cap
ill
ar
yf
orce w
ill d
raw
fl
u
id
a
l
on
g
t
h
e trac
h
eo
l
es
.

Thou
g
h carbon dioxide is more soluble, and has a
g
reater permeabilit
y
constant, tha
n
ox
yg
en in water and could conceivabl
y
move b
y
diffusion throu
g
h the hemol
y
mph to leav
e
th
e
b
o
d
yv
i
at
h
e

i
ntegument, t
hi
s route
d
oes not norma
ll
ye
li
m
i
nate a s
i
gn
ifi
cant quant
i
ty
o
f
t
h
e gas (e.g., 2–10% o
f
t
h
e tota
li
n some
di

pteran
l
arvae w
i
t
h
t
hi
n cut
i
c
l
es). T
h
e grea
t
ma
j
or
i
t
y
o
f
car
b
on
di
ox
id

e
l
eaves
by g
aseous
diff
us
i
on v
i
at
h
e trac
h
ea
l
s
y
stem.
47
6
CHAPTER
15
F
I
GU
RE 15.5
.
Ch
an

g
es
i
n
l
eve
l
o
f
trac
h
eo
l
ar
fl
u
id
as a resu
l
to
f
muscu
l
ar act
i
v
i
t
y
. (A) Rest

i
n
g
musc
l
e; an
d
(B)
active muscle. [After V. B. Wigglesworth, 1965
,
T
he Principles o
f
Insect Physiology
,
6th ed., Methuen and Co
.
B
y perm
i
ss
i
on o
f
t
h
e aut
h
or.
]

3
.2. D
i
scont
i
nuous
G
as Exchange
O
ri
g
inall
y
discovered in diapausin
g
pupae o
f
H
yalophora cecropia and other le
p
-
i
dopterans, the discontinuous
g
as exchan
g
ec
y
cle (DGC) [formerl
y

known as passiv
e
(
suct
i
on) vent
il
at
i
on]
i
snow
k
nown to occur
i
na
ll
ants, many
b
ees, some wasps, sev
-
e
ral different families of beetles, cockroaches, grasshoppers and locusts (Lighton 1996,
1
998). T
h
e DGC, w
hi
c
h

ma
k
es use o
f
t
h
e
hi
g
h
so
l
u
bili
ty o
f
car
b
on
di
ox
id
e
i
n water, com-
prises three phases (Fi
g
ure 1
5
.6): constricted- or closed-spiracle phase, flutterin

g
-spiracl
e
p
hase, and o
p
en-s
p
iracle
p
hase. In the constricted-s
p
iracle
p
hase the s
p
iracular valves are
k
ept almost closed. As oxygen is used in metabolism, the carbon dioxide so produced is
store
d
,
l
arge
l
yas
bi
car
b
onate

i
nt
h
e
h
emo
l
ymp
h
an
d
t
i
ssues
b
ut part
i
a
ll
ya
l
so
i
nt
h
e gaseou
s
state
i
nt

h
e trac
h
ea
l
system. T
h
us,as
li
g
h
t vacuum
i
s create
d
w
i
t
hi
nt
h
e trac
h
ea
l
system t
h
at
sucks in more air. Eventuall
y

, the tracheal ox
yg
en concentration falls to about 3.
5
% and the
c
arbon dioxide concentration rises to about 4%. At this point, the low ox
yg
en concentratio
n
i
nduces “fluttering” (rapid opening and closing of the valves), the effect of which is to allo
w
some outwar
d diff
us
i
on o
f
n
i
trogen an
d
more a
i
rto
fl
ow
i
nto t

h
e trac
h
ea
l
system. However
,
c
arbon dioxide cannot escape and its concentration increases to about 6.
5
%, at which point
the valves are opened and remain open between 1
5
and 30 minutes. Durin
g
this period
there is rapid diffusion of carbon dioxide out of the tracheal s
y
stem and massive release
o
f carbon dioxide from the hemol
y
mph. When the concentration of carbon dioxide in the
trac
h
ea
l
system
f
a

ll
s to 3.0%, t
h
eva
l
ves rec
l
ose. Exper
i
ments
i
nw
hi
c
h
gases o
f diff
eren
t
c
ompos
i
t
i
on are per
f
use
d
t
h

roug
h
t
h
e trac
h
ea
l
system or over t
h
e segmenta
l
gang
li
a
h
av
e
s
h
own t
h
at t
h
ere
i
s
d
ua
l

contro
l
over t
h
e open
i
n
g
o
f
t
h
eva
l
ves. H
y
percapn
i
a(a
b
ove norma
l
c
arbon dioxide concentration) directl
y
stimulates relaxation of the valve closer muscle (the
v
a
lve opens as a result of cuticular elasticit
y

), whereas h
y
poxia (insufficient ox
yg
en) acts a
t
t
h
e
l
eve
l
o
f
t
h
e centra
l
nervous system (pro
b
a
bl
yt
h
e metat
h
orac
i
c gang
li

on). In
di
apaus
i
n
g
Hy
a
l
op
h
ora pupae t
h
e per
i
o
d
s
b
etween
b
ursts o
f
car
b
on
di
ox
id
ere

l
ease may
b
eas
l
ong as
7h
ours.
F
or
d
iapausin
g
pupae and certain other postembr
y
onic sta
g
es of insects, the sli
g
ht net
i
nflow of air durin
g
the constricted-spiracle phase of the DGC ma
y
serve as a means of
c
onserv
i
ng mo

i
sture t
h
at wou
ld
ot
h
erw
i
se
b
e
l
ost as a resu
l
to
f
gas exc
h
ange. However
,
t
h
ere are many
i
nsects t
h
at s
h
ow DGC

b
ut
d
o not norma
ll
y exper
i
ence water-
l
oss pro
bl
ems.
Converse
l
y, t
h
ere are many
d
esert
i
nsects
i
nw
hi
c
h
DGC
d
oes not occur. T
hi

s
h
as
l
e
d
to t
h
e
proposal that DGC evolved primaril
y
to facilitate
g
as exchan
g
einh
y
poxic and h
y
percapni
c
4
7
7
GAS
EX
C
H
A
N

G
E
F
I
GU
RE 15.6.
D
iscontinuous release of carbon dioxide in
p
u
p
ao
f
H
y
alophora cecropia in relation to s
p
iracular
valve opening and closing. [After R. I. Levy and H. A. Schneiderman, 1966, Discontinuous respiration in insects.
I
V
,
J
.
I
nsect P
h
ysio
l
.

