Entomology 3rd edition - C.Gillott - Chapter 14 ppt

14
M
usc
l
es an
d
Locomotion
1
. Introductio
n
The ability to move is a characteristic of living animals and facilitates distribution, foo
d
p
rocurement, location of a mate or e
gg
-la
y
in
g
site, and avoidance of unsuitable conditions.
I
nsects,
l
ar
g
e
ly
t
h
rou
gh

t
h
e
i
ra
bili
t
y
to
fly
w
h
en a
d
u
l
t, are amon
g
t
h
e most mo
bil
ean
d
wid
e
ly di
str
ib
ute

d
o
f
an
i
ma
l
s. Deve
l
o
p
ment o
f
t
hi
sa
bili
t
y
ear
ly i
nt
h
eevo
l
ut
i
on o
f
t

h
ec
l
as
s
h
as made the Insecta the most diverse and successful animal group (Chapter 2, Section 3.1).
However, flight is only one method of locomotion employed by insects. Terrestrial specie
s
m
a
y
walk,
j
um
p
, or crawl over the substrate, or burrow within it. A
q
uatic forms can swim
i
navar
i
et
y
o
f
wa
y
s or run on t
h

e water sur
f
ace.
I
nt
h
e
i
r
l
ocomotor
y
movements,
i
nsects con
f
orm to norma
ldy
nam
i
can
d
mec
h
an
i
ca
l
pr
i

nc
i
p
l
es. However, t
h
e
i
r genera
ll
y sma
ll
s
i
ze an
dli
g
h
twe
i
g
h
t
h
ave
l
e
d
to t
h

e
d
eve
l
opment
of some unique structural, physiological, and biochemical features in their locomotor
y
s
y
s
t
ems
.
2
.
M
us
c
le
s
Essent
i
a
lly
,t
h
e structure an
d
contract
il

e mec
h
an
i
sm o
fi
nsect musc
l
es are com
p
ara
ble
t
ot
h
ose o
f
verte
b
rate s
k
e
l
eta
l
(cross-str
i
ate
d
) musc

l
e; t
h
at
i
s, t
h
ere are no musc
l
es
i
n
i
nsects
o
f the smooth (non-striated) type. Within muscle cells, the contractile elements actin and
m
yosin have been identified, and Huxley’s sliding filament theory of muscle contractio
n
a
pp
lies. Thou
g
h insect muscles are alwa
y
s cross-striated, there is considerable variation i
n
th
e
i

r structure,
bi
oc
h
em
i
str
y
,an
d
neura
l
contro
l
,
i
n accor
d
w
i
t
h
s
p
ec
i
fic
f
unct
i

ons
.
Because o
f
t
h
e
i
r sma
ll
s
i
ze an
d
t
h
evar
i
a
bl
e compos
i
t
i
on o
f
t
h
e
h

emo
l
ymp
h
o
fi
nsects
,
t
he neuromuscular system has some unique features (Hoyle, 1974). Being small, an insect
h
as a limited space for muscles which are, accordingly, reduced in size. Though this is
achieved to some extent b
y
a decrease in the size of individual cells (fibers), the
p
rinci
p
a
l
c
h
an
g
e
h
as
b
een a
d

ec
li
ne
i
nt
h
e num
b
er o
f
fi
b
ers
p
er musc
l
e suc
h
t
h
at some
i
nsect musc
l
es
compr
i
se on
l
y one or two ce

ll
s. T
h
us, to ac
hi
eve a gra
d
e
d
musc
l
e contract
i
on, eac
h
fi
b
er must
b
e capable of a variable response, in contrast to the vertebrate situation where graded muscle
r
esponses result in part from stimulation of a varied number of fibers. Similarly, the volume
o
f nervous tissue is limited
,
so that there are few motor neurons for the control of muscle
43
7
4
3

8
C
HAPTER
14
c
ontraction. The hemolymph surrounding muscles may contain high concentrations of ions
(es
p
eciall
y
divalent ions such as M
g
2
+
) (Cha
p
ter 17, Section 4.1.1) that could interfere with
i
m
p
u
l
se transm
i
ss
i
on at s
y
na
p

ses an
d
neuromuscu
l
ar
j
unct
i
ons. T
h
at t
hi
s
d
oes not occur
i
s
t
h
e resu
l
to
f
t
h
eevo
l
ut
i
on o

f
am
y
e
li
ns
h
eat
h
t
h
at covers
g
an
gli
a, nerves, an
d
neuromuscu
l
a
r
junctions
.
2.1. Stru
c
tur
e
Insect muscles can be arranged in two categories: (1) skeletal muscles whose functio
n
is to move one

p
art of the skeleton in relation to another, the two
p
arts bein
g
se
p
arated b
y
a
j
o
i
nt o
f
some
ki
n
d
,an
d
(2) v
i
scera
l
musc
l
es, w
hi
c

hf
orm
l
a
y
ers o
f
t
i
ssue enve
l
o
pi
n
gi
nterna
l
o
r
g
ans suc
h
as t
h
e
h
eart,
g
ut, an
d

re
p
ro
d
uct
i
ve tract
.
A
ttachment of a muscle to the integument must take into account the fact that period-
ically the remains of the old cuticle are shed; therefore, an insertion must be able to brea
k
a
nd re-form easil
y
.AsFi
g
ure 14.1 indicates, a muscle terminates at the basal lamina l
y
in
g
b
eneat
h
t
h
ee
pid
erm
i

s. T
h
e musc
l
ece
ll
san
d
e
pid
erma
l
ce
ll
s
i
nter
digi
tate,
i
ncreas
i
n
g
t
h
e
s
ur
f

ace area
f
or attac
h
ment
by
a
b
out 10 t
i
mes, an
dd
esmosomes occur at
i
nterva
l
s, re
pl
ac-
i
ng t
h
e
b
asa
ll
am
i
na. Attac
h

ment o
f
a musc
l
ece
ll
to t
h
er
i
g
id
cut
i
c
l
e
i
sac
hi
eve
d
t
h
roug
h
l
arge numbers of parallel microtubules (called “tonofibrillae” by earlier authors). Distally,
the epidermal cell membrane is invaginated, forming numbers of conical hemidesmosomes
o

nw
hi
c
h
t
h
em
i
crotu
b
u
l
es term
i
nate. Runn
i
n
gdi
sta
df
rom eac
hh
em
id
esmosome
i
s one
,
rare
ly

two, musc
l
e attac
h
ment fi
b
ers (
=
tonofi
b
r
il
s). Eac
h
fi
b
er
p
asses a
l
on
g
a
p
ore cana
l
FI
G
URE 14.1. Musc
l

e
i
nsert
i
on. [A
f
ter A. C. Nev
ill
e,
1
975,
B
iology of the Arthropod Cuticle
.
By p
ermissio
n
o
f
Spr
i
nger-Ver
l
ag, New Yor
k
.
]
4
3
9

M
U
S
CLE
S
AND
LO
C
OMOTIO
N
t
o the cuticulin envelope of the epicuticle to which they are attached by a special cement.
As the cuticulin la
y
er is the first one formed durin
gp
roduction of a new cuticle (Cha
p
te
r
11, Sect
i
on 3.1), attac
h
ment o
f
new
ly f
orme
d

fi
b
ers can rea
dily
occur. Unt
il
t
h
e actua
l
mo
l
t,
h
owever
,
t
h
ese are cont
i
nuous w
i
t
h
t
h
eo
ld
fi
b

ers an
d,
t
h
ere
f
ore
,
norma
l
musc
l
e contract
i
on
i
s possible (Neville, 197
5
).
M
uscles comprise a varied number of elongate, multinucleated cells (fibers) (not t
o
b
e confused with the muscle attachment fibers mentioned above) that ma
y
extend alon
g
th
e
l

en
g
t
h
o
f
a musc
l
e. A musc
l
e
i
s arran
g
e
d
usua
lly i
nun
i
ts o
f
10–20 fi
b
ers, eac
h
un
i
t
b

e
i
n
g
se
p
arate
df
rom t
h
eot
h
ers
by
a trac
h
eo
l
ate
d
mem
b
rane. Eac
h
un
i
t
h
asase
p

arate nerve
supp
l
y. T
h
e cytop
l
asm (sarcop
l
asm) o
f
eac
h
fi
b
er conta
i
nsavar
i
e
d
num
b
er o
f
m
i
toc
h
on

d
r
i
a
(
sarcosomes). Even at the light microscope level, the transversely striated nature of muscles
i
s visible. Higher magnification reveals that each fiber contains a large number of myofibril
s
(
=
fi
b
r
illae
=
sarcost
yl
es)
lyi
n
gp
ara
ll
e
li
nt
h
e sarco
pl

asm an
d
exten
di
n
g
t
h
e
l
en
g
t
h
o
f
t
h
e
ce
ll
. Eac
h
m
y
ofi
b
r
il
com

p
r
i
ses t
h
e contract
il
efi
l
aments, ma
d
eu
pp
r
i
mar
ily
o
f
two
p
rote
i
ns,
act
i
nan
d
myos
i

n. T
h
et
hi
c
k
er myos
i
nfi
l
aments are surroun
d
e
db
yt
h
et
hi
nner
b
ut mor
e
n
umerous actin filaments. Filaments of each myofibril within a cell tend to be aligned, and
i
t is this that creates the striated appearance (alternating light and dark bands) of the cell. Th
e
d
ark bands (A bands) corres
p

ond to re
g
ions where the actin and m
y
osin overla
p
, whereas
th
e
ligh
ter
b
an
d
s
i
n
di
cate re
gi
ons w
h
ere t
h
ere
i
son
ly
act
i

n(I
b
an
d
s) or m
y
os
i
n(H
b
an
d
s)
(
F
i
gure 14.2). E
l
ectron m
i
croscopy
h
as revea
l
e
di
na
ddi
t
i

on to t
h
ese
b
an
d
s a num
b
er o
f
t
hin
t
ransverse structures in the muscle fiber. Each of these Z lines
(
discs
)
runs across the fibe
r
i
n the center of the I bands, separating individual contractile segments called sarcomeres.
Attached to each side of the Z line are the actin filaments, which in contracted muscle ar
e
F
IGURE 14
.
2
.
D
etails of a muscle fiber. [After R. F. Chapman, 1971,

T
he Insects:
S
tructure and Function.
By
p
erm
i
ss
i
on o
f
E
l
sev
i
er
/
Nort
h
-Ho
ll
an
d
, Inc., an
d
t
h
e aut
h

or.
]
44
0
C
HAPTER
14
c
onnected to the myosin filaments by a means of cross bridges present at each end of the
m
y
osin. Periodicall
y
, the
p
lasma membrane (sarcolemma) of the muscle fiber is dee
p
l
y
i
nva
gi
nate
d
an
df
orms t
h
e so-ca
ll

e
d
Ts
y
stem (transverse s
y
stem). In most
i
nsect musc
l
e
s
t
h
eTs
y
stem occurs m
id
wa
yb
etween t
h
eZ
li
ne an
d
H
b
an
d

;
i
nfi
b
r
ill
ar musc
l
es,
h
owever
,
t
h
ere
i
snoregu
l
ar pattern
f
or t
h
e pos
i
t
i
on o
f
t
h

e
i
nvag
i
nat
i
ons
.
T
hough the above description is applicable to all insect muscles, different types o
f
muscles can be distin
g
uished,
p
rimaril
y
on the basis of the arran
g
ement of m
y
ofibrils
,
m
i
toc
h
on
d
r

i
a, an
d
nuc
l
e
i
;t
h
e
d
e
g
ree o
f
se
p
arat
i
on o
f
t
h
em
y
ofi
b
r
il
s; t

h
e
d
e
g
ree o
fd
eve
l-
op
ment o
f
t
h
e sarco
pl
asm
i
c ret
i
cu
l
um; an
d
t
h
e num
b
er o
f

act
i
ns surroun
di
n
g
eac
h
m
y
os
i
n
(F
i
gure 14.3). T
h
ese
i
nc
l
u
d
etu
b
u
l
ar (
l
ame

ll
ar), c
l
ose-pac
k
e
d
,an
d
fi
b
r
ill
ar musc
l
es, a
ll
o
f
w
hich are skeletal, and visceral muscles.
L
eg and segmental muscles of many adult insects and the flight muscles of primitive
fli
ers, suc
h
as O
d
onata an
d

D
i
ct
y
o
p
tera, are o
f
t
h
etu
b
u
l
ar t
yp
e,
i
nw
hi
c
h
t
h
e
fl
attene
d
(
l

ame
ll
ate) m
y
ofi
b
r
il
s are arran
g
e
d
ra
di
a
lly
aroun
d
t
h
e centra
l
sarco
pl
asm. T
h
e nuc
l
e
i

are
di
str
ib
ute
d
w
i
t
hi
nt
h
e core o
f
sarcop
l
asm an
d
t
h
es
l
a
blik
em
i
toc
h
on
d

r
i
a are
i
ntersperse
d
F
IGURE 14.3.
T
ransverse sections of insect skeletal muscles. (A) Tubular leg muscle of
V
es
pa
(Hymenoptera)
;
(B) tu
b
u
l
ar
fli
g
h
t musc
l
eo
f
E
na
ll

a
g
ma
(
O
d
onata); (C) c
l
ose-pac
k
e
dfli
g
h
t musc
l
eo
f
a
b
utter
fl
y; an
d
(D) fi
b
r
ill
a
r

fligh
t musc
l
eo
f
T
ene
b
ri
o
(Co
l
eo
p
tera). (Not to same sca
l
e.) [A, a
f
ter H. E. Jor
d
an, 1920, Stu
di
es on str
ip
e
d
musc
l
e
structure.