12
:
46
5
–492. B
y
permission of Per
g
amon Press Ltd.
]
environments (Lighton 199
6
, 1998). Certainly, DGC is common in some subterranea
n
g
roups, nota
bly
ants an
db
eet
l
es t
h
at
b
urrow
i
nso
il
,

d
un
g
or woo
d
. However, t
h
ere are
exceptions to this
g
eneralization, perhaps the ma
j
or one bein
g
termites (Shelton and Appel,
2000, 2001). Further, some species that normall
y
use DGC ma
y
abandon it under h
y
poxi
c
con
di
t
i
ons (C
h
own an

d
Ho
l
ter, 2000; C
h
own, 2002)
.
3.3. Act
i
ve Vent
i
lat
i
o
n
B
y
alternatel
y
decreasin
g
and increasin
g
the volume of the tracheal s
y
stem throu
gh
compression and expansion of lar
g
er air tubes, a fraction of the air in the s

y
stem is pe-
riodically renewed and the diffusion gradient between tracheae and tissues kept near the
max
i
mum. T
h
ese
b
reat
hi
ng (vent
il
at
i
on) movements may
b
e cont
i
nuous as
i
n
l
ocusts an
d
d
ragon
fli
es,
i

nterm
i
ttent as
i
n coc
k
roac
h
es, or occur on
l
ya
f
ter act
i
v
i
ty as
i
s seen
i
n wasps.
T
he volume chan
g
es are normall
y
brou
g
ht about b
y

contraction of abdominal dorsoventra
l
and/or lon
g
itudinal muscles, which increases the hemol
y
mph pressure, thus causin
g
th
e
4
7
8
CHAPTER
15
tracheae to flatten or collapse. In some species both inspiration and expiration are brou
g
h
t
about b
y
muscles; in others, onl
y
expiration is under muscular control, and inspiration oc
-
c
urs as a result of the natural elasticit
y
of the bod
y

wall. Durin
g
hi
g
h metabolic activit
y,
supp
l
ementary vent
il
at
i
on movements may occur. For examp
l
e, t
h
e
d
esert
l
ocust norma
ll
y
v
ent
il
ates
b
y means o
fd

orsoventra
l
movements o
f
t
h
ea
bd
omen
b
ut can supp
l
ement t
h
es
e
by
“te
l
escop
i
n
g
”t
h
ea
bd
omen an
d
protract

i
on/retract
i
on o
f
t
h
e
h
ea
d
an
d
prot
h
orax (M
ill
er,
1
9
6
0). Remarkabl
y
, it has recentl
y
been reported that man
y
insects showin
g
no obvious si

g
ns
o
f breathin
g
have rapid c
y
cles of tracheal compression in the head and thorax (Westneat
et a
l.
,
2003). In ana
l
ogy w
i
t
h
t
h
es
i
tuat
i
on
i
nt
h
ea
bd
omen, trac

h
ea
l
compress
i
on
i
nt
h
ese
reg
i
ons
i
s
i
n
d
uce
di
n
di
rect
l
y,
b
y contract
i
on o
f

man
dibl
ean
dl
eg musc
l
es. W
h
en t
h
ese mus-
cl
es re
l
ax, t
h
ee
l
ast
i
c
i
ty
i
nt
h
e taen
idi
a
l

r
i
ngs returns t
h
e trac
h
eae to t
h
e
i
ror
i
g
i
na
l
s
h
ape an
d
v
olume. This discover
y
ma
y
require reconsideration of the proposal that diffusion alon
e
satisfies the
g
as-exchan

g
e requirements of small insects
.
T
he diffusion gradient can be further improved by increasing the volume of air in
t
h
e trac
h
ea
l
system t
h
at
i
s renewe
dd
ur
i
ng eac
h
stro
k
e(t
h
et
id
a
l
vo

l
ume). T
hi
s
h
as
b
ee
n
ac
hi
eve
d
t
h
roug
h
t
h
e
d
eve
l
opment o
fl
arge, compress
ibl
ea
i
r sacs. However, s

i
mp
l
et
id
a
l
flow (pumpin
g
of air in to and out of all spiracles) is still somewhat inefficient because
a
c
onsiderable volume of air (the dead air space) remains within the s
y
stem at each stroke.
The size of the dead air space is greatly reduced by using unidirectional ventilation in which
a
i
r
i
sma
d
eto
fl
ow
i
n one
di
rect
i

on (usua
ll
y anteroposter
i
or
l
y) t
h
roug
h
t
h
e trac
h
ea
l
system.
Un
idi
rect
i
ona
l
a
i
r
fl
ow
i
sac

hi
eve
db
y sync
h
ron
i
z
i
ng t
h
e open
i
ng an
d
c
l
os
i
ng o
f
sp
i
racu
l
a
r
v
alves with ventilation movements. In the restin
g

desert locust, for example, the first, second,
and fourth spiracles are inspirator
y
, while the tenth (most posterior) is expirator
y
. When
the insect becomes more active, the first four spiracles become inspirator
y
, the remainder
e
xp
i
ratory. T
h
esp
i
racu
l
ar va
l
ves
d
o not
f
orm an a
i
rt
i
g
h

t sea
l
,
h
owever, so t
h
at a proport
i
o
n
of
t
h
e
i
nsp
i
re
d
a
i
r cont
i
nues to move t
id
a
ll
y rat
h
er t

h
an un
idi
rect
i
ona
ll
y (20%
i
nt
h
e rest
i
n
g
d
esert
l
ocust
).
D
urin
g
fli
g
ht, the ox
yg
en consumption of an insect increases enormousl
y
(up to 24

times in the desert locust), almost entirel
y
because of the metabolic activit
y
of the fli
g
ht
m
usc
l
es. To
f
ac
ili
tate t
hi
s act
i
v
i
ty, a mass
i
ve exc
h
ange o
f
a
i
r occurs
i

nt
h
e pterot
h
orax, ma
d
e
poss
ibl
e
b
y certa
i
n structura
lf
eatures o
f
t
h
e pterot
h
orac
i
c trac
h
ea
l
system an
db
yc

h
anges
i
nt
h
e
b
o
d
y’s norma
l
(rest
i
ng) vent
il
at
i
on pattern. As note
d
ear
li
er, t
h
e trac
h
ea
l
system o
f
the pterothorax is effectivel

y
isolated from that of the rest of the bod
y
b
y
reduction in the
diameter or occlusion of the main lon
g
itudinal tracheae. Autoventilation of fli
g
ht muscl
e
tracheae also occurs. This is ventilation that results from movements of the nota and
p
leura
d
ur
i
ng w
i
ng
b
eat
i
ng, an
di
t
b
r
i

ngs a
b
out a cons
id
era
bl
e
fl
ow o
f
a
i
r
i
nto an
d
out o
f
t
he
t
h
orac
i
c trac
h
eae. Dur
i
ng autovent
il

at
i
on, norma
l
un
idi
rect
i
ona
lfl
ow , w
h
ere suc
h
occurs,
becomes masked b
y
the massive increase in tidal flow in the pterothorax. To achieve this
tidal flow, in the desert locust, spiracles 2 and 3 remain permanentl
y
open. Spiracles 1 an
d
4–10, however, continue to open and close in synchrony with abdominal ventilation so
t
h
at some un
idi
rect
i
ona

lfl
o
w
occurs. T
h
e rate o
f
a
bd
om
i
na
lv
ent
il
at
i
on mo
v
ements a
l
s
o
i
ncreases
d
ur
i
ng
fli

g
h
ttoa
b
out
f
our t
i
mes t
h
e rest
i
ng va
l
ue,
b
ut t
h
ese movements pro
b
a
bl
y
serve pr
i
mar
ily
to
i
ncrease t

h
e rate o
ffl
ow o
fh
emo
ly
mp
h
aroun
d
t
h
e
b
o
dy
,
b
r
i
n
gi
n
gf
res
h
supplies of metabolites to the fli
g
ht musculature. However, keepin

g
the central nervous
s
y
stem well supplied with ox
yg
en also appears to be important.
Autovent
il
at
i
on
i
s use
db
y many O
d
onata, Ort
h
optera, D
i
ctyoptera, Isoptera
,
H
em
i
ptera, Lep
id
optera, an
d

Co
l
eoptera,
b
ut
i
so
fli
tt
l
e
i
mportance
i
nD
i
ptera an
d
Hy-
m
enoptera. Its s
ig
n
ifi
cance can
b
e
b
roa
dly

corre
l
ate
d
w
i
t
hb
o
dy
s
i
ze, t
h
et
y
pe o
f
musc
l
es
used in fli
g
ht (Chapter 14, Section 2.1), and the extent of movements of the thorax durin
g
4
7
9
GAS
EX

C
H
A
N
G
E
fl
i
g
ht. Odonata, for example, are
g
enerall
y
lar
g
e; movements of their thorax durin
g
win
g
b
eatin
g
are pronounced and their fli
g
ht muscles are of the tubular t
y
pe which lack indente
d
t
racheoles. Therefore, autoventilation is extremel

y
important in this order. In contrast, i
n
Hymenoptera an
d
D
i
ptera, movements o
f
t
h
et
h
orax
i
n
fli
g
h
t are re
l
at
i
ve
l
ys
li
g
h
tsot

h
at t
he
vo
l
ume c
h
ange t
h
at can
b
eac
hi
eve
di
nt
h
e trac
h
ea
l
system
i
s not s
i
gn
ifi
cant. However, t
he
fi

brillar fli
g
ht muscles of these insects are much indented with tracheoles so that
g
aseou
s
ox
yg
en is brou
g
ht close to the mitochondria. Thus, in H
y
menoptera simple telescopic
abdominal ventilation normall
y
creates sufficient air exchan
g
e in the thorax. In Diptera,
a
bd
om
i
na
l
vent
il
at
i
on movements are wea
k

or non-ex
i
stent, an
d diff
us
i
on a
l
one sat
i
s
fi
es
th
e
i
nsects’ oxygen requ
i
rements
i
n
fli
g
h
t(M
ill
er, 1974)
.
Vent
il

at
i
on movements are
i
n
i
t
i
ate
d
w
i
t
hi
nan
d
contro
ll
e
d
v
i
at
h
e centra
l
nervous s
y
s
-

t
em. Some isolated abdominal se
g
ments, provided that the
y
contain a
g
an
g
lion, can carr
y
out normal respirator
y
movements, thou
g
h usuall
y
an appropriate stimulus such as h
y-
percapn
i
aor
h
ypox
i
a
i
s necessary to
i
n

i
t
i
ate t
h
e movements. T
h
e coor
di
nat
i
on o
f
t
h
es
e
autonomous vent
il
at
i
on movements an
d
,w
h
ere un
idi
rect
i
ona

l
a
i
r
fl
ow occurs, o
f
sp
i
racu
l
ar
va
l
ve open
i
n
g
an
d
c
l
os
i
n
g
,
i
sac
hi

eve
dby
a centra
l
pattern
g
enerator (CPG) s
i
tuate
d
usua
lly
in the metathoracic or first abdominal
g
an
g
lion. The nature of the CPG is not understood
.
However, in the desert locust, it sends bursts of impulses to each
g
an
g
lion, which bot
h
exc
i
te t
h
e motor neurons to t
h

e musc
l
es use
di
nexp
i
rat
i
on an
di
n
hibi
tt
h
ose go
i
ng to
i
n-
sp
i
ratory musc
l
es. T
h
e act
i
v
i
ty o

f
t
h
e CPG
i
smo
difi
e
db
y sensory
i
nput. For examp
l
e,
in
th
e
g
rass
h
oppe
r
T
aeniopo
d
ae
q
ues
r
eceptors

i
nt
h
e centra
l
nervous s
y
stem are sens
i
t
i
ve to
chan
g
in
g
carbon dioxide and ox
yg
en concentrations, which stimulate CPG activit
y
so that
ventilation is increased and decreased, respectivel
y
(Bustami
et al.
,
2002).
4.
G
as Exchange

i
n Aquat
i
c Insect
s
Perhaps not surprisin
g
l
y
, in view of the rapid rate at which
g
ases can diffuse within it
,
a
g
a
s-filled tracheal system has been retained by almost all aquatic forms in their evolutio
n
f
rom terrestr
i
a
l
ancestors. On
l
y rare
l
y,
f
or examp

l
e,
i
nt
h
e ear
l
y
l
arva
l
stages o
f
Ch
ironomus
an
d
S
imu
l
iu
m
(
D
i
ptera), an
d
A
centro
p

u
s
(Lep
id
optera),
i
st
h
e system
fill
e
d
w
i
t
hli
qu
id
.
Ox
yg
en ma
y
enter the tracheal s
y
stem in
g
aseous form, that is, via functional spiracle
s
(the “open” tracheal s

y
stem) or ma
y
pass, in solution, directl
y
across the bod
y
wall to the
t
racheal system, in which arrangement the spiracles are sealed (non-functional), and the
t
rac
h
ea
l
system
i
ssa
id
to
b
e“c
l
ose
d
.” Aquat
i
c
i
nsects w

i
t
h
open trac
h
ea
l
systems exc
h
ange
th
e gas w
i
t
hi
nt
h
e system
b
y per
i
o
di
ca
ll
yv
i
s
i
t