VI,
A
m.
J
.
A
nat
.
2
7
:
1–66. By permission of Wistar Press. B, C, redrawn from electron micrograph
s
i
n D. S. Smith, 1965, The flight muscles of insects, Scienti
fi
c America
n
, June 1965, W. H. Freeman and Co. B
y
p
erm
i
ss
i
on o
f
t
h
e aut

h
or.D,re
d
rawn
f
rom an e
l
ectron m
i
cro
g
ra
ph i
nD.S.Sm
i
t
h
,19
6
1, T
h
e structure o
fi
nsec
t
fi
brillar muscles. A study made with special reference to the membrane systems of the fiber,
J
. Biophys. Biochem
.

Cy
to
l
. 1
0
:
123–158. By permission of the Rockefeller Institute Press and the author.]
4
4
1
M
U
S
CLE
S
AND
LOCOMOTIO
N
b
etween the myofibrils.The body musculature of apterygotes and some larval pterygotes,th
e
le
g
muscles of some adult
p
ter
yg
otes, and the fli
g
ht muscles of Ortho

p
tera and Le
p
ido
p
tera
are o
f
t
h
ec
l
ose-
p
ac
k
e
d
t
yp
e. Here t
h
em
y
ofi
b
r
il
san
d

m
i
toc
h
on
d
r
i
a are concentrate
di
nt
h
e
center o
f
t
h
efi
b
er an
d
t
h
e nuc
l
e
i
are arran
g
e

dp
er
iph
era
lly
.Inc
l
ose-
p
ac
k
e
d fligh
t musc
l
es,
th
efi
b
ers are cons
id
era
bl
y
l
arger t
h
an t
h
ose o

f
tu
b
u
l
ar
fli
g
h
t musc
l
es. In a
ddi
t
i
on, trac
h
eo
l
e
s
d
eeply indent the fiber, whereas in tubular muscles tracheoles simply lie alongside each
fiber. It should be a
pp
reciated that the tracheoles do not actuall
yp
enetrate the muscl
e
ce

ll
mem
b
rane, t
h
at
i
s, t
h
e
y
are extrace
ll
u
l
ar. In most
i
nsects t
h
e
i
n
di
rect musc
l
es, w
hi
c
h
p

rov
id
et
h
e
p
ower
f
or
fligh
t, are near
ly
a
l
wa
y
sfi
b
r
ill
ar, so-ca
ll
e
db
ecause
i
n
di
v
id

ua
l
fi
b
r
il
s
are c
h
aracter
i
st
i
ca
ll
y very
l
arge an
d
, toget
h
er w
i
t
h
t
h
e mass
i
ve m

i
toc
h
on
d
r
i
a, occupy a
l
most
all of the volume of the fiber. Very little sarcoplasm is present, and the nuclei are squeezed
r
andomly between the fibrils. Because of their size, there are often only a few fibrils pe
r
ce
ll
,an
d
t
h
ese are
f
re
q
uent
ly q
u
i
te
i

so
l
ate
df
rom eac
h
ot
h
er
by
t
h
e mass
i
ve
ly i
n
d
ente
d
an
d
i
ntertw
i
n
i
n
g
s

y
stem o
f
trac
h
eo
l
es. T
h
e
p
resence o
fl
ar
g
e
q
uant
i
t
i
es o
f
c
y
toc
h
romes
i
nt

he
mi
toc
h
on
d
r
i
ag
i
ves t
h
ese musc
l
esac
h
aracter
i
st
i
cp
i
n
k
or ye
ll
ow co
l
or. It s
h

ou
ld b
e apparen
t
ev
e
n from this brief description that fibrillar muscles are designed to facilitate a high rat
e
of aerobic respiration in connection with the energetics of flight
.
Visceral muscles differ from skeletal muscles in several wa
y
s. The cells com
p
risin
g
th
em are un
i
nuc
l
eate, ma
yb
ranc
h
,an
d
are
j
o

i
ne
d
to a
dj
acent ce
ll
s
by
se
p
tate
d
esmosomes
.
T
h
e
i
r contract
il
ee
l
ements are not arrange
di
nfi
b
r
il
san

d
conta
i
na
l
arger proport
i
on o
f
act
i
n
t
o myosin. Nevertheless, the visceral muscles are striated (sometimes only weakly), and
t
heir method of contraction is apparently identical to that of skeletal muscles.
All skeletal muscles and man
y
visceral muscles are innervated. The skeletal muscles
a
l
wa
y
s rece
i
ve nerves
f
rom t
h
e centra

l
nervous s
y
stem, w
h
ereas t
h
ev
i
scera
l
musc
l
es are
i
nnervate
df
rom e
i
t
h
er t
h
e stomato
g
astr
i
cort
h
e centra

l
nervous s
y
stem. W
i
t
hi
na
p
art
i
cu
l
a
r
m
usc
l
eun
i
t, eac
h
fi
b
er may
b
e
i
nnervate
db

y one, two, or t
h
ree
f
unct
i
ona
ll
y
di
st
i
nct axons.
One of these is always excitatory; where two occur (the commonest arrangement), the
y
are usuall
y
both excitator
y
(“fast” and “slow” axons), but ma
y
be a “slow” excitator
y
axon
pl
us an
i
n
hibi
tor

y
axon;
i
n some cases a
ll
t
h
ree t
yp
es o
f
axon occur. T
hi
s arran
g
ement,
k
nown as
p
o
ly
neurona
li
nnervat
i
on,
f
ac
ili
tates a var

i
a
bl
e res
p
onse on t
h
e
p
art o
f
a musc
l
e
(
Sect
i
on 2.2). Eac
h
axon, regar
dl
ess o
fi
ts
f
unct
i
on,
i
s muc

hb
ranc
h
e
d
an
d
,
i
n contrast t
o
t
he situation in vertebrate muscle, there are several motor neuron endings from each axo
n
on each muscle fiber (multiterminal innervation) (Figure 14.4).
2
.2. Ph
y
s
i
olog
y
Like those of vertebrates, insect muscles contract according to the sliding filament
t
heory. The arrival of an excitatory nerve impulse at a neuromuscular junction causes depo-
larization of the ad
j
acent sarcolemma. A wave of de
p
olarization s

p
reads over the fiber and
i
nto t
h
e
i
nter
i
or o
f
t
h
ece
ll
v
i
at
h
eTs
y
stem. De
p
o
l
ar
i
zat
i
on o

f
t
h
eTs
y
stem mem
b
ranes
i
n
d
uces a momentar
yi
ncrease
i
nt
h
e
p
ermea
bili
t
y
o
f
t
h
ea
dj
acent sarco

pl
asm
i
c ret
i
cu
l
um,
so that calcium ions, stored in vesicles of the reticulum, are released into the sarcoplas
m
surrounding the myofibrils. The calcium ions activate cross-bridge formation between the
actin and m
y
osin, enablin
g
the filaments to slide over each other so that the distance between
a
dj
acent Z
li
nes
i
s
d
ecrease
d
.T
h
e net e
ff

ect
i
s
f
or t
h
e musc
l
e to contract. Ener
gy d
er
i
ve
d
f
rom t
h
e
hyd
ro
ly
s
i
so
f
a
d
enos
i
ne tr

iph
os
ph
ate (ATP)
i
sre
q
u
i
re
df
or contract
i
on, t
h
ou
gh
i
ts prec
i
se
f
unct
i
on
i
sun
k
nown. It may
b

e use
di
n
b
rea
ki
ng t
h
e cross-
b
r
id
ges, or
f
or t
h
e
active transport of the calcium ions back into the vesicles, or for both of these processes. In
442
C
HAPTER
14
F
I
G
URE 14
.
4
.
Pol

y
neuronal and multitermi-
na
li
nnervat
i
on o
f
an
i
nsect musc
l
e.
[
A
f
ter G
.
H
o
yl
e, 1974, Neura
l
contro
l
o
f
s
k
e

l
eta
l
mus-
c
le, in:
T
he Physiology of Insecta, 2nd ed., Vol.
I
V (M. Roc
k
ste
i
n, e
d
.). By perm
i
ss
i
on o
f
Aca-
d
em
i
c Press, Inc., an
d
t
h
e aut

h
or.
]
addition to sliding over each other, both the actin and the myosin filaments may shorten (by
c
o
ili
n
g
), an
di
n some m
y
ofi
b
r
il
st
h
eZ
li
nes
di
s
i
nte
g
rate to a
ll
ow t

h
eA
b
an
d
so
f
a
dj
acent
sarcomeres to over
l
a
p
eac
h
ot
h
er, t
h
us ena
bli
n
g
an even
g
reater
d
e
g

ree o
f
contract
i
on to
occ
u
r.
E
xtension (relaxation) of a muscle may result simply from the opposing elasticity of
the cuticle to which the muscle is attached. More commonly, muscles occur in pairs, each
member of the
p
air workin
g
anta
g
onisticall
y
to the other; that is, as one muscle is stimulate
d
to contract,
i
ts
p
artner (unst
i
mu
l
ate

d
)
i
s stretc
h
e
d
. Norma
lly
,t
h
e
p
rev
i
ous
ly
unst
i
mu
l
ate
d
musc
l
e
i
sst
i
mu

l
ate
d
to
b
eg
i
n contract
i
on w
hil
e act
i
ve contract
i
on o
f
t
h
e partner
i
sst
ill
o
ccurring (cocontraction). This is thought to bring about dampening of contraction, perhap
s
thereby preventing damage to a vigorously contracting muscle. Also, in slow movements
,
it
p

rovides an insect with a means of
p
recisel
y
controllin
g
such movements (Ho
y
le, 1974).
M
usc
l
e anta
g
on
i
sm
i
sac
hi
eve
dby
centra
li
n
hibi
t
i
on, t
h

at
i
s, at t
h
e
l
eve
l
o
fi
nterneuron
s
wi
t
hi
nt
h
e centra
l
nervous s
y
stem (C
h
a
p
ter 13, Sect
i
on 2.3). T
h
us,

f
or a
gi
ven st
i
mu
l
us
,
t
h
e passage o
fi
mpu
l
ses a
l
ong an axon to one musc
l
eo
f
t
h
epa
i
rw
ill b
e perm
i
tte

d
,an
d
hence that muscle will contract. However, passage of impulses to the partner is inhibited
and the muscle will be
p
assivel
y
stretched. It should be em
p
hasized that in this arran
g
emen
t
t
h
e axon to eac
h
musc
l
e
i
sexc
i
tator
y
.Ins
l
ow wa
lki

n
g
movements,
f
or exam
pl
e, a
l
ternat
i
n
g
st
i
mu
l
at
i
on o
f
eac
h
musc
l
e
i
s
q
u
i

te
di
st
i
nct. At
high
er s
p
ee
d
st
hi
s rec
ip
roca
li
n
hibi
t
i
on
b
rea
k
s
d
own, an
d
one o
f

t
h
e musc
l
es rema
i
ns permanent
l
y
i
nam
ildl
y contracte
d
state
,
serving as an “elastic restoring element” (Hoyle, 1974). The other muscle continues to be
alternately stimulated and thus provides the driving power for the activity.
As note
d
ear
li
er, common
ly
musc
l
es rece
i
ve two exc
i

tator
y
axons, one “s
l
ow,” t
h
eot
h
er
“
f
ast.” T
h
ese terms are somew
h
at m
i
s
l
ea
di
n
gf
or t
h
e
yd
o not
i
n

di
cate t
h
es
p
ee
d
at w
hi
c
h
i
mpu
l
ses trave
l
a
l
ong t
h
e axons,
b
ut rat
h
er t
h
e spee
d
at w
hi

c
h
as
i
gn
i
ficant contract
i
on can
be observed in the muscle. Thus, an impulse traveling along a fast axon induces a strong
4
4
3
M
U
S
CLE
S
AND
LOCOMOTIO
N
contraction of the “all or nothing” type; that is, a further contraction cannot be initiated unti
l
t
he ori
g
inal ionic conditions have been restored. In contrast, a sin
g
le im
p

ulse from a slow
axon causes on
ly
a wea
k
contract
i
on
i
nt
h
e musc
l
e. However, a
ddi
t
i
ona
li
m
p
u
l
ses arr
i
v
i
n
g
i

nqu
i
c
k
success
i
on are a
ddi
t
i
ve
i
nt
h
e
i
re
ff
ect (summat
i
on) so t
h
at, w
i
t
h
t
h
es
l

ow axo
n
arrangement a graded response is possible for a particular muscle, despite the relativel
y
few fibers it may contain. Muscles with dual innervation use only the slow axon for mos
t
r
e
q
uirements; the fast axon functions onl
y
when immediate and/or massive contraction i
s
n
ecessar
y
. For exam
pl
e, t
h
e extensor t
ibi
a musc
l
eo
f
t
h
e
hi

n
dl
e
g
o
f
a
g
rass
h
o
pp
er
i
sor
di
nar
ily
contro
ll
e
d
so
l
e
ly
v
i
at
h

es
l
ow axon. For
j
um
pi
n
g
,
h
owever, t
h
e
f
ast axon
i
s
b
rou
gh
t
i
nto
play
.
The function of inhibitory axons remains questionable. Electrophysiological work ha
s
shown that in normal activit
y
the inhibitor

y
axon is electricall
y
silent, that is, shows no
el
ectr
i
ca
l
act
i
v
i
t
y
,an
di
sc
l
ear
ly b
e
i
n
gi
n
hibi
te
df
rom w

i
t
hi
nt
h
e centra
l
nervous s
y
stem.
Dur
i
n
gp
er
i
o
d
so
fg
reat act
i
v
i
t
y
,
i
m
p