i
ng t
h
e water sur
f
ace,
b
yo
b
ta
i
n
i
ng gas
f
ro
m
g
as-filled spaces in aquatic plants, or throu
g
h the use of a “
g
as
g
ill” (a bubble or film of ai
r
t
hat covers the spiracles, in to or out of which ox
yg
en and carbon dioxide, respectivel

y
,ca
n
d
iffuse from/to the surrounding water). A significant amount of gas exchange may occu
r
b
y
di
rect
diff
us
i
on across t
h
e
b
o
d
y sur
f
ace (cutaneous resp
i
rat
i
on)
i
n
l
arvae w

i
t
h
an ope
n
system w
h
ose
i
ntegument
i
st
hi
n,
f
or examp
l
e, mosqu
i
to
l
arvae. Cutaneous resp
i
rat
i
on may
entirel
y
satisf
y

the requirements of insects with closed tracheal s
y
stems. However, in man
y
species supplementar
y
respirator
y
surfaces, “tracheal
g
ills,” have evolved, thou
g
h these
often become important only under oxygen-deficient conditions.
4.1. Closed Tracheal Systems
For
s
mall aquatic insects or those with a low metabolic rate, diffusion of
g
ases across th
e
b
od
y
wall provides an adequate means of obtainin
g
ox
yg
en and excretin
g

carbon dioxide.
480
CHAPTER
15
In lar
g
er and/or more active forms, all or part of the bod
y
wall has a ver
y
thin cuticle and
becomes richl
y
tracheated to facilitate rapid entr
y
and exit of
g
ases from the tracheal s
y
stem
.
S
ome tube-dwellin
g
species show rh
y
thmic movements that create water currents over th
e
b
o

d
ysot
h
at water
i
nt
h
etu
b
e
i
s per
i
o
di
ca
ll
y renewe
d
an
d
t
h
et
hi
c
k
ness o
f
t

h
e“
b
oun
d
ary
l
ayer” (t
h
e
l
ayer o
f
st
ill
water a
dj
acent to t
h
e
b
o
d
ywa
ll
)
i
sre
d
uce

d.
In man
y
aquat
i
c
l
arvae t
h
ere are r
i
c
hly
trac
h
eate
d
out
g
rowt
h
so
f
t
h
e
b
o
dy
wa

ll
(
hi
n
dg
u
t
i
n dra
g
onfl
y
larvae) collectivel
y
known as tracheal
g
ills. Whether these function as ac
-
c
essor
y
respirator
y
structures was ori
g
inall
y
controversial because even without them a
n
i

nsect may surv
i
ve per
f
ect
l
ywe
ll
an
di
ts oxygen consumpt
i
on may not c
h
ange. Trac
h
ea
l
g
ill
s
i
nc
l
u
d
e cau
d
a
ll

ame
ll
ae (
i
n Zygoptera),
l
atera
l
a
bd
om
i
na
l
g
ill
s(
i
nEp
h
emeroptera,
an
d
some Zygoptera, P
l
ecoptera, Neuroptera, an
d
Co
l
eoptera), recta

l
g
ill
s(
i
nAn
i
soptera)
,
and fin
g
erlike structures, often found in tufts on various parts of the bod
y
(e.
g
., in som
e
P
lecoptera and case-bearin
g
Trichoptera)
.
Juvenile Zygoptera have three caudal lamellae (Figure 6.11) whose functions have lon
g
been controversial (Burnside and Robinson, 199
5
), in large part because even without them
l
arvae surv
i

ve per
f
ect
l
ywe
ll
. Suggeste
d
uses o
f
t
h
e
l
ame
ll
ae
i
nc
l
u
d
esw
i
mm
i
ng, espec
i
a
ll

yto
av
oid predators, sacrificial structures for divertin
g
a predator’s attention, and
g
as exchan
g
e
.
There is evidence that all these possibilities ma
y
be important. For example, larvae wit
h
l
amellae missing are poorer swimmers than those with a full complement; further, ther
e
are s
i
gn
ifi
cant
diff
erences
i
nt
h
e
d
es

i
gn o
fl
ame
ll
ae
b
etween goo
d
an
d
poor sw
i
mmers. T
h
e
l
ame
ll
ae
h
ave a
b
rea
ki
ng
j
o
i
nt near t

h
e
i
r
b
ase, ena
bli
ng t
h
em to
b
es
h
e
d
eas
il
yw
h
en graspe
d
b
y
a predator. The lamellae are also hi
g
hl
y
tracheated, and experiments have demonstrated
that the lamellae normall
y

are ma
j
or sites of
g
as exchan
g
e and in ox
yg
en-deficient wate
r
become especiall
y
important. For example, in
C
oenagrion up to 60% of ox
yg
en uptake ma
y
o
ccur via the lamellae (Harnisch, 1958; cited from Mill, 1974). In certain Ena
ll
a
g
m
a
s
p
ec
i
e

s
n
orma
ll
arvae can surv
i
ve
i
n water w
i
t
h
an oxygen content o
f
on
l
y 2.4% saturat
i
on, w
h
ereas
the minimum for lamellaeless larvae is 14.
5
% saturation. Above this value
,
lamellaeles
s
l
arvae live apparentl
y

normall
y
and obtain sufficient ox
yg
en b
y
cutaneous diffusion (Pennak
and McColl, 1944
).
In
l
arva
l
Ep
h
emeroptera t
h
e
l
atera
l
a
bd
om
i
na
l
g
ill
s are pa

i
re
d
, segmenta
l
, norma
ll
y
platelike or branched structures (Figures 6.4–6.7) whose size is inversely related to the
o
xygen content o
f
t
h
e surroun
di
ng water. In ot
h
er or
d
ers, t
h
eg
ill
s are
fil
amentous (M
ill,
1
974). In burrowin

g
ma
y
fl
y
larvae and larvae of other species that live in an ox
yg
en-poo
r
e
nvironment, the
g
ills are an important site of
g
as exchan
g
e, and about 50% of an insect’
s
o
xygen requirement may be obtained via this route. In addition, their rhythmic beatin
g
f
ac
ili
tates cutaneous resp
i
rat
i
on
b

ymov
i
ng a current o
f
water over t
h
e
b
o
d
yan
d
re
d
uc
i
ng
t
h
et
hi
c
k
ness o
f
t
h
e
b
oun

d
ary
l
ayer. T
h
e
f
requency at w
hi
c
h
t
h
eg
ill
s
b
eat
d
epen
d
s
b
ot
h
o
n their size and on the ox
yg
en content of the water. In species that inhabit fast-flowin
g

w
ater, the
g
ills do not beat, and removal of them does not affect ox
yg
en consumption
,
i
ndicating that most gas exchange occurs cutaneously
.
Th
e anter
i
or part o
f
t
h
e rectum o
fl
arva
l
An
i
soptera
i
sen
l
arge
d
to

f
orm a
b
ranc
hi
a
l
ch
am
b
er w
h
ose wa
ll
s
b
ear s
i
xrowso
f
r
i
c
hl
y trac
h
eate
d
g
ill

s. Water
i
s per
i
o
di
ca
ll
y
d
rawn
i
nto an
df
orce
d
out o
f
t
h
e rectum v
i
at
h
e anus as a resu
l
to
f
muscu
l

ar movements o
f
t
he
abdomen, com
p
arable to those that effect ventilation in terrestrial s
p
ecies. Contraction of
dorsoventral muscles in the posterior abdominal se
g
ments decreases the abdominal volume
an
d
resu
l
ts
i
n water
b
e
i
ng
f
orce
d
out o
f
t
h

e rectum. A muscu
l
ar
di
ap
h
ragm
i
nt
h
e
fif
t
h
s
egment may prevent
h
emo
l
ymp
hf
rom
b
e
i
ng
f
orce
d
anter

i
or
l
y. Water enters t
h
e rectum a
s
t
h
evo
l
ume o
f
t
h
ea
bd
omen
i
s
i
ncrease
d,
as a resu
l
to
f
t
h
e contract

i
on o
f
two transverse
481
GAS
EX
C
H
A
N
G
E
muscles, the diaphra
g
m and subintestinal muscles, which pull the ter
g
al walls inward an
d
force the sterna downward. This is aided b
y
the natural elasticit
y
of the bod
y
wall and
by
relaxation of the dorsoventral muscles (Hu
g
hes and Mill, 1966; Mill, 1977). The rate

o
f
vent
il
at
i
on o
f
t
h
e
b
ranc
hi
a
l
c
h
am
b
er var
i
es w
i
t
h
t
h
e oxygen content o
f

t
h
e water an
d
meta
b
o
li
c rate o
f
t
h
e
i
nsect. Cutaneous resp
i
rat
i
on
i
s pro
b
a
bl
y not s
i
gn
ifi
cant
i

nAn
i
soptera
,
wh
ose
b
o
dy
wa
ll
cut
i
c
l
e
i
s
g
enera
lly
t
hi
c
k
. Recta
l
pump
i
n

g
a
l
so occurs
i
n
l
arva
l
Z
yg
optera,
t
hou
g
h its function here is primaril
y
in relation to ion uptake (Chapter 18, Section 4.2) as
t
hese insects lack rectal
g
ills (Miller, 1993).
4.2. Open Tracheal
S
ystems
Amon
g
insects that have an open tracheal s
y
stem can be traced a series of sta

g
es leadin
g
f
rom comp
l
ete
d
epen
d
ence on atmosp
h
er
i
ca
i
r(
i
.e., w
h
ere an
i
nsect must
f
requent
l
yv
i
s
i

t
th
e water sur
f
ace to exc
h
ange t
h
e gas
i
n
i
ts trac
h
ea
l
system) to t
h
e stage w
h
ere an
i
nsec
t
maintains around its bod
y
a suppl
y
of atmospheric
g

as into which ox
yg
en can diffuse fro
m
t
he surroundin
g
water at a sufficient rate to totall
y
satisf
y
the insect’s needs. Thus, the insec
t
is completely independent of atmospheric air.
S
ur
f
ace-
b
reat
hi
ng
i
nsects must so
l
ve two pro
bl
ems. F
i
rst, t

h
ey must prevent water
l
og
-
g
i
ng o
f
t
h
e trac
h
ea
l
system w
h
en t
h
ey are su
b
merge
d
,an
d
secon
d
,t
h
ey must

b
ea
bl
et
o
ov
e
rcome the surface tension force at the air-water interface. Both problems are solved b
y
h
avin
g
h
y
drofu
g
e (water-repellent) structures around the spiracles. In man
y
dipteran larva
e
special epidermal
g
lands (perispiracular/peristi
g
matic
g
lands) secrete an oil
y
material a
t

th
e entrance o
f
t
h
esp
i
rac
l
e. T
h
esp
i
rac
l
es o
f
some ot
h
er aquat
i
c
i
nsects are surroun
d
e
dby
h
y
d

ro
f
uge
h
a
i
rs, w
hi
c
h
,w
h
en su
b
merge
d
,c
l
ose over t
h
e open
i
ng
b
ut w
h
en
i
n contact w
i

t
h
t
he water surface spread out to permit exchan
g
e of air (Fi
g
ure 1
5
.7). In addition, insects
ma
y
possess other modifications to the tracheal s
y
stem to help cope with these problems
,
for exam
p
le, reduction of the number of functional s
p
iracles and restriction of the s
p
iracles
t
o spec
i
a
l
s
i

tes, typ
i
ca
ll
yatt
h
et
i
po
f
a poster
i
or extens
i
on o
f
t
h
e
b
o
d
y (posta
bd
om
i
na
l
respiratory siphon), as occurs in mosquito larvae (Figure 9.6F) and water scorpions (Figure
8.1

6
D). In larvae of some Syrphidae (e.g., Eri
s
ta
l
i
s
)
t
h
es
i
p
h
on
i
s very extens
ibl
e,
i
ts s
h
ap
e
and flexibilit
yg
ivin
g
rise to the common name of these insects—rattailed ma
gg

ots. In
a
few species of Coleoptera and Diptera, whose larvae live in mud, the siphon, which is ri
g
i
d
and
p
ointed, is forced into air s
p
aces in the roots of a
q
uatic
p
lants.
I
nsects
h
ave ga
i
ne
d
var
i
a
bl
e
d
egrees o
fi

n
d
epen
d
ence
f
rom atmosp
h
er
i
ca
i
r
b
y
h
o
ldi
n
g
a
g
a
s store a
b
out t
h
e
i
r

b
o
d
y. T
h
e gas store may
b
esu
b
e
l
ytra
l
or may occur as a t
hi
n
film
F
IGURE 15.7. H
yd
ro
f
u
g
e
h
a
i
rs sur
-

r
oundin
g
a spiracle. (A) Position whe
n
s
ubmerged; and (B) position when at water
s
urface. [After V. B. Wi
gg
lesworth, 196
5,
The Principles o
f
Insect Physiology
,
6th
ed., Methuen and Co. By permission of the
aut
h
or.
]
482
CHAPTER
15
F
IGURE 15.8
.
E
xamples of gas stores. (A) Hair pile on abdominal sternum o