u
l
ses can somet
i
mes
b
eo
b
serve
dp
ass
i
n
g
a
l
on
g
t
h
e axon
,
per
h
aps to acce
l
erate musc
l
ere
l

axat
i
on, t
h
oug
h
norma
ll
yt
h
e use o
f
antagon
i
st
i
c musc
l
es
and central inhibition is adequate. Hoyle (1974) suggested that peripheral inhibition may
b
e necessar
y
at certain sta
g
es in the life c
y
cle, such as moltin
g
, when central inhibition ma

y
n
ot
b
e
p
oss
ibl
e.
3
.Lo
c
omotio
n
3
.1. Movement on or Through a
S
ubstrat
e
3
.
1
.
1
. Walk
i
n
g
I
nsects can walk at almost imperceptibly slow speed (watch a mantis stalking its prey)

o
r run at seemingly very high rates (try to catch a cockroach). The latter is, however,
a
w
ron
g
im
p
ression created b
y
the smallness of the or
g
anism, the rate at which its le
g
s move
,
an
d
t
h
e rate at w
hi
c
hi
t can c
h
an
g
e
di

rect
i
on. Ants scurr
yi
n
g
a
b
out on a
h
ot summer
d
a
y
are traveling only about 1.
5
km/hr, and the elusive cockroach has a top speed of just unde
r
5
km/hr (Hughes and Mill, 1974).
Nevertheless, an insect leg is structurally well adapted for locomotion. Like the limbs of
o
ther activel
y
movin
g
animals, it ta
p
ers toward the distal end, which is li
g

ht and easil
y
lifted.
I
ts tarsa
l
se
g
ments are e
q
u
ipp
e
d
w
i
t
h
c
l
aws or
p
u
l
v
illi
t
h
at
p

rov
id
et
h
e necessar
yf
r
i
ct
i
on
b
etween t
h
e
li
m
b
an
d
t
h
esu
b
strate. A
l
e
g
com
p

r
i
ses
f
our ma
i
nse
g
ments (C
h
a
p
ter 3, Sect
i
on
4
.3.1), which articulate with each other and with the body. The coxa articulates proximall
y
w
ith the thorax, usually by means of a dicondylic joint and distally, with the fused trochante
r
and femur, also via a dicond
y
lic
j
oint. Dicond
y
lic
j
oints

p
ermit movement in a sin
g
le
p
lane.
However, t
h
etwo
j
o
i
nts are set at r
igh
tan
gl
es to eac
h
ot
h
er an
d
,t
h
ere
f
ore, t
h
et
ip

o
f
a
l
e
g
can move
i
nt
h
ree
di
mens
i
ons
.
T
h
e musc
l
es t
h
at move a
l
eg are
b
ot
h
extr
i

ns
i
c(
h
av
i
ng one en
di
nserte
d
on t
h
ewa
ll
o
f the thorax) and intrinsic (having both ends inserted within the leg) (Figure 14.
5
). Th
e
m
a
j
orit
y
of extrinsic muscles move the coxa, rarel
y
the fused trochantofemoral se
g
ment,
wh

ereas t
h
e
p
a
i
re
di
ntr
i
ns
i
c musc
l
es move
l
e
g
se
g
ments
i
nre
l
at
i
on to eac
h
ot
h

er. Som
e
of
t
h
e extr
i
ns
i
c musc
l
es
h
ave a
d
ua
lf
unct
i
on, serv
i
n
g
to
b
r
i
n
g
a

b
out
b
ot
hl
e
g
an
d
w
i
n
g
m
ovements. Typ
i
ca
ll
y, t
h
e
l
eg musc
l
es
i
nc
l
u
d

e (1) t
h
e coxa
l
promotor an
di
ts antagon
i
st, t
h
e
coxal remotor, which run from the tergum to the anterior and posterior edges, respectively,
444
C
HAPTER
14
F
IGURE 14
.
5
.
(A) Musculature of coxa; (B) segmental musculature of leg; and (C) musculature of hindleg of
g
rass
h
opper. [A, C,
f
rom R. E. Sno
d
grass, Princip

l
es o
f
Insect Morp
h
o
l
og
y
. Copyright 193
5
by McGraw-Hill,
I
nc. Used with
p
ermission of McGraw-Hill Book Com
p
an
y
.B,re
p
roduced b
yp
ermission of the Smithsonia
n
I
n
st
i
tut

i
o
nPr
ess
fr
o
m
S
mithsonian Miscellaneous Collection
s
,
V
olume 80, Morphology and mechanism of the
VV
i
nsect thorax, Number 1, June 2
5
, 1927, 108
p
a
g
es, b
y
R. E. Snod
g
rass: Fi
g
ure 39,
p
a

g
e 89. Washin
g
ton, D.C.
,
1
928, Smithsonian Institution.]
of
t
h
e coxa; contract
i
on o
f
t
h
e coxa
l
promotor causes t
h
e coxa to tw
i
st
f
orwar
d
,t
h
ere
b

y
effecting protraction (a forward swing) of the entire leg; (2) the coxal adductor and abductor
(attached to the sternum and pleuron, respectively), which move the coxa toward or away
f
rom the bod
y
; (3) anterior and
p
osterior coxal rotators, which arise on the sternum an
d
ass
i
st
i
nra
i
s
i
n
g
an
d
mov
i
n
g
t
h
e
l

e
gf
orwar
d
or
b
ac
k
war
d
;an
d
(4) an extensor (
l
evator
)
an
dfl
exor (
d
e
p
ressor) musc
l
e
i
n eac
hl
e
g

se
g
ment, w
hi
c
h
serve to
i
ncrease an
dd
ecrease
,
respectively, the angle between adjacent segments. It should be noted that the muscles that
move a particular leg segment are actually located in the next more proximal segment. Fo
r
exam
p
le, the tibial extensor and flexor muscles, which alter the an
g
le between the femur
an
d
t
ibi
a, are
l
ocate
d
w
i

t
hi
nt
h
e
f
emur an
d
are attac
h
e
dby
s
h
ort ten
d
ons
i
nserte
d
at t
h
e
h
ea
d
of
t
h
et

ibi
a
.
It
i
st
h
e coor
di
nate
d
act
i
ons o
f
t
h
e extr
i
ns
i
can
di
ntr
i
ns
i
c musc
l
es t

h
at move a
l
eg
and propel an insect forward. In considering how propulsion is achieved, it must also b
e
remembered that another im
p
ortant function of a le
g
is to su
pp
ort the bod
y
, that is, to kee
p
44
5
M
U
S
CLE
S
AND
LOCOMOTIO
N
F
I
G
URE 14.6.

M
a
g
n
i
tu
d
eo
f
t
h
e
l
on
gi
tu
di
na
l
an
dl
atera
lf
orces resu
l
t
i
n
gf
rom t

h
e strut e
ff
ect
f
or eac
hl
e
gi
n
i
ts
extreme
p
osition. [After G. M. Hu
g
hes, 19
5
2, The coordination of insect movements. I. The walkin
g
movements
of insects
,
J.
Ex
p
. Biol. 2
9
:
267–284. By permission of Cambridge University Press, London.

]
i
to
ff
t
h
e groun
d
.Int
h
e
l
atter s
i
tuat
i
on, a
l
eg may
b
e cons
id
ere
d
asas
i
ng
l
e-segmente
d

structure—a rigid strut. If the strut is vertical, the force along its length (axial force) will be
solely supporting and will have no propulsive component. If the strut is inclined, the axia
l
force can be resolved into two com
p
onents, a vertical su
pp
ortive force and a horizonta
l
p
ro
p
u
l
s
i
ve
f
orce. Because t
h
e
l
e
gp
rotru
d
es
l
atera
lly f

rom t
h
e
b
o
dy
,t
h
e
h
or
i
zonta
lf
orce can
b
e
f
urt
h
er reso
l
ve
di
nto a transverse
f
orce pus
hi
ng t
h

e
i
nsect s
id
eways an
d
a
l
ong
i
tu
di
na
l
force that causes backward or forward motion. The relative sizes of these horizontal force
s
d
epend on (1) which leg is being considered and (2) the position of that leg. Figure 14.6
i
ndicates the size of these forces for each le
g
at its two extreme
p
ositions. It will be a
pp
arent
th
at
i
na

l
most a
ll
o
fi
ts
p
os
i
t
i
ons t
h
e
f
ore
l
e
g
w
ill i
n
hibi
t
f
orwar
d
movement, w
h
ereas t

h
e
mid
-an
dhi
n
dl
egs a
l
ways promote
f
orwar
d
movement. In equ
ilib
r
i
um, t
h
at
i
s, w
h
en an
i
nsect is standing still, the forces will be equal and opposite. Movement of an insect’s body
w
ill occur only if the center of gravity of the body falls. This occurs when the forces become
i
mbalanced, for exam

p
le, b
y
chan
g
in
g
the
p
osition of a forele
g
so that its retardin
g
effec
t
i
sno
l
on
g
er e
q
ua
l
to t
h
e
p
romot
i

n
g
e
ff
ect o
f
t
h
eot
h
er
l
e
g
s, w
h
ereu
p
on t
h
e
i
nsect to
ppl
e
s
f
orwar
d
(Hu

gh
es an
d
M
ill
, 1974)
.
A
l
so
i
mportant
f
rom t
h
epo
i
nt o
f
v
i
ew o
fl
ocomot
i
on
i
st
h
e

l
eg’s a
bili
ty to
f
unct
i
on a
s
al
e
ver, that is, a solid bar that rotates about a fulcrum and on which work can be done.
The fulcrum is the coxothoracic
j
oint and the work is done b
y
the lar
g
e, extrinsic muscles
.
44
6
C
HAPTER
14
B
ecause of the large angle through which it can rotate and because of its angle to the body,
the forele
g
is most im

p
ortant as a lever. In contrast, the mid- and hindle
g
s, which each
rotate t
h
rou
gh
on
ly
a sma
ll
an
gl
e, exert on
ly
as
ligh
t
l
ever e
ff
ect an
d
serve
p
r
i
mar
ily

a
s
struts (
i
nt
h
e
f
u
lly
exten
d
e
d
,r
igid p
os
i
t
i
on). For t
h
e
f
ore
l
e
gi
n
i

ts
f
u
lly p
rotracte
dp
os
i
t
i
on
,
c
ontract
i
on o
f
t
h
e retractor musc
l
e(
i
.e., t
h
e
l
ever e
ff
ect) w

ill b
esu
f
fic
i
ent to overcome t
h
e
o
pposing retarding (strut) effect and, provided that the frictional forces between the ground
and tarsi are sufficient, the bod
y
will be moved forward.
H
owever, t
h
e
l
ar
g
est com
p
onent o
f
t
h
e
p
ro
p

u
l
s
i
ve
f
orce
i
s
d
er
i
ve
d
as a resu
l
to
f
t
he
l
e
g
’s a
bili
t
y
to
fl
ex an

d
exten
dby
v
i
rtue o
f
t
h
e
i
r
j
o
i
nte
d
nature. F
l
exure (a
d
ecrease
i
nt
h
e
ang
l
e
b

etween a
dj
acent
l
eg segments) w
ill
ra
i
se t
h
e
l
eg o
ff
t
h
e groun
d
so t
h
at
i
t can
be
moved forward without the need to overcome frictional forces between it and the ground
.
In the case of the foreleg, flexure first will remove, by lifting the leg from the ground, the
retar
di
n

g
e
ff
ect as a resu
l
to
fi
ts act
i
on as a strut an
d
, secon
d
,w
h
en t
h
e
l
e
gi
sre
pl
ace
d
o
n
t
h
esu

b
strate, w
ill
cause t
h
e
b
o
dy
to
b
e
p
u
ll
e
df
orwar
d
.F
l
exure o
f
t
h
e
f
ore
l
e

g
cont
i
nues
unt
il
t
h
e
l
eg
i
s perpen
di
cu
l
ar to t
h
e
b
o
d
y, at w
hi
c
h
po
i
nt extens
i

on
b
eg
i
ns so t
h
at now t
he
body is pushed forward. For the mid- and hindlegs, flexure serves to bring the legs into
a
new forward position. Extension, as in the case of the foreleg, will push the body forward.
B
ecause the hindle
g
is usuall
y
the lar
g
est of the three, it exerts the
g
reatest
p
ro
p
ulsive force.
As note
d
a
b
ove, t

h
e
h
or
i
zonta
l
ax
i
a
lf
orce a
l
on
g
eac
hl
e
gh
as a transverse as we
ll
a
s
a
l
ong
i
tu
di
na

l
component. T
h
us, as an
i
nsect moves,
i
ts
b
o
d
yz
i
gzags s
li
g
h
t
l
y
f
rom s
id
eto
side, the transverse forces exerted by the fore- and hindlegs of one side being balanced by
an opposite force exerted by the middle leg of the opposite side in the normal rhythm of le
g
movemen
t
s

.
R
hythms o
f
Leg Movements. Most
i
nsects use a
ll
s
i
x
l
egs
d
ur
i
ng norma
l
wa
lki
ng.
O
ther species habitually employ only the two anterior or the two posterior pairs of legs bu
t
may use all legs at higher speeds. In all instances, however, the legs are lifted in an orderly
se
q
uence (thou
g
h this ma

y
var
y
with the s
p
eed of the insect), and there are alwa
y
s at least
t
h
ree
p
o
i
nts o
f
contact w
i
t
h
t
h
esu
b
strate
f
orm
i
n
g

a “tr
i
an
gl
eo
f
su
pp
ort”
f
or t
h
e
b
o
dy
. (In
some s
p
ec
i
es t
h
at em
pl
o
y
two
p
a

i
rs o
fl
e
g
s, t
h
et
ip
o
f
t
h
ea
bd
omen ma
y
serve as a
p
o
i
nt o
f
support.) Two other generalizations that may be made are (1) no leg is lifted until the le
g
behind has taken up a supporting position and (2) the legs of a segment alternate in their
movemen
t
s
.

In t
h
et
ypi
ca
lh
exa
p
o
d
a
lg
a
i
tat
l
ow s
p
ee
d
,on
ly
one
l
e
g
atat
i
me
i

sra
i
se
d
o
ff
t
h
e
g
roun
d,
so t
h
at t
h
e ste
ppi
n
g
se
q
uence
i
s R3, R2, R
l
, L3, L2, L
l
(w
h

ereRan
d
L are r
igh
tan
dl
e
ft
l
egs, respect
i
ve
l
y, an
d
1, 2, an
d
3
i
n
di
cate t
h
e
f
ore-, m
id
-, an
dhi
n

dl
egs, respect
i
ve
l
y). W
i
t
h
increase in speed, overlap occurs between both sides so that the sequence first becomes R3
Ll, R2, Rl L3, L2, etc., and, then, R3 Rl L2, R2 L3 Ll, etc., that is, a true alternatin
g
tri
p
odal
g
a
i
t.
Th
e ort
h
o
p
teran
R
hipipter
yx
h
as a

q
ua
d
ru
p
e
d
a
lg
a
i
t, us
i
n
g
on
ly
t
h
e anter
i
or two
p
a
i
r
s
of l
egs an
d

us
i
ng t
h
et
i
po
f
t
h
ea
bd
omen as a support. Its stepp
i
ng sequence
i
sR
l
L2, R2 LI.,
etc. Mantids are likewise quadrupedal at low speed, using the posterior two pairs of legs
(sequence R3 L2, R2 L3, etc.). At high speed, the forelegs are brought into action though
the insects remain effectivel
yq
uadru
p
edal (se
q
uence Ll R3, L3 R2, L2 R1, etc.).
Av
a

r
i
et
y
o
f
met
h
o
d
s
f
or turn
i
n
gh
ave
b
een o
b
serve
d
,o
f
ten
i
nt
h
e same s
p

ec
i
es. T
h
e
y
i
nc
l
u
d
e
i
ncreas
i
ng t
h
e
l
engt
h
o
f
t
h
e str
id
eont
h
e outs

id
eo
f
t
h
e turn,
i
ncreas
i
ng t
h
e
f
requency
o
f stepping on the outside of the turn, fixing one or more of the “inside” legs as pivots, and
moving the legs on the inside of the turn backward.
Coordination of the movements both amon
g
se
g
ments of the same le
g
and amon
g
diff
erent
l
e
g

sre
q
u
i
res a
high l
eve
l
o
f
neura
l
act
i
v
i
t
y
,
b
ot
h
sensor
y
an
d
motor. L
ik
eot
h

er
44
7
M
U
S
CLE
S
AND
LOCOMOTIO
N
r
hythmic activities, the walking rhythm is centrally generated; that is, the endogenou
s
activit
y
of a network of neurons within each thoracic
g
an
g
lion re
g
ulates the alternatin
g
contract
i
on o
f
t
h

e
l
e
gfl
exor an
d
extensor musc
l
es,
h
ence t
h
e
fl
ex
i
on an
d
extens
i
on o
f
t
h
e
li
m
b
. Interse
g

menta
l
coor
di
nat
i
on o
fl
e
g
movements
i
sac
hi
eve
dp
r
i
nc
ip
a
lly by
“centra
l
coup
li
ng,” t
h
at
i

s,
b
ys
i
gna
l
s trave
li
ng w
i
t
hi
nt
h
e centra
l
nervous system
f
rom one networ
k
t
o another. Starting and stopping, turning, and change of speed are controlled by the brain
and subeso
p
ha
g
eal
g
an
g

lion, via so-called “command neurons,” thou
g
h how these center
s
e
x
e
rt t
h
e
i
r contro
li
s unc
l
ear. Su
p
er
i
m
p
ose
d
on t
hi
s centra
l
contro
li
st

h
e
i
n
p
ut
f
rom t
he
i
nsect’s sense or
g
ans, es
p
ec
i
a
lly p
ro
p
r
i
oce
p
tors on t
h
e
l
e
g

st
h
emse
l
ves, w
hi
c
hp
erm
i
ts t
he
i
nsect to a
dj
ust
i
ts wa
lki
ng r
h
yt
h
m to compensate
f
or c
h
ang
i
ng env

i
ronmenta
l
con
di
t
i
ons
.
(
See Chapter 13, Section 2.3).
3
.1.2. Jumpin
g
J
ump
i
ng
i
s espec
i
a
ll
ywe
ll d
eve
l
ope
di
n grass

h
oppers,
fl
eas,
fl
ea
b
eet
l
es, c
li
c
kb
eet
l
es
,
and Collembola. In the first three mentioned groups, jumping involves the hindlegs, which,
like those of other
j
um
p
in
g
animals, are elon
g
ate and ca
p
able of
g

reat extension. Thei
r
l
en
g
t
h
ensures t
h
at t
h
e
li
m
b
s are
i
n contact w
i
t
h
t
h
esu
b
strate
f
or a
l
on

g
t
i
me
d
ur
i
n
g
ta
k
eo
ff.
E
xtens
i
on
i
sac
hi
eve
d
as t
h
e
i
n
i
t
i

a
lly
acute an
gl
e
b
etween t
h
e
f
emur an
d
t
ibi
a
i
s
i
ncrease
d
t
o more t
h
an
9
0
◦
b
yt
h

et
i
me t
h
e tars
il
eave t
h
esu
b
strate. T
h
e
l
engt
h
an
d
extens
i
on toget
h
er
e
nable sufficient thrust to be developed that the insect can jump heights and distances many
t
imes its body length. For example, a fifth-instar locust (length about 4 cm) may “hig
h
j
um

p
”30cman
d
, concurrent
ly
,“
l
on
gj
um
p
”70cm
.
I
n Ort
h
o
p
tera t
h
e
p
ower
f
or
j
um
pi
n
gi

s
d
eve
l
o
p
e
dby
t
h
e
l
ar
g
e extensor t
ibi
ae musc
l
e
i
n the femur (Figure 14.
5
C). The muscle is arranged in two masses of tissue that arise on the
femur wall and are inserted obliquely on a long flat apodeme attached to the upper end of
t
he tibia. The resultant herringbone arrangement increases the effective cross-sectional area
o
f muscle attached to the a
p
odeme, thereb

y
increasin
g
the
p
ower that the muscle develo
p
s.
As t
h
e extensor t
ibi
ae contracts, a
ll
act
i
v
i
t
y
ceases
i
nt
h
e motoneurons runn
i
n
g
to
i

ts
anta
g
on
i
st, t
h
e
fl
exor t
ibi
ae musc
l
e, t
h
us
p
erm
i
tt
i
n
g
a
ll
o
f
t
h
e

p
ower
d
eve
l
o
p
e
d
to
b
e use
di
n
e
xtending the tibia. This inhibition results from the activity of a single, branched inhibitory
i
nterneuron. Because the apodeme is attached to the upper end of the tibia, slight contractio
n
o
f the extensor muscle will cause a relativel
y
enormous movement at the tarsus (ratio o
f
m
ovements
6
0:1 w
h
en t

h
et
ibi
o
f
emora
lj
o
i
nt
i
st
igh
t
ly fl
exe
d
).
I
t
h
as
b
een ca
l
cu
l
ate
d
t

h
at
f
or t
h
e
l
ocust to ac
hi
eve t
h
e max
i
mum t
h
rust
f
or ta
k
eo
ff,
t
he body must be accelerated at about 1.
5
×
10
4
c
m
/

sec
2
o
v
e
ra
time span of 20 msec. Th
e
force exerted by each extensor muscle is about
5
×
10
5
dynes
(
=
5
00 g wt) for an insec
t
w
ei
g
hi
n
g3g
(Alexander, 1968, cited from Hu
g
hes and Mill, 1974). To withstand this force,
th
ea

p
o
d
eme must
h
ave a stren
g
t
h
c
l
ose to t
h
at o
f
mo
d
erate stee
l
.T
h
e extreme
ly
s
h
ort t
i
m
e
p

er
i
o
d
over w
hi
c
h
t
hi
s acce
l
erat
i
on
i
s
d
eve
l
o
p
e
d
ma
k
es
i
tun
lik

e
ly
t
h
at
j
um
pi
n
g
occurs as a
d
irect result of muscle contraction. Indeed, Heitler (1974) showed that the initial energy of
m
uscle contraction is stored as elastic energy using a cuticular locking device that holds th
e
flexor tendon in o
pp
osition to the force develo
p
ed within the extensor muscle. At a critica
l
l
eve
l
,t
h
e ten
d
on

i
sre
l
ease
d
,a
ll
ow
i
n
g
t
h
et
ibi
a to rotate ra
pidly b
ac
k
war
d.
L
ik
ew
i
se,
i
n
fl
eas, t

h
e ener
gy
o
f
musc
l
e contract
i
on
i
s first store
d
as e
l
ast
i
c ener
gy
.
Pr
i
or to
j
ump
i
ng, t
h
e
fl

ea contracts var
i
ous extr
i
ns
i
c musc
l
es o
f
t
h
e metat
h
orax, w
hi
c
h
are
i
nserted via a tendon on the fused trochantofemoral segment. This serves to draw the le
g
c
loser to the bod
y
, com
p
ressin
g
a

p
ad of resilin and causin
g
the
p
leural and coxal walls
t
o
b
en
d
. At a certa
i
n
p
o
i
nt o
f
contract
i
on, t
h
et
h
orac
i
c catc
h
es (

p
e
g
so
f
cut
i
c
l
e) s
lip i
nt
o
44
8
C
HAPTER
14
notches on the sternum, thereby “cocking the system.” The jump is initiated when other
l
aterall
y
inserted muscles contract to
p
ull the catches out of the notches, thus allowin
g
the
store
d
ener

gy
to
b
era
pidly
re
l
ease
d
(Rot
h
sc
hild
e
t al.
,19
7
2)
.
Once a
i
r
b
orne, an
i
nsect ma
y
or ma
y
not sta

bili
ze
i
tse
lf i
n
p
re
p
arat
i
on
f
or
l
an
di
n
g
or
fli
g
h
t. For examp
l
e, t
h
e
fl
ea

b
eet
l
e
Ch
a
l
coi
d
es aurata somet
i
mes
j
umps “out o
f
contro
l
,”
i
t
s
body rotating continuously till it hits the ground. However, it can, when necessary, control
its
j
um
p
b
y
extendin
g

the win
g
s so that a “feet-first” landin
g
occurs (Brackenbur
y
and
Wan
g
, 1995). Lar
g
er s
p
ecies such as Ortho
p
tera use their hindle
g
s as rudders durin
g
the
j
um
p
,
f
ac
ili
tat
i
n

g
an u
p
r
igh
t
l
an
di
n
g
or ta
k
eo
ff f
or
fligh
t (Burrows an
d
Morr
i
s, 2003)
.
3.1.3.
C
rawling and Burrowing
Man
y
en
d

o
p
ter
yg
ote
l
arvae em
pl
o
y
t
h
et
h
orac
i
c
l
e
g
s
f
or
l
ocomot
i
on
i
nt
h

e manner t
yp-
i
ca
l
o
f
a
d
u
l
t
i
nsects; t
h
at
i
s, t
h
e
y
ste
p
w
i
t
h
t
h
e

l
e
g
s
i
nas
p
ec
i
fie
d
se
q
uence, t
h
e
l
e
g
so
f
a
gi
ve
n
segment a
l
ternat
i
ng w

i
t
h
eac
h
ot
h
er. Usua
ll
y,
h
owever, c
h
anges
i
n
b
o
d
ys
h
ape, ac
hi
eve
d
by synchronized contraction/relaxation of specific body muscles, are used for locomotion
in soft-bodied larvae. In this method the le
g
s, to
g

ether with various accessor
y
locomotor
y
a
pp
en
d
a
g
es,
f
or exam
pl
e, t
h
ea
bd
om
i
na
lp
ro
l
e
g
so
f
cater
pill

ars, are use
d
so
l
e
ly
as
f
r
i
ct
i
on
p
o
i
nts
b
etween t
h
e
b
o
dy
an
d
su
b
strate. A
p

o
d
ous
l
arvae
d
e
p
en
d
so
l
e
ly
on
p
er
i
sta
l
s
i
so
f
t
h
e
b
o
d

ywa
ll f
or
l
ocomot
i
on.
Where changes in body shape are used forlocomotion the body fluids act as a hydrostatic
skeleton. In other words, the insect employs the principle of incompressibility of liquids,
so that contraction of muscles in one
p
art of the bod
y
, leadin
g
to a decrease in volume, will
re
q
u
i
reare
l
axat
i
on o
f
musc
l
es an
d

a concom
i
tant
i
ncrease
i
nvo
l
ume
i
n anot
h
er re
gi
on o
f
t
h
e
b
o
d
y. Spec
i
a
l
musc
l
es
k

eep t
h
e
b
o
d
y turg
id
, ena
bli
ng t
h
e
l
ocomotor musc
l
es to e
ff
ect
these volume changes.
Crawling in lepidopteran caterpillars is probably the best studied method of locomotion
in endo
p
ter
yg
ote larvae and com
p
rises anteriorl
y
directed waves of contraction of the lon-

gi
tu
di
na
l
musc
l
es, eac
h
wave caus
i
n
g
t
h
e
b
o
dy
to
b
e
p
us
h
e
d
u
p
war

d
an
df
orwar
d
(Hu
gh
e
s
an
d
M
ill
, 1974; Brac
k
en
b
ury, 1999). T
h
ree ma
i
np
h
ases can
b
e recogn
i
ze
di
n eac