f
A
p
helocheirus
(
Hemiptera); (B
)
sp
i
racu
l
ar
gill
o
f
pupa o
f
Psep
h
enoi
d
es ga
h
ani
(
Co
l
eoptera) compr
i
s

i
n
g
a
b
out 40
h
o
ll
ow
b
ranc
h
es; an
d
(C) part o
f
w
all of spiracular
g
ill branch of
P.
g
ahani
s
howin
g
cuticular struts that support the plastron. [A, after W. H. Thorpe
a
nd D. J. Crisp, 1947, Studies on plastron respiration. I. J. Ex

p
. Biol.
24
:227–269. By permission of Cambridg
e
Universit
y
Press. B, C, after H. E. Hinton, 19
6
8, Spiracular
g
ills
,
A
d
v. Insect P
h
ysio
l
.
5
:
6
5
–162. B
y
permission o
f
Academic Press Ltd.
]

o
f
g
as over certain parts of the bod
y
, held in place b
y
a mat of h
y
drofu
g
e hairs (Fi
g
ur
e
1
5.8A). A third arrangement is for the gas to be held as a layer adjacent to the body b
y
c
ut
i
cu
l
ar extens
i
ons o
f
t
h
e

b
o
d
ywa
ll
a
dj
acent to t
h
esp
i
rac
l
es,
k
nown as sp
i
racu
l
ar g
ills
(
Figure 1
5
.8B,C)
.
T
he de
g
ree of independence from atmospheric air (measured as the len

g
th of time tha
t
an insect is able to remain submer
g
ed between visits to the surface) depends on a number
o
f factors. These include (1) the metabolic rate of the insect, which itself is tem
p
erature-
d
epen
d
ent; (2) t
h
evo
l
ume, s
h
ape, an
dl
ocat
i
on o
f
t
h
e gas store, w
hi
c

hd
eterm
i
ne t
h
e sur
f
ac
e
area o
f
t
h
e store
i
n contact w
i
t
h
t
h
e water; an
d
(3) t
h
e oxygen content o
f
t
h
e water. Factor

s
(
2) an
d
(3) re
l
ate part
i
cu
l
ar
ly
to use o
f
t
h
e
g
as store as a p
hy
s
i
ca
l
(
g
as)
gill
,t
h

at
i
s,
a
structure that can take up ox
yg
en from the surroundin
g
water. When the ox
yg
en used b
y
an insect can be onl
y
partiall
y
replaced b
y
diffusion into the
g
as store of ox
yg
en from th
e
w
ater, t
h
evo
l
ume o

f
t
h
e gas store w
ill d
ecrease an
d
, eventua
ll
y, t
h
e
i
nsect must return t
o
t
h
e sur
f
ace to renew t
h
e gas store. T
hi
s
i
s
k
nown as a temporary (compress
ibl
e) gas g

ill.
W
h
en an
i
nsect’s ox
yg
en requ
i
rements can
b
e
f
u
lly
sat
i
s
fi
e
d by diff
us
i
on o
f
ox
yg
en
i
nto

the
g
ill, whose volume will therefore remain constant, the
g
ill is described as a permanent
(
incompressible)
g
as
g
ill or plastron
.
483
GAS
EX
C
H
A
N
G
E
I
n a compressible
g
ill the pressure of the
g
as will be equal to that of the surroundin
g
w
ater. The

g
as in the
g
ill ma
y
be considered to include onl
y
ox
yg
en and nitro
g
en, as th
e
carbon dioxide produced in metabolism will readil
y
dissolve in the water. Immediatel
y
afte
r
a
vi
s
i
ttot
h
e sur
f
ace, t
h
e compos

i
t
i
on o
f
t
h
e gas
i
nt
h
eg
ill
w
ill
approx
i
mate t
h
at o
f
a
i
r, t
h
a
t
i
s, a
b

out 20% oxygen an
d
80% n
i
trogen an
d
w
ill b
e
i
n equ
ilib
r
i
um w
i
t
h
t
h
e
di
sso
l
ve
d
gase
s
i
nt

h
e surroun
di
n
g
water. As an
i
nsect uses ox
yg
en, a
diff
us
i
on
g
ra
di
ent w
ill b
e set up s
o
t
hat this
g
as will tend to move into the
g
ill. At the same time, the proportion of nitro
g
e
n

in the
g
as will have increased and, therefore, nitro
g
en will tend to diffuse out of the
g
il
l
i
nor
d
er to restore equ
ilib
r
i
um. However, oxygen
diff
uses
i
nto t
h
eg
ill
a
b
out t
h
ree t
i
mes as

rap
idl
yasn
i
trogen
diff
uses out. T
h
us,
i
nwar
d
movement o
f
oxygen w
ill b
e more
i
mportan
t
th
an outwar
d
movement o
f
n
i
trogen
i
n restor

i
ng equ
ilib
r
i
um. T
h
ee
ff
ect o
f
t
hi
s
i
stopro
l
ong
considerabl
y
the life of the
g
as store and, therefore, the duration over which an insect ca
n
remain submer
g
ed. The rate of diffusion, which is a function of the surface area of th
e
gill exposed to the water, will obviously be greater in the case of films of gas spread ove
r

th
e
b
o
d
y sur
f
ace t
h
an
i
nsu
b
e
l
ytra
l
gas stores w
h
ose contact w
i
t
h
t
h
e surroun
di
ng water
is
re

l
at
i
ve
l
ys
li
g
h
t. U
l
t
i
mate
l
y,
h
owever,
i
n a compress
ibl
eg
ill
t
h
e rate o
f
oxygen use
b
yt

h
e
insect will reduce the proportion of ox
yg
en in the
g
ill below a critical level, and the insec
t
w
ill be stimulated to return to the surface.
F
o
re
xample, adult water beetles of the family Dytiscidae and back swimmers
(
Notonecta spp.: Hem
i
ptera) are genera
ll
yme
di
um to
l
arge
i
nsects, w
hi
c
hi
n summer, w

h
en
w
ater temperatures may approximate 20–2
5
◦
C, s
h
ow
g
reat act
i
v
i
t
y
.Un
d
er t
h
ese con
di
t
i
ons,
t
he
g
as stored beneath the el
y

tra (and also on the ventral bod
y
surface i
n
N
otonecta
)
mus
t
b
ere
g
ularl
y
exchan
g
ed b
y
visits to the water surface. However, in winter, when the water is
cold (or may even be continuously frozen for several months as occurs, for example, on th
e
Cana
di
an pra
i
r
i
es), t
h
e

i
nsects are more or
l
ess
i
nact
i
ve. Dur
i
ng t
hi
s per
i
o
d
,t
h
e gas stor
e
sat
i
s
fi
es most or a
ll
o
f
t
h
e

i
nsects’ oxygen requ
i
rements.
I
n contrast, the volume of a plastron is constant but small. Hence, a plastron doe
s
n
ot serve as a store of ox
yg
en but solel
y
as a
g
as
g
ill. In certain adult Hemiptera (e.
g
.
,
A
phelocheiru
s
) and Coleoptera (e.g.
,
E
lmis
)
the plastron is held in place by dense mats o
f

h
y
d
ro
f
uge
h
a
i
rs. T
h
e
h
a
i
rs num
b
er a
b
out 20
0
×
1
0
6
/
c
m
2
in

A
p
h
e
l
oc
h
eirus
,
are
b
ent at t
h
e
ti
p, an
d
are s
li
g
h
t
l
yt
hi
c
k
ene
d
at t

h
e
b
ase. As a resu
l
t, t
h
ey can res
i
st
b
ecom
i
ng
fl
attene
d
(
which would destro
y
the plastron) b
y
the considerable pressure differences that ma
y
arise
b
etween the
g
as in the plastron and the surroundin
g

water as the insect moves into deepe
r
w
ater or uses up its oxygen supply. Spiracular gills are mostly found on the pupae of certain
Di
ptera (e.g., T
i
pu
lid
ae an
d
S
i
mu
liid
ae) an
d
Co
l
eoptera (e.g., Psep
h
en
id
ae)
b
ut occas
i
ona
ll
y

occur on beetle larvae (Hinton, 19
6
8). In almost all instances they include a plastron. I
n
m
an
y
dipteran pupae the
g
ill is a lon
g
, hollowed-out structure (Fi
g
ure 1
5
.8C) that carrie
s
a plastron over its surface. The plastron is held in place b
y
means of ri
g
id cuticular struts
and connects via fine tubes with the gas-filled center of the gill (and hence the spiracle)
.
B
ecause t
h
evo
l
ume o

f
t
h
ep
l
astron rema
i
ns constant, t
h
en
i
trogen
d
oes not
diff
use out.
However, t
h
e rate an
ddi
rect
i
on o
f diff
us
i
on o
f
oxygen w
ill d

epen
d
on
diff
erences
i
nt
h
e
ox
yg
en content of the plastron (alwa
y
s somewhat less than maximum because of use of
ox
yg
en b
y
the insect) and the surroundin
g
water. Therefore, to ensure that ox
yg
en alwa
ys
d
iffuses into the plastron, the water around it should be saturated with the
g
as. If the wate
r
i

s not saturate
d
w
i
t
h
oxygen, t
h
en t
h
e
l
atter w
ill
e
i
t
h
er
diff
use
i
nto t
h
ep
l
astron re
l
at
i

ve
l
y
s
l
ow
l
y or may even
diff
use out,
l
ea
di
ng eventua
ll
ytoasp
h
yx
i
at
i
on o
f
t
h
e
i
nsect. It
i
sno

t
surpr
i
s
i
n
g
,t
h
en, to
di
scover t
h
at p
l
astron resp
i
rat
i
on
i
s use
dby
aquat
i
c
i
nsects
li
v

i
n
gi
n
f
ast
-
m
ovin
g
streams, at the ed
g
es of shallow lakes, and in the intertidal zone. Plastron-bearin
g
species known to inhabit water whose ox
yg
en content ma
y
fluctuate dail
y
, for example, that
484
CHAPTER
15
o
f marshes which drops
g
reatl
y
at ni

g
ht, ma
y
emplo
y
behavioral means to overcome the
dan
g
er of asph
y
xiation, such as movin
g
closer to the water surface or even climbin
g
out o
f
the water. Hinton (1968) also pointed out that the waters occupied b
y
plastron-bearers are
of
ten su
bj
ect to c
h
anges
i
n
l
eve
l

,
l
eav
i
ng t
h
e
i
nsects per
i
o
di
ca
ll
y expose
d
to atmosp
h
er
i
ca
i
r.
H
owever,
d
es
i
ccat
i

on
d
oes not present a pro
bl
em to t
h
ese
i
nsects
b
ecause t
h
e connect
i
o
n
between the plastron and internal tissues ma
y
be quite restricted. In addition, bulk flow of
g
as within the plastron is ne
g
li
g
ible, so that evaporative water loss is small
.
5. Gas Exchan
g
e in Endoparasitic Insects
It

i
s pro
b
a
bl
y not surpr
i
s
i
ng t
h
at en
d
oparas
i
t
i
c
i
nsects, as t
h
ey too are surroun
d
e
db
y
fl
u
id
,s

h
ow many para
ll
e
l
sw
i
t
h
aquat
i
c
i
nsects
i
nt
h
e way t
h
at t
h
ey o
b
ta
i
n oxygen. Most
e
n
d
oparas

i
tes sat
i
s
fy
a proport
i
on o
f
t
h
e
i
r requ
i
rements
by
cutaneous
diff
us
i
on. In some
first-instar larvae of H
y
menoptera and Diptera the tracheal s
y
stem ma
y
be liquid-filled, but
g

enerall
y
it is
g
as-filled with closed spiracles and includes a rich network of branches im
-
m
e
di
ate
l
y
b
eneat
h
t
h
e
i
ntegument. Many en
d
oparas
i
t
i
c
f
orms, espec
i
a

ll
y
l
arva
l
Bracon
id
ae,
C
h
a
l
c
idid
ae, an
d
Ic
h
neumon
id
ae (Hymenoptera), an
d
some D
i
ptera, possess ‘ta
il
s’
fill
e
d

wi
t
hh
emo
ly
mp
h
or can eva
gi
nate t
h
ewa
ll
o
f
t
h
e
hi
n
dg
ut t
h
rou
gh
t
h
e anus. It
h
as

b
ee
n
su
gg
ested that these structures ma
y
facilitate
g
as exchan
g
e, thou
g
h the evidence on whic
h
this su
gg
estion is based is
g
enerall
y
not stron
g
.
E
n
d
oparas
i
tes w

i
t
h
greater oxygen requ
i
rements usua
ll
y are
i
n
di
rect contact w
i
t
h
atmosp
h
er
i
ca
i
re
i
t
h
er v
i
at
h
e

i
ntegument o
f
t
h
e
h
ost or v
i
at
h
e
h
ost’s trac
h
ea
l
system.
In
l
arvae o
f
man
y
C
h
a
l
c
id

o
id
ea,
f
or examp
l
e, on
ly
t
h
e poster
i
or sp
i
rac
l
es are
f
unct
i
ona
l
,
and these open into an air cavit
y
formed at the base of the e
gg
pedicel that penetrates the
host’s inte
g

ument (Fi
g
ure 15.9A). Man
y
larval Tachinidae (Diptera) become enclosed in a
F
IGURE 15.9.
R
esp
i
rator
y
s
y
stems o
f
en
d
oparas
i
tes. (A) Larva o
f
B
l
astot
h
ri
x
(H
y

menoptera) attac
h
e
d
pos-
teriorl
y
to remains of e
gg
, thereb
y
maintainin
g
contact with the atmosphere via the e
gg
pedicel; and (B) larv
a
o
f
T
hr
ixio
n
(
Diptera) surrounded by the respiratory funnel formed by ingrowth of the host’s integument. [Fro
m
A. D. Imms
, 193
7
,