h
wave o
f
c
ontraction (Figure 14.7). First, contraction of the dorsal longitudinal muscles and trans-
v
erse muscles causes a segment to shorten dorsally and its posterior end to be raised so that
the se
g
ment behind is lifted from the substrate. The dorsoventral muscles and le
g
retractor
musc
l
es t
h
en contract,
lif
t
i
n
gb
ot
hf
eet o
f
t
h
ese
g

ment
f
rom t
h
esu
b
strate. F
i
na
lly
, contrac
-
t
i
on o
f
t
h
e ventra
ll
on
gi
tu
di
na
l
musc
l
es, com
bi

ne
d
w
i
t
h
t
h
ere
l
axat
i
on o
f
t
h
e
d
orsoventra
l
an
dl
eg retractor musc
l
es, moves t
h
e segment
f
orwar
d

an
dd
owntot
h
esu
b
strate. Compare
d
to walking, crawling and burrowing are relatively slow means of forward progression, with
s
p
eeds of about 1 cm/sec for t
yp
ical cater
p
illars. To take evasive action, for exam
p
le, from
a
p
re
d
ator, cater
pill
ars ma
y
wa
lk b
ac
k

war
dby
s
i
m
ply
revers
i
n
g
t
h
e
di
rect
i
on o
fp
er
i
sta
l
s
i
s.
U
n
d
er extreme
p

rovocat
i
on, t
h
e cater
pill
ar ma
y
co
il
u
pi
ntoaw
h
ee
l
an
d
s
i
m
ply
ro
ll b
ac
k-
w
ar
d
,ac

hi
ev
i
ng spee
d
supto40t
i
mes greater t
h
an norma
l
wa
lki
ng (Brac
k
en
b
ury, 1999).
Little work has been done on the neural coordination of crawling, though it seems probable
that endogenous activity within the central nervous system is responsible. However, pro
-
p
r
i
oce
p
t
i
ve st
i

mu
li
un
d
ou
b
te
dly i
n
fl
uence t
h
e
p
rocess.
Craw
li
n
g
or
b
urrow
i
n
gi
na
p
o
d
ous

l
arvae
i
s com
p
ara
bl
eto
p
er
i
sta
l
t
i
c
l
ocomotor
y
move-
ments
f
oun
di
not
h
er
i
nverte
b

rates,
f
or examp
l
e, mo
ll
us
k
san
d
anne
lid
s. Larvae t
h
at craw
l
o
v
er
the surface of the substrate grip the substrate with, for example, protrusible prolegs
o
r creeping welts (transversely arranged thickenings equipped with stiff hairs) situated at
4
4
9
M
U
S
CLE
S

AND
LO
C
OMOTIO
N
F
IGURE 14
.
7
.
P
hases in the passage of a peristaltic wave along the body of a caterpillar. [After G. M. Hughes,
1965, Locomotion: Terrestrial, in
:
Th
eP
h
ysio
l
ogy o
f
Insecta
,
1st e
d
., Vo
l
. II (M. Roc
k
ste

i
n, e
d
.). By perm
i
ss
i
on
o
f
Aca
d
em
i
c Press, Inc., an
d
t
h
e aut
h
or.
]
t
he
p
osterior end of the bod
y
.A
p
eristaltic wave of contraction then moves anteriorl

y,
l
en
g
t
h
en
i
n
g
an
d
narrow
i
n
g
t
h
e
b
o
dy
.T
h
e anter
i
or en
di
s attac
h

e
d
to t
h
esu
b
strate w
hil
et
he
p
oster
i
or
i
sre
l
ease
d
an
dp
u
ll
e
df
orwar
d
as t
h
e anter

i
or
l
on
gi
tu
di
na
l
musc
l
es contract. In
m
any
b
urrow
i
ng
f
orms per
i
sta
l
s
i
s procee
d
s
i
nt

h
e oppos
i
te
di
rect
i
on to movement, so t
h
at
t
he narrowing and elongation begins at the anterior end and runs posteriorly. As the anterio
r
e
nd relaxes behind the
p
eristlatic wave, it ex
p
ands. This ex
p
ansion serves both to anchor
th
e anter
i
or en
d
an
d
to en
l

ar
g
et
h
e
di
ameter o
f
t
h
e
b
urrow (Hu
gh
es an
d
M
ill
, 1974; Berr
ig
a
n
and Pe
p
in, 1995).
3
.2. Movement on or Through Wate
r
Progression on or through water presents very different problems to movement on a
so

lid
su
b
strate. For sma
ll
or
g
an
i
sms, suc
h
as
i
nsects t
h
at
li
ve on t
h
e water sur
f
ace, sur
f
ac
e
t
ens
i
on
i

sa
hi
n
d
rance
i
n
p
ro
d
uct
i
on o
fp
ro
p
u
l
s
i
ve
l
e
g
movements. For su
b
mer
g
e
di

nsects,
th
e
li
qu
id
me
di
um o
ff
ers cons
id
era
bl
e res
i
stance to movement, espec
i
a
ll
y
f
or act
i
ve
l
ysw
i
m
-

m
ing forms
.
I
nsects that move slowly over the surface of the water, for example
,
H
yd
rometra
(
Hemi
p
tera), or crawl alon
g
the bottom, for exam
p
le, larval Odonata and Tricho
p
tera,
n
orma
lly
em
pl
o
y
t
h
e
h

exa
p
o
d
a
lg
a
i
t
d
escr
ib
e
d
a
b
ove
f
or terrestr
i
a
l
s
p
ec
i
es. More ra
pidly
m
ov

i
ng spec
i
es typ
i
ca
ll
y operate t
h
e
l
egs
i
narow
i
ng mot
i
on; t
h
at
i
s,
b
ot
hl
egs o
f
t
h
e segment

m
ove synchronously. Some species do not use legs but have evolved special mechanisms
t
o facilitate rapid locomotion.
3
.2.1. Surface Running
T
h
ea
bili
t
y
to move ra
pidly
over t
h
e sur
f
ace o
f
water
h
as
b
een
d
eve
l
o
p

e
dby
mos
t
G
erroidea (Hemiptera), whose common names include pondskaters and waterstriders. T
o
stay on the surface, that is, to avoid becoming waterlogged, these insects have developed
v
arious water
p
roofin
g
features, es
p
eciall
y
h
y
dro
p
hobic (wax
y
) secretions, on the distal
p
art
s
45
0
C

HAPTER
14
o
f the legs. However, these features considerably reduce the frictional force between the
l
e
g
s and water surface which is necessar
y
for locomotion. This
p
roblem is overcome in
man
y
s
p
ec
i
es
by h
av
i
n
g
certa
i
n
p
arts o
f

t
h
e tarsus,
p
art
i
cu
l
ar
ly
t
h
ec
l
aws,
p
enetrate t
h
e
sur
f
ace fi
l
man
d/
or
by h
av
i
n

g
s
p
ec
i
a
l
structures,
f
or exam
pl
e, an ex
p
an
d
a
bl
e
f
an t
h
at o
p
en
s
wh
en t
h
e
l

eg
i
s pus
h
e
db
ac
k
war
d
.Int
h
e Gerr
id
ae,
h
owever, t
h
e
b
ac
k
war
d
pus
h
o
f
t
h

e
l
egs
is sufficiently strong that a wave of water is produced that acts as a “starting block” agains
t
w
hich the tarsi can
p
ush (Nachti
g
all, 1974)
.
Th
e
f
unct
i
ona
l
mor
ph
o
l
o
gy
an
d
mec
h
an

i
cs o
f
movement
h
ave
b
een exam
i
ne
di
n
d
eta
il
in
G
erri
s
(Brinkhurst, 1959; Darnhofer-Demar, 1969). This insect has
g
reatl
y
elon
g
ated
m
iddl
e
l

egs t
h
roug
h
w
hi
c
h
most o
f
t
h
e power
f
or movement
i
s supp
li
e
d
. Some power
i
s
derived from the hindlegs, though these function primarily as direction stabilizers. The
articulation of the coxa with the pleuron is such that the power derived from contraction of
t
h
e
l
ar

g
e troc
h
antera
l
retractor musc
l
es
i
s use
d
exc
l
us
i
ve
ly
to move t
h
e
l
e
g
s
i
nt
h
e
h
or

i
zonta
l
pl
ane, t
h
at
i
s, to e
ff
ect t
h
erow
i
n
g
mot
i
on. E
q
ua
lly
,t
h
e coxa
l
musc
l
es serve on
ly

to
lif
tt
he
l
egs
f
rom t
h
e water sur
f
ace
d
ur
i
ng protract
i
on. At t
h
e
b
eg
i
nn
i
ng o
f
a stro
k
e, t

h
e
f
ore
l
egs ar
e
l
ifted off the surface. The middle legs are rapidly retracted so that a wave of water form
s
behind the tarsi. As the legs are accelerated backward, the tarsi then push against this wave
,
c
ausin
g
the insect to move forward. After each acceleration stroke, the insect
g
lides ove
r
the surface for distances u
p
to 15 cm. The
p
ower develo
p
ed in each le
g
ofase
g
ment is

id
ent
i
ca
l
an
d
t
h
e
i
nsect g
lid
es, t
h
ere
f
ore,
i
n a stra
i
g
h
t
li
ne. Turn
i
ng can occur on
l
y

b
etween
strokes and is achieved by the independent backward or forward movement of the middl
e
l
egs over the water surface.
Waterstriders of the
g
enus
V
e
l
i
a
a
nd the sta
p
h
y
linid beetl
e
S
tenu
s
u
se an in
g
eniou
s
means o

f
s
ki
mm
i
n
g
across t
h
e water sur
f
ace. T
h
e
y
re
l
ease a sur
f
ace tens
i
on-re
d
uc
i
n
g
se
-
c

retion behind themselves and are thus
p
ulled ra
p
idl
y
forward, reachin
g
s
p
eeds of 45–70
c
m
/
sec
(
Stenus).
3.2.2. Swimming b
y
Means of Legs
B
ot
hl
arva
l
an
d
a
d
u

l
t aquat
i
cCo
l
eoptera (Dyt
i
sc
id
ae, Hy
d
rop
hilid
ae, Gyr
i
n
id
ae, Ha
li
-
p
lidae) and Hemiptera (Corixidae, Belostomatidae, Nepidae, Notonectidae) swim by means
o
f their legs. Normally, only the hindlegs or the mid- and hindlegs are used and these are
v
ariousl
y
modified so that their surface area can be increased durin
g
the

p
ro
p
ulsive strok
e
an
d
re
d
uce
d
w
h
en t
h
e
li
m
b
s are mov
i
n
g
anter
i
or
ly
.Mo
di
ficat

i
ons
i
nc
l
u
d
e (1) an
i
ncrease
i
nt
h
ere
l
at
i
ve
l
engt
h
an
d
a
fl
atten
i
ng o
f
t

h
e tarsus; (2) arrangement o
f
t
h
e
l
eg art
i
cu
l
a
-
tion, so that during the active stroke the flattened surface is presented perpendicularly to
the direction of the movement, whereas during recovery the limb is pulled with the flat
-
tened surface
p
arallel to the direction of movement; the le
g
is also flexed and drawn bac
k
cl
ose to t
h
e
b
o
dy d
ur

i
n
g
recover
y
; (3)
d
eve
l
o
p
ment o
f
art
i
cu
l
ate
dh
a
i
rs on t
h
e tarsus an
d
t
ibi
at
h
at sprea

d
perpen
di
cu
l
ar
l
ytot
h
e
di
rect
i
on o
f
movement
d
ur
i
ng t
h
e power stro
k
e
,
y
et lie flat against the leg during recovery; such hairs may increase the effective area b
y
up to five times; and (4) i
n

G
y
rinu
s
,
d
e
velopment of swimming blades on the tibia and
tarsus (Fi
g
ure 3.24A). These are articulated
p
lates that normall
y
lie flattened a
g
ainst eac
h
o
t
h
er. Dur
i
n
g
t
h
e
p
ower stro

k
e, t
h
e water res
i
stance causes t
h
em to rotate so t
h
at t
h
e
ir
e
dg
es over
l
a
p
an
d
t
h
e
i
r
fl
attene
d
sur

f
ace
i
s
p
er
p
en
di
cu
l
ar to t
h
e
di
rect
i
on o
f
movement o
f
t
h
e
l
eg
.
In addition to the surface area presented, the speed at which theleg moves is proportional
to the force develo
p

ed. Thus, it is im
p
ortant for the
p
ro
p
ulsive stroke to be ra
p
id, whereas
4
5
1
M
U
S
CLE
S
AND
LOCOMOTIO
N
t
he recovery stroke is relatively slow. Accordingly, the retractor muscles are well develope
d
com
p
ared with the
p
rotractor muscles
.
I

nt
h
e
b
est sw
i
mmers ot
h
er
i
m
p
ortant structura
l
c
h
an
g
es can
b
e seen, suc
h
as stream
-
li
n
i
n
g
o

f
t
h
e
b
o
dy
an
d
restr
i
ct
i
on o
f
movement an
d/
or c
h
an
g
e
i
n
p
os
i
t
i
on o

f
t
h
e coxa. In
a
d
u
lt
D
yt
i
scus,
f
or examp
l
e, w
hi
c
h
may reac
h
spee
d
so
f
100 cm
/
sec w
h
en pursu

i
ng prey,
t
he coxa is inserted more posteriorly than in terrestrial beetles and is fused to the thorax
.
Thus, the fulcrum for the rowin
g
action is the dicond
y
lic coxotrochanteral
j
oint whic
h
o
p
erates
lik
ea
hi
n
g
esot
h
at t
h
e
l
e
g
moves on

ly i
n one
pl
ane. Because o
f
t
hi
s arran
g
e-
m
ent, a
ll
o
f
t
h
e musc
l
e
p
ower can
b
e use
d
to e
ff
ect mot
i
on

i
nt
hi
s
pl
ane (R
ib
era
e
t al.
,
1997).
S
everal variations are found in the rhythms of leg movements. Where a single pair o
f
legs is used in swimming, both legs retract together. When both the midlegs and hindlegs
are use
d
,
b
ot
h
mem
b
ers o
f
t
h
e same
b

o
dy
se
g
ment usua
lly
move s
i
mu
l
taneous
ly
,
b
ut are
i
n
o
pp
os
i
te
ph
ase w
i
t
h
t
h
e

l
e
g
so
f
t
h
eot
h
er se
g
ment; t
h
at
i
s, w
h
en one
p
a
i
r
i
s
b
e
i
n
g
retracte

d
,
th
eot
h
er pa
i
r
i
s
b
e
i
ng protracte
d
.Ina
d
u
l
tHa
li
p
lid
ae an
d
Hy
d
rop
hilid
ae an

d
many
l
arva
l
b
eetles all three pairs of legs are used, in a manner comparable with the tripodal gait o
f
t
errestrial insects.
S
teerin
g
in the horizontal
p
lane (control of
y
awin
g
) is achieved b
y
var
y
in
g
the
p
ower
e
x

e
rte
dby
t
h
e
l
e
g
soneac
h
s
id
e. For vert
i
ca
l
steer
i
n
g
(movement u
p
or
d
own) t
h
e non
-
propu

l
s
i
ve
l
egs
b
ecome
i
nvo
l
ve
d
.T
h
ese may
b
e
h
e
ld
out
f
rom t
h
e
b
o
d
y

i
nt
h
e manner o
f
a rudder or may act as weakly beating oars. By varying the angle to the body at which
t
he legs are placed the insect will either dive, surface, or move horizontally through the
w
ater. Most a
q
uatic insects are
q
uite stable in the rollin
g
and
p
itchin
gp
lanes because of
th
e
i
r
d
orsoventra
lly fl
attene
db
o

dy
. (See F
ig
ure 14.14
f
or ex
pl
anat
i
on o
f
t
h
e terms
y
aw
i
n
g,
pi
tc
hi
n
g
,an
d
ro
lli
n
g

.)
3
.2.3. Swimming b
y
Other Means
A
v
a
r
i
et
y
o
f
ot
h
er met
h
o
d
s
f
or mov
i
n
g
t
h
rou
gh

water can
b
e
f
oun
di
n
i
nsects,
i
nc
l
u
di
n
g
b
o
d
y cur
li
ng an
d
somersau
l
t
i
ng
f
oun

di
n many
l
arva
l
an
d
pupa
l
D
i
ptera,
b
o
d
yun
d
u
l
at
i
o
n
(
larval Ephemeroptera and Zygoptera), jet propulsion (larval Anisoptera), and flying (a fe
w
adult Lepidoptera and Hymenoptera) (Nachtigall, 1974)
.
M
an

y
mid
g
e and mos
q
uito larvae ra
p
idl
y
coil the bod
y
sidewa
y
s, first in one direc-
ti
on, t
h
en t
h
eot
h
er,toac
hi
eveare
l
at
i
ve
ly i
ne

f
fic
i
ent
f
orm o
fl
ocomot
i
on. C
hi
ronom
id
s,
f
or exam
pl
e,
l
ose 92% o
f
t
h
e ener
gy
ex
p
en
d
e

di
nt
h
e
p
ower stro
k
e
d
ur
i
n
g
recover
y
. Conse-
quently, a
5
.
5
-mm larva oscillating its body 10 times per second moves at only 1.7 mm/sec
t
hrough the water. Mosquito larvae possess flattened groups of hairs (swimming fans) or
solid “
p
addles” at the ti
p
of the abdomen and are conse
q
uentl

y
more efficient and more
act
i
ve sw
i
mmers t
h
an c
hi
ronom
id
s
.
Pu
p
ae o
f
m
idg
es an
d
mos
q
u
i
toes somersau
l
tt
h

rou
gh
t
h
e water, es
p
ec
i
a
lly
w
h
en at-
t
empt
i
ng to escape pre
d
ators. Interest
i
ng
l
y, t
h
e sur
f
ace-
d
we
lli

ng pupa o
f
t
h
e mosqu
i
t
o
Cu
l
e
x
pipi
ens
s
omersaults at a greater frequency (hence swims faster) than the bottom-dwellin
g
p
u
p
a of the mid
g
e C
h
ironomus p
l
umosu
s
,p
erha

p
s because there is
g
reater
p
redator
p
ressure
f
or a sur
f
ace-
d
we
ll
er (Brac
k
en
b
ur
y
, 2000)
.
Larvae o
f
Z
yg
o
p
tera an

d
some E
ph
emero
p
tera un
d
u
l
ate t
h
ea
bd
omen, w
hi
c
hi
s
e
qu
i
ppe
d
at
i
ts t
i
pw
i
t

h
t
h
ree
fl
attene
dl
ame
ll
ae (Zygoptera, F
i
gure
6
.11) or sw
i
mm
i
n
g
fans (Ephemeroptera, Figure 6.4). Some ephemeropteran larvae supplement the action o
f
t
he fans b
y
ra
p
idl
y
foldin
g

their abdominal
g
ills a
g
ainst the bod
y.
452
C
HAPTER
14
D
ragonfly larvae (Anisoptera) normally take in and expel water from the rectum durin
g
g
as exchan
g
e (Cha
p
ter 15, Section 4.1). In emer
g
encies this arran
g
ement can be converte
d
into a
j
et
p
ro
p

ulsion s
y
stem for movin
g
an insect forward at hi
g
hs
p
eed (u
p
to 50 cm/sec).
Ra
pid
contract
i
on o
fl
on
gi
tu
di
na
l
musc
l
es causes t
h
ea
bd
omen to s

h
orten
by
u
p
to 10%.
Si
mu
l
taneous contract
i
on o
f
t
h
e
d
orsoventra
l
musc
l
es
l
ea
d
stoan
i
ncrease
i
n

h
emo
l
ymp
h
p
ressure which forces water out of the rectum via the narrow anus at speeds approaching
2
50 cm
/
sec.
Fe
m
ale
H
y
drocampa n
y
mpheat
a
(
Le
pid
o
p
tera) an
d
a
d
u

l
t
D
acun
s
a
(
H
y
meno
p
tera
)
use
t
h
e
i
rw
i
n
g
s
i
na
ddi
t
i
on to
l

e
g
s
f
or sw
i
mm
i
n
g
un
d
erwater. Ot
h
er H
y
meno
p
tera (
P
olynem
a
an
d
Limn
od
ite
s
)
sw

i
mso
l
e
l
y
b
yt
h
e use o
f
t
h
e
i
rw
i
ngs.
3.3. Fli
g
h
t
As note
di
nC
h
a
p
ter 2, Sect
i

on 3.1, w
i
n
gp
recursors or
igi
na
lly h
a
df
unct
i
ons
q
u
i
te
unre
l
ate
d
to
fli
g
h
t. Su
b
sequent evo
l
ut

i
on
l
e
d
to en
l
argement an
d
per
h
aps art
i
cu
l
at
i
on o
f
these structures as they took on a new function, propulsion of an insect through the air,
p
artly as a result of which insects were able to move into new environments to become the
diverse
g
rou
p
we know toda
y
. Des
p

ite this diversit
y
, there is sufficient similarit
y
of skeletal
an
d
neuromuscu
l
ar structure an
df
unct
i
on to su
gg
est t
h
at w
i
n
g
s
h
a
d
a mono
phyl
et
i
cor

igin
(Pr
i
ng
l
e, 1974)
.
E
xamination of the form and mode of operation of the pterothorax reveals certain
trends, all of which lead to an improvement in flying ability. Primitively, the power for wing
movement was derived from various “direct” muscles, that is, those directl
y
connected with
t
h
ew
i
n
g
art
i
cu
l
at
i
ons. T
h
ese musc
l
es serve a

l
so to
d
eterm
i
ne t
h
e nature o
f
t
h
ew
i
n
gb
eat
.
Even to
d
a
y
,t
h
e
di
rect musc
l
es rema
i
n

i
m
p
ortant
p
ower su
ppli
ers
i
nt
h
eO
d
onata, Ort
h
o
p
tera
,
Di
ctyoptera (B
l
atto
d
ea), an
d
Co
l
eoptera. In ot
h

er
i
nsect groups, e
f
fic
i
ency
i
s
i
ncrease
dby
separating the control of wing beat (by the direct muscles) from power production, whic
h
becomes the
j
ob of lar
g
e “indirect” muscles located in the thorax
.
Th
ere are
i
m
p
ortant
diff
erences
i
nt

h
e fine structure an
d
neuromuscu
l
ar
phy
s
i
o
l
o
gy
o
f
t
h
e
di
rect an
di
n
di
rect
fligh
t musc
l
es. Genera
lly
,

i
n
i
nsects t
h
at
fl
a
p
t
h
e
i
rw
i
n
g
sre
l
at
i
ve
ly
s
l
ow
l
y (up to 100
b
eats

/
sec), eac
hb
eat o
f
t
h
ew
i
ngs
i
s
i
n
i
t
i
ate
db
ya
b
urst o
fi
mpu
l
ses to t
h
e
p
ower-producing muscles, which are of the tubular or close-packed type (Figure 14.3B, C).

T
his applies to all users of direct muscles for powering flight, plus Lepidoptera in which the
indirect muscles are used. In contrast, in fliers that use indirect muscles and whose win
g
-beat
f
re
q
uenc
yi
s
high
(u
p
to 1000
b
eats
/
sec), musc
l
e contract
i
on
i
s not
i
ns
y
nc
h

ron
y
w
i
t
h
t
h
e
arr
i
va
l
o
f
nerve
i
mpu
l
ses at t
h
e neuromuscu
l
ar
j
unct
i
on. Rat
h
er, t

h
er
h
yt
h
mo
f
contract
i
on
is
generated within the muscles themselves, which are fibrillar (Figure 14.3D). Accordingly
,
the two forms of rhythm are described as synchronous (neurogenic) and asynchronou
s
(m
y
o
g
enic), res
p
ectivel
y
. The use of as
y
nchronous muscles to
p
ower fli
g
ht has evolved

severa
l
t
i
mes w
i
t
hi
nt
h
e Insecta. Its s
ig
n
i
ficance a
pp
ears to
b
et
h
e
f
ac
ili
tat
i
on o
f high
w
i

n
g
-
b
eat
f
re
q
uenc
i
es, t
h
ere
by
mov
i
n
g
more a
i
r, so t
h
at even
i
nsects w
i
t
h
sma
ll

w
i
n
g
sre
l
at
i
ve t
o
their body size are efficient fliers.
3.3.1. Structural Basis
E
ach wing-bearing segment is essentially an elastic box whose shape can be change
d
by contractions of the muscles within, the changes in shape causing the wings to mov
e
u
p
and down. The skeletal com
p
onents of a
g
eneralized win
g
-bearin
g
se
g
ment are shown

4
5
3
M
U
S
CLE
S
AND
LOCOMOTIO
N
i
n Figure 3.18. The essential features are as follows. Each segment contains two large
i
nterse
g
mental inva
g
inations, the
p
re
p
hra
g
ma and
p
ost
p
hra
g

ma, between which the dorsal
l
on
gi
tu
di
na
l
musc
l
es stretc
h
.T
h
ea
li
notum
b
ears on eac
h
s
id
e an anter
i
or an
d
a
p
oster
i

or
n
ota
lp
rocess, to w
hi
c
h
t
h
ew
i
n
gi
s attac
h
e
d
v
i
at
h
e first an
d
t
hi
r
d
ax
ill

ar
y
sc
l
er
i
tes. T
h
e
p
l
euron
i
s
l
arge
l
ysc
l
erot
i
ze
d
an
d
art
i
cu
l
ates w

i
t
h
t
h
ew
i
ng
b
y means o
f
t
h
ep
l
eura
l
w
i
n
g
process, above which sits the second axillary sclerite. The hinge so formed is important
i
n win
g
movement because of the resilin that it contains (but see Section 3.3.3). Two
ot
h
er
i

m
p
ortant art
i
cu
l
at
i
n
g
sc
l
er
i
tes, w
hi
c
h
are usua
lly q
u
i
te se
p
arate
f
rom t
h
esc
l

erot
i
ze
d
p
ort
i
on o
f
t
h
e
pl
euron, are t
h
e anter
i
or
b
asa
l
ar an
dp
oster
i
or su
b
a
l
ar. Interna

lly
,t
h
e
pl
euro
n
an
d
sternum are t
hi
c
k
ene
d
,
f
orm
i
ng t
h
ep
l
eura
l
an
d
sterna
l
apop

h
yses, respect
i
ve
l
y, w
hi
c
h
b
race the pterothorax. In some insects these apophyses are fused, but generally they ar
e
j
oined by a short but powerful pleurosternal muscle (Figure 14.8B).
T
h
e musc
l
es use
di
n
fligh
tma
yb
ese
p
arate
di
nto t
h

ree cate
g
or
i
es accor
di
n
g
to t
h
e
i
r
anatom
i
ca
l
arran
g
ement (F
ig
ure 14.8A, B). T
h
e
i
n
di
rect
fligh
t musc

l
es
i
nc
l
u
d
et
h
e
d
orsa
l
l
ong
i
tu
di
na
l
musc
l
es,
d
orsoventra
l
musc
l
es, o
bli