R
ecent A
d
vances in Entomo
l
ogy
,
2n
d
e
d
.B
y
perm
i
ss
i
on o
f
C
h
urc
hill
-L
i
v
i
n
g
stone, Pu

bli
s
h
ers.)
485
GAS
EX
C
H
A
N
G
E
respirator
y
funnel produced b
y
the host in an attempt to encapsulate the parasite (Fi
g
ure
15.9B). The funnel is produced b
y
inward
g
rowth of the host’s inte
g
ument or tracheal wall.
Within it, the parasite attaches itself b
y
means of mouth hooks while retainin

g
contact with
atmosp
h
er
i
ca
i
rv
i
at
h
e entrance o
f
t
h
e
f
unne
l.
6
.
S
ummar
y
The tracheal system is a system of gas-filled tubes that develops embryonically as
a
ser
i
es o

f
segmenta
li
nvag
i
nat
i
ons o
f
t
h
e
i
ntegument. T
h
e
i
nvag
i
nat
i
ons anastomose an
d
b
ranc
h
an
d
eventua
ll

y
f
orm trac
h
eo
l
es across w
hi
c
h
t
h
e vast ma
j
or
i
ty o
f
gas exc
h
ang
e
occurs. The external openin
g
s of the tracheal s
y
stem (spiracles) are
g
enerall
y

equipped
w
ith valves, hairs, or sieve plates, whose primar
y
function is probabl
y
prevention of wate
r
loss
.
Because oxygen can
diff
use more rap
idl
y
i
nt
h
e gaseous state an
di
s
i
n
hi
g
h
er con
-
centrat
i

on
i
na
i
rt
h
an
i
n water, t
h
e requ
i
rements o
f
most sma
ll i
nsects an
d
many
l
arge
restin
g
insects can be satisfied entirel
y
b
y
diffusion. Possibl
y
to reduce water loss or as

an adaptation to livin
g
in h
y
poxic or h
y
percapnic environments, some lar
g
er insects use
a
d
iscontinuous gas exchange cycle (DGC). In DGC the spiracles are kept almost closed an
d
car
b
on
di
ox
id
e
i
s temporar
il
y store
d
,
l
arge
l
yas

bi
car
b
onate
i
nt
h
e
h
emo
l
ymp
h
. As oxyge
n
i
s use
d
,as
li
g
h
t vacuum
i
s create
di
nt
h
e trac
h

ea
l
system t
h
at suc
k
s
i
n more a
i
ran
d
re
d
uces
outward diffusion of water vapor. Periodicall
y
, the spiracular valves are opened for a shor
t
t
ime when massive release of carbon dioxide occurs
.
To
i
ncrease the diffusion
g
radient between the tracheal s
y
stem and tissues, man
y

lar
g
e
i
nsects vent
il
ate t
h
e system
b
ya
l
ternate
l
y
i
ncreas
i
ng an
dd
ecreas
i
ng
i
ts vo
l
ume. Frequent
l
y
th

evo
l
ume o
f
t
id
a
l
a
i
r move
dd
ur
i
ng vent
il
at
i
on
i
s
i
ncrease
d
t
h
roug
h
t
h

e
d
eve
l
opment o
f
l
ar
g
e compress
ibl
ea
i
r sacs, an
dby
un
idi
rect
i
ona
l
a
i
r
fl
ow. Autovent
il
at
i
on, w

hi
c
h
re
li
e
s
on movements of the pterothorax durin
g
win
g
beatin
g
, occurs in man
yg
roups that have
s
y
nchronous fli
g
ht muscles
.
Aquat
i
c
i
nsects
h
ave e
i

t
h
erac
l
ose
d
trac
h
ea
l
system
i
nw
hi
c
h
t
h
esp
i
rac
l
es are sea
l
e
d
or an open trac
h
ea
l

system w
i
t
hf
unct
i
ona
l
sp
i
rac
l
es. In many
i
nsects w
i
t
h
ac
l
ose
d
tra-
c
h
ea
l
s
y
stem, cutaneous

diff
us
i
on ma
y
ent
i
re
ly
sat
i
s
fy
ox
yg
en requ
i
rements. Accessor
y
respirator
y
structures (tracheal
g
ills) ma
y
be present thou
g
h these are often important onl
y
u

nder ox
yg
en-deficient conditions. Some insects with open tracheal s
y
stems obtain ox
yg
en
b
y per
i
o
di
cv
i
s
i
ts to t
h
e water sur
f
ace, or
f
rom a
i
r spaces
i
np
l
ants. Ot
h

ers
h
o
ld
a store o
f
gas (gas g
ill
)a
b
out t
h
e
i
r
b
o
d
y. T
hi
s may
b
ee
i
t
h
er temporary, w
h
en an
i

nsect must v
i
s
it
th
e water sur
f
ace to renew t
h
eox
yg
en content o
f
t
h
e
gill
, or permanent (a p
l
astron), w
h
en
ox
yg
en is renewed b
y
diffusion into the
g
ill from the surroundin
g

medium
.
For
m
an
y
endoparasitic insects, cutaneous diffusion is sufficient to satisf
y
requirements.
I
n others there are s
p
ecial structural ada
p
tations that ensure that the
p
arasite remains in
contact w
i
t
h
atmosp
h
er
i
ca
i
r.
7. Literatur
e

G
as exchange is reviewed by Mill (1972, 1974, 198
5
), and Miller (1974). Hinton (1968)
d
iscusses spiracular
g
ills. The re
g
ulation of
g
as exchan
g
e is examined b
y
Miller (19
66
)
.
Whitten (1972) and Mill (1997) provide structural details of the tracheal s
y
stem.
4
86
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