que
d
orsa
l
musc
l
es, an
d
o
bli
que
i
nterseg-
m
ental muscles. The direct muscles are the basalar and subalar muscles, and the axillar
y
m
uscles attached to the axillary sclerites (including the wing flexor muscle, which runs from
t
he
p
leuron to the third axillar
y
sclerite). In the third cate
g
or
y
are the accessor
y
indirect

m
usc
l
es t
h
at com
p
r
i
se t
h
e
pl
eurosterna
l
, ter
g
o
pl
eura
l
,an
di
nterse
g
menta
l
musc
l
es. T

h
e
i
r
f
unct
i
on
i
sto
b
race t
h
e pterot
h
orax or to c
h
ange t
h
e pos
i
t
i
on o
fi
ts components re
l
at
i
ve t

o
e
ach other. In addition, certain extrinsic leg muscles may also be important in wing move-
m
ents. For example, in Coleoptera, whose coxae are fused to the thorax, the coxoterga
l
m
uscles can assist the dorsoventral muscles in su
pp
l
y
in
gp
ower to raise the win
g
s. In other
s
p
ec
i
es w
i
t
h
art
i
cu
l
ate
d

coxae t
h
eu
pp
er
p
o
i
nt o
fi
nsert
i
on o
f
t
h
e extr
i
ns
i
c coxa
l
musc
l
es
m
a
y
c
h

an
g
etot
h
e
b
asa
l
ar or su
b
a
l
ar. T
h
us, t
h
e musc
l
es can a
l
ter
b
ot
hl
e
g
an
d
w
i

n
gp
o-
s
i
t
i
ons, t
h
at
i
s, t
h
ey may
h
ave a
d
ua
ll
ocomotory
f
unct
i
on. For examp
l
e,
in
S
c
h

istocerca
gregar
ia
the anterior and posterior tergocoxal (indirect) muscles act synergistically durin
g
fli
g
ht (1) to
p
rovide
p
ower for the u
p
stroke of the win
g
s and (2) to draw the le
g
su
p
clos
e
t
ot
h
e
b
o
dy
.T
hi

s
i
sac
hi
eve
d
t
h
rou
gh p
o
ly
neurona
li
nnervat
i
on, w
h
ere
by
t
h
e
p
arts o
f
t
he
t
er

g
ocoxa
l
musc
l
es t
h
at rece
i
ve s
l
ow an
di
n
hibi
tor
y
motor axons are res
p
ons
ibl
e
f
or t
he
d
raw
i
ng up o
f

t
h
e
l
egs, an
d
t
h
e musc
l
efi
b
ers
i
nnervate
db
yt
h
e
f
ast axon move t
h
ew
i
ngs. I
n
contrast, when the insect is running, the anterior and posterior tergocoxal muscles function
antagonistically, effecting promotion and remotion, respectively, of the legs. In the sam
e
s

p
ecies, the (direct) second basalar and subalar muscles, while actin
g
s
y
ner
g
isticall
y
to ai
d
th
e
i
n
di
rect musc
l
es
i
nt
h
e
p
ro
d
uct
i
on o
fp

ower
f
or t
h
e
d
ownstro
k
eo
f
t
h
ew
i
n
g
s, act anta
g-
on
i
st
i
ca
ll
yto
b
r
i
ng a
b

out w
i
ng tw
i
st
i
ng (pronat
i
on an
d
sup
i
nat
i
on, respect
i
ve
l
y) or, w
h
en
r
unning, promotion and remotion, respectively, of the legs (Figure 14.9) (Wilson, 1962)
.
3
.3.2. Aerod
y
namic Consideration
s
Flight occurs when the air pressure is greater on the lower than on the upper surface of

a body. The wings, with their large surface area, act as aerofoils, that is, the portion of the
b
od
y
that is lar
g
el
y
res
p
onsible for lift (the com
p
onent of net aerod
y
namic force that acts
p
er
p
en
di
cu
l
ar to t
h
e
di
rect
i
on o
f

movement). In a fixe
d
-w
i
n
g
a
i
rcra
f
t
flyi
n
gh
or
i
zonta
lly
,
lift
o
nt
h
ew
i
n
g
s
i
s vert

i
ca
l
(e
q
ua
l
an
d
o
pp
os
i
te to t
h
ea
i
rcra
f
t’s we
igh
t). In
i
nsects,
h
owever,
wh
ere t
h
ew

i
ngs
fl
ap, tw
i
st, an
dd
e
f
orm cyc
li
ca
ll
y,
lif
tont
h
ew
i
ngs var
i
es t
h
roug
h
t
h
ecyc
l
e.

Lift develops when air is accelerated unequally over the upper and lower surfaces
o
f a win
g
. Aerofoils on fixed-win
g
aircraft are desi
g
ned with their u
pp
er surface curved
,
4
5
4
C
HAPTER
14
F
IGURE 14.8
.
(
A) Indirect; and (B) accessory indirect muscles and direct muscles of right side of wing-bearing
se
g
ment, seen from within. [After J. W. S. Prin
g
le, 19
5
7

,
Insect F
l
i
gh
t.
By p
erm
i
ss
i
on o
f
Cam
b
r
idg
eUn
i
vers
i
t
y
Press, London.]
their lower surface flat (Figure 14.10A), so as to make use of Bernoulli’s principle that the
p
ressure exerted by flowing air is inversely related to the square of the velocity. Air flowing
ove
r
t

he u
pp
er surface of an aerofoil travels farther and therefore has a
g
reater velocit
y
tha
n
t
h
ea
i
r
fl
ow
i
n
gb
eneat
h
. Hence, t
h
e
p
ressure
b
eneat
h
t
h

e aero
f
o
il i
s
g
reater t
h
an t
h
at a
b
ove
4
55
M
U
S
CLE
S
AND
LOCOMOTIO
N
F
I
GU
RE 14
.
9
.

D
ia
g
ram illustratin
g
t
he synergistic-antagonistic relation-
ship
s
b
etween
bif
unct
i
ona
l
musc
l
es
i
n
t
he thorax of the desert locust. [After
D. M. Wilson, 1962, Bifunctional mus-
c
l
es
i
nt
h

et
h
orax o
fg
rass
h
o
pp
ers
,
J.
Ex
p
. Biol.
39
:669–677. B
yp
ermission of
Cambridge University Press, London.]
F
IGURE 14.10. Generation of lift as a result of different air speeds above and below an aerofoil. (A) Fixed-
w
i
n
g
a
i
rcra
f
tw

h
ose w
i
n
gh
as curve
d
u
pp
er an
dfl
at
l
ower sur
f
ace; an
d
(B)
i
nsect w
i
n
g
w
hi
c
hi
so
f
more un

if
orm
t
hickness. At stroke initiation, a startin
g
vortex is develo
p
ed at the win
g
’s trailin
g
ed
g
e, which then
p
roduces a
b
ound vortex circulating clockwise round the wing.
45
6
C
HAPTER
14
and, provided that the force generated is greater than the gravitational force as a result of
the bod
y
’s mass, the bod
y
will be raised into the air.
In a

i
rcra
f
tt
h
efixe
d
w
i
n
g
ssu
pply
on
ly lif
t, an
dh
or
i
zonta
lp
ro
p
u
l
s
i
ve
f
orce (t

h
rust)
i
s
su
ppli
e
dby
en
gi
nes. In
i
nsects, w
i
n
g
s are mova
bl
ean
d
su
pply
t
h
rust as we
ll
as
lif
t. Furt
h

er,
i
nsect w
i
ngs are o
f
un
if
orm t
hi
c
k
ness; t
h
at
i
s, t
h
ey
d
o not
h
ave curve
d
upper an
dfl
at
l
ower
surfaces. Thus, to develop both lift and thrust during their stroke, wings both move up and

down and chan
g
e their an
g
le of attack
.
W
h
en an
i
nsect w
i
n
gb
e
gi
ns to acce
l
erate t
h
rou
gh
a
i
r, a start
i
n
g
vortex (c
i

rcu
l
at
i
o
n
of
a
i
r, as
i
naw
hi
r
l
w
i
n
d
)
i
s
d
eve
l
o
p
e
d
at t

h
ew
i
n
g
’s tra
ili
n
g
e
dg
e(F
ig
ure 14.10B). T
hi
s
v
ortex,
i
n turn, creates a secon
d
vortex (
b
oun
d
vortex) t
h
at moves c
l
oc

k
w
i
se roun
d
t
he
w
ing, backward over the upper surface, and forward over the lower surface. This causes th
e
air flow to speed up on the wing’s upper surface, whereas on the lower surface air flow i
s
s
l
owe
d
.T
h
ese
diff
erences
i
na
i
rs
p
ee
dg
enerate
lif

t.
Th
ere
l
at
i
ve va
l
ues o
f lif
tan
d
t
h
rust w
ill
c
h
an
g
et
h
rou
gh
out t
h
ew
i
n
gb

ea
t
(F
i
gure 14.11). In t
h
em
iddl
eo
f
a
d
ownstro
k
e, t
h
e rap
id d
ownwar
d
movement o
f
t
h
ew
i
n
g
o
perating in conjunction with the already moving horizontal stream of air over the wings

(assuming the insect is in forward flight) will result in a positive angle of attack (i.e., the air
w
ill strike the underside of the win
g
) and
g
ive rise to a stron
g
l
yp
ositive lift. Concurrentl
y
,
b
ecause t
h
ew
i
n
gi
s
p
ronate
d
(
i
ts
l
ea
di

n
g
e
dg
e
i
s
p
u
ll
e
dd
own), t
h
ere w
ill b
eas
ligh
t
ly
p
os
i
t
i
ve t
h
rust (F
i
gure 14.11B). Dur

i
ng an upstro
k
e, t
h
e ang
l
eo
f
attac
kb
ecomes s
li
g
h
t
l
y
negative (pressure of air above is greater than pressure of air below the wing) causin
g
slightly negative lift, yet increasing the positive thrust (Figure 14.11C). The angle at whic
h
an insect holds its bod
y
in fli
g
ht also results in
p
ositive lift, thou
g

h this amounts to less than
5
% of the total lift in the desert locust and about 20% in some Di
p
tera.
Fo
r man
yy
ears
i
t was assume
d
t
h
at t
h
e
lif
t
g
enerate
dby
t
h
ew
i
n
g
movements
d

e-
scr
ib
e
d
a
b
ove was su
f
fic
i
ent
f
or
i
nsect
fli
g
h
t. However, ca
l
cu
l
at
i
ons s
h
owe
d
t

h
at conven-
tional (steady-state) aerodynamic theory, which is based on rigid wings moving at con
-
stant velocit
y
, cannot account for the
p
roduction of lift in most insects. Ellin
g
ton’s and
D
ickinson’s
g
rou
p
s (see Ellin
g
ton, 1995, 1999; Ellin
g
ton
e
t al.
,
199
6;
D
i
c
ki

nson
e
t al.
,
1
999; D
i
c
ki
nson an
d
Du
dl
e
y
, 2003; Sane, 2003) stu
di
e
d
t
h
e aero
dy
nam
i
c
p
er
f
ormanc

e
of b
ot
h
t
h
ew
i
ngs o
f
tet
h
ere
di
nsects (
b
um
bl
e
b
ees an
dh
aw
k
mot
h
s) an
d
mec
h

an
i
ca
ll
y
p
owered model wings. As a result, it is now considered that lift in most flying insects
is produced by three interactive mechanisms: delayed (dynamic) stall, rapid wing rota-
tion, and wake ca
p
ture (Fi
g
ure 14.12). Dela
y
ed stall o
p
erates durin
g
the main “transla
-
t
i
ona
l
”
p
art o
f
a stro
k

e(
b
ot
h
u
p
an
dd
own), w
h
ereas t
h
eot
h
er two mec
h
an
i
sms occur
d
ur
i
ng stro
k
e reversa
l
,t
h
at
i

s, w
h
en t
h
ew
i
ngs tw
i
st an
d
reverse
di
rect
i
on (D
i
c
ki
nso
n
e
tal
.
,
1
999
).
D
elayed stall refers to the condition in which for a brief period wings can be held wit
h

ahi
g
han
g
le of attack, thus
p
roducin
g
a leadin
g
-ed
g
e vortex. The latter creates a re
g
ion of
l
ow
p
ressure a
b
ove t
h
ew
i
n
g
s, t
h
us au
g

ment
i
n
g lif
t. T
h
e vortex a
pp
ears at t
h
e
b
e
gi
nn
i
n
g
o
f
t
h
e
d
ownstro
k
ean
df
orms a con
i

ca
l
s
pi
ra
l
,
g
ett
i
n
gl
ar
g
er as
i
tmovestowar
d
t
h
ew
i
n
g
t
ip
,
generating lift equivalent to about 1.
5
times the weight of the hawk moth (Ellingto

n
e
ta
l
.
,
1
996). The tipward flow of the vortex also increases stability. Toward the end of a stroke,
the vortex is shed as the win
g
s twist and reverse direction
.
Dicki
n
so
n
e
tal
.
(
1999), w
hil
e confirm
i
n
g
t
h
e
i

m
p
ortance o
fd
e
l
a
y
e
d
sta
ll
,s
h
owe
d
t
h
a
t
ra
pid
w
i
n
g
rotat
i
on an
d

wa
k
eca
p
ture a
l
so contr
ib
ute to t
h
e
g
enerat
i
on o
f lif
tus
i
n
g
t
h
e
ir
l
arge-sca
l
emo
d
e

l
o
f
t
h
e
D
roso
ph
i
l
a w
i
ng. Rap
id
c
i
rcu
l
at
i
on o
f
a
i
r
i
nt
h
e

b
oun
d
ary
l
ayer
is induced around a spinning object, for example, a ball. If the ball is thrown with spin
,
4
57
M
U
S
CLE
S
AND
LOCOMOTIO
N
F
IGURE 14.11
.
(
A) C
h
anges
i
nt
h
e ang
l

eatw
hi
c
h
aw
i
ng
i
s
h
e
ld i
n
fli
g
h
tre
l
at
i
ve to
di
rect
i
on o
f
movement.
A
rrows indicate the an
g

le at which air strikes the win
g
. Numbers indicate chronolo
g
ical se
q
uence of win
gp
ositions
during a stroke; and (B,C) Magnitude of lift and thrust approximately midway through downstroke and upstroke,
r
espectively. [A, after M. Jensen, 19
5
6, Biology and physics of locust flight. III. The aerodynamics of locust flight
,
Philos. Trans. R. Soc. Lond. Ser. B
2
3
9
:
5
11–
55
2. B
yp
ermission of The Ro
y
al Societ
y
, London, and the author.

B, C, after R. F. Chapman, 1971
,
T
he Insects:
S
tructure and Function
.
B
y permission of Elsevier/North-Holland,
I
nc., an
d
t
h
e aut
h
or.
]
air flows unequally over the top and bottom of the ball causing it to swerve. Dickinson
e
ta
l
.
(
1999) su
gg
ested that the transient increase in lift which occurs as a win
g
rotate
s

j
ust
b
e
f
ore t
h
een
d
o
f
a stro
k
e
h
asas
i
m
il
ar ex
pl
anat
i
on. T
h
e
k
e
y
to rotat

i
on-
g
enerate
d lift
i
st
h
et
i
m
i
n
g
o
f
w
i
n
g
rotat
i
on. I
f
rotat
i
on
p
rece
d

es stro
k
e reversa
l
,w
hi
c
hi
s ana
l
o
g
ous to
i
mpart
i
ng
b
ac
k
sp
i
ntot
h
e
b
a
ll
, pos
i

t
i
ve
lif
t
i
s generate
d
;
if i
t
f
o
ll
ows stro
k
e reversa
l
(a
ki
n
t
o topspin), the lift is negative. Rotation-generated lift is probably of particular importanc
e
i
n the fine control of fli
g
ht maneuvres. The remainin
g
contribution is derived from wak

e
458
C
HAPTER
14
F
I
GU
RE 14
.
12
.
A
ir flow around the win
g
and the resultin
g
forces at
p
oints durin
g
a win
g
stroke. Dela
y
ed stall
(1) results from formation of a leading edge vortex on the wing. Rotation-generated lift (2,3) occurs when the
w
ing rapidly rotates at the end of the stroke. Wake capture (4,
5

) results from collision of the wing with the wake
shed durin
g
the
p
revious stroke. [Re
p
rinted from Enc
y
clopedia of Insect
s
,M.
D
ickinson and R. Dudle
y
, Fli
g
ht,
pages 416–426
,

c
2003, with permission from Elsevier.]
c
a
p
ture; t
h
at
i

s, a
f
ter revers
i
n
gdi
rect
i
on t
h
ew
i
n
gd
oes not move t
h
rou
gh
un
di
stur
b
e
d
a
i
r
b
u
t

r
e-encounters t
h
e vort
i
ces s
h
e
df
rom t
h
ew
i
ng t
i
ps
d
ur
i
ng t
h
e prev
i
ous stro
k
etopro
d
uce
a pulse of lift. Collectively, delayed stall, rotational circulation and wake capture enable
insects to

g
enerate lift e
q
uivalent to several times their bod
y
wei
g
ht.
Af
ew,
f
f
es
p
ec
i
a
lly
ver
y
sma
ll
,
i
nsects suc
h
as t
h
r
ip

s, w
hi
te
fly
,an
dp
aras
i
to
id
was
p
s
(w
h
ose w
i
n
g
s
p
ans are a
b
out1mmor
l
ess) use a
p
art
i
cu

l
ar
f
orm o
f
rotat
i
on-
g
enerate
d lift
k
nown as t
h
e“c
l
ap an
dfli
ng” mec
h
an
i
sm (We
i
s-Fog
h
, 1973) (F
i
gure 14.13). In t
hi

s system
l
ift is generated by rotation of the wings as they separate after they have clapped together a
t
the end of the upstroke and are flung apart as the downstroke begins. As the wings rotate,
a
s
tart
i
n
g
vortex
i
s
f
orme
d
a
b
ove eac
h
w
i
n
g
,w
hi
c
h
serves to

g
enerate a
b
oun
d
vortex aroun
d
eac
h
w
i
n
g
.Asout
li
ne
d
a
b
ove
f
or convent
i
ona
lly fl
a
ppi
n
g
w

i
n
g
s, t
h
e vortex causes t
h
e
v
e
l
oc
i
ty o
f
a
i
r pass
i
ng over t
h
e top o
f
eac
h
w
i
ng to
i
ncrease, w

hil
et
h
at pass
i
ng
b
eneat
h
t
he
w
ing decreases. Thus, by Bernoulli’s principle, lift is generated
.
3.3.3. Mechanics of Wing Movement
s
A
ll i
nsects use t
h
e
i
n
di
rect tergosterna
l
or tergocoxa
l
musc
l

es to ra
i
se t
h
ew
i
ng. Con-
traction of these muscles pulls the tergum down so that its points of articulation with th
e
w
ing fall below the articulation of the wing with the pleural wing process which serve
s
as a
f
u
l
crum (F
ig
ure 14.14A). In most
i
nsects
i
n
di
rect musc
l
es are a
l
so use
d

to
l
ower t
he
wi
n
g
.S
h
orten
i
n
g
o
f
t
h
e
d
orsa
ll
on
gi
tu
di
na
l
musc
l
es causes t

h
e ter
g
um to
b
ow u
p
war
d
,
ra
i
s
i
ng t
h
e anter
i
or an
d
poster
i
or nota
l
processes a
b
ove t
h
et
i

po
f
t
h
ep
l
eura
l
w
i
ng process
F
IGURE 14
.
1
3.
Clap and fling mechanism for generating lift. The wings clap together at the end of the upstroke
(A), t
h
en are
fl
ung apart as t
h
e
d
ownstro
k
e
b
eg

i
ns (B,C), creat
i
ng a
b
oun
d
vortex (D) (greater a
i
r spee
d
over t
h
e
u
pp
er win
g
surface com
p
ared to the lower win
g
surface, thereb
y
creatin
g
lift). [From T. Weis-Fo
g
h, 197
5

, Unusua
l
mechanisms for the generation of lift,
S
ci. Amer
.
2
33
(
November):80–87. Original drawn by Tom Prentiss. By
p
erm
i
ss
i
on o
f
Ne
l
son H. Prent
i
ss.
]
4
5
9
M
U
S
CLE

S
AND
LO
C
OMOTIO
N
F
I
GU
RE 14
.
14
.
D
ia
g
rammatic transverse sections of thorax to show muscles used in u
p
stroke and downstroke.
(
A) Use of indirect muscles to raise wing; (B) use of indirect muscles to lower wing; and (C) use of direct
m
usc
l
es to
l
ower w
i
ng. [A
f

ter R. F. C
h
apman, 1971,
Th
e Insects: Structure an
d
Function
.
B
y perm
i
ss
i
on o
f
E
lsevier/North-Holland, Inc., and the author.
]
an
d
,t
h
ere
f
ore, t
h
ew
i
n
g

to
b
e
l
owere
d
(F
ig
ure 14.14B). In Co
l
eo
p
tera an
d
Ort
h
o
p
tera some
power
f
or a
d
ownstro
k
e
i
sa
l
so o

b
ta
i
ne
db
y contract
i
on o
f
t
h
e
b
asa
l
ar an
d
su
b
a
l
ar musc
l
e
s
and in Odonata and Blattodea, this power is derived entirely from contraction of these direct
m
uscles. The points of articulation of these muscles with the wing sclerites lie outside th
e
pl

eura
l
w
i
n
gp
rocess so t
h
at w
h
en t
h
e musc
l
es contract t
h
ew
i
n
gi
s
l
owere
d
(F
ig
ure 14.14C).
I
na
ll i

nsects,
h
owever, t
h
e
b
asa
l
ar an
d
su
b
a
l
ar musc
l
es are
i
m
p
ortant
i
nw
i
n
g
tw
i
st
i

n
g
,t
h
a
t
i
s, a
l
ter
i
ng t
h
e ang
l
eatw
hi
c
h
t
h
ew
i
ng meets t
h
ea
i
r, t
h
ere

b
ya
ff
ect
i
ng t
h
eva
l
ues o
f
t
h
e
lift and thrust generated. Contraction of the basalar muscles causes the anterior edge of th
e
w
ing to be pulled down (pronation), whereas contraction of the subalar induces supinatio
n
(
t
h
e
p
u
lli
n
gd
own o
f

t
h
e
p
oster
i
or e
dg
eo
f
t
h
ew
i
n
g
). Contract
i
on o
f
t
h
eot
h
er
di
rect musc
l
e,
th

ew
i
n
gfl
exor, causes t
h
et
hi
r
d
ax
ill
ar
y
sc
l
er
i
te to tw
i
st an
d
to
b
e
p
u
ll
e
di

nwar
d
an
dd
or
-
sa
ll
y. T
hi
spu
ll
st
h
e vanna
l
area o
f
t
h
ew
i
ng (F
i
gure 3.27) up over t
h
e
b
o
d

yan
d
ena
bl
es t
h
e
w
ing to fold along predetermined lines (usually the anal veins, and vannal and jugal folds)
.
Unfolding (extension) of the wing occurs when the basalar muscle contracts.
Earl
y
descri
p
tions of the role of muscles in win
g
fla
pp
in
g
envisioned the muscles a
s
su
pplyi
n
gp
ower
di
rect

ly
to t
h
ew
i
n
g
stoe
ff
ect t
h
ew
i
n
gb
eat. T
h
us, t
h
es
p
ee
d
w
i
t
h
w
hi
c

h
m
usc
l
es cou
ld
contract wou
ld d
eterm
i
ne t
h
e spee
d
at w
hi
c
h
aw
i
ng was
l
owere
d
or ra
i
se
d
.
I

n turn, this determined the value of the lift generated. Not until the 19
5
0s was it realize
d
t
hat a critical feature is the ability to store a large proportion of the energy released at the end
of each stroke, when a win
g
’s momentum is ra
p
idl
y
reduced. The momentum is reduced
by
(an
d
t
h
e ener
gy
store
di
n) e
l
ast
i
c structures. T
h
en,
i

nt
h
e
f
o
ll
ow
i
n
g
stro
k
et
h
ee
l
ast
i
c
e
ner
gy i
s use
d
to
p
ower w
i
n
g

movement, ma
ki
n
g
t
h
e
p
rocess remar
k
a
bly
e
f
fic
i
ent. For
e
xamp
l
e,
b
ecause t
h
e upstro
k
e
i
sa
id

e
db
yt
h
e pressure o
f
t
h
e onrus
hi
ng a
i
ront
h
eun
d
ers
id
e
of the wing, only a small amount of the stored elastic energy is used to raise the wing. The
r
emainder (about 86% in the desert locust) is then used to
p
ower the followin
g
downstroke
(
Pr
i
n

gl
e, 1974). In
i
nsects t
h
at use s
y
nc
h
ronous musc
l
es to
g
enerate
p
ower, t
h
e
p
r
i
nc
ip
a
l
s
i
tes
f
or stora

g
eo
f
e
l
ast
i
c ener
gy
are t
h
e
l
atera
l
wa
ll
so
f
t
h
e
p
terot
h
orax an
d
t
h
e res

ili
n-
conta
i
n
i
ng
hi
nge
b
etween t
h
ep
l
eura
l
w
i
ng process an
d
secon
d
ax
ill
ary sc
l
er
i
te. However
,

i
n insects that have fibrillar muscles with their greater elasticity (i.e., use asynchronou
s
control of muscle contraction) the energy is mainly stored in the muscles themselves.
4
60
C
HAPTER
14
3.3.4. Control of Wing Movement
s
L
ike leg movements, wing flapping is a centrally generated, rhythmically repeate
d
p
rocess; that is, each wing has its own muscles and motor neurons whose activity is initiated
b
y
s
p
ecific interneurons in each se
g
mental
g
an
g
lion. I
n
L
ocusta migratori

a
Robertson and
P
earson (1982) identified 25 such interneurons whose s
p
ike activit
y
or membrane
p
otential
ch
an
g
e
d
r
hy
t
h
m
i
ca
lly d
ur
i
n
g
fict
i
ve

fligh
t
.
*
F
ligh
t
i
s not, o
f
course, s
i
m
ply
t
h
e
fl
a
ppi
n
g
o
f
t
h
ew
i
ngs. It
i

s a comp
l
ex process an
d
at any po
i
nt
i
nt
i
me an
i
nsect
i
s concerne
d
w
i
t
h
monitoring, and varying if necessary, many parameters. During flight, an insect must b
e
able to control the fre
q
uenc
y
of win
g
beat, the amount of lift and thrust develo
p

ed, and
t
h
e
di
rect
i
on (sta
bili
t
y
)o
f fligh
t. It must a
l
so
h
ave contro
l
mec
h
an
i
sms
f
or t
h
e
i
n

i
t
i
at
i
on
an
d
term
i
nat
i
on o
f fligh
t. T
h
e sense or
g
ans t
h
at
p
rov
id
et
h
e centra
l
nervous s
y

stem w
i
t
h
i
n
f
ormat
i
on on w
h
at c
h
anges are occurr
i
ng
i
nre
l
at
i
on to
fli
g
h
t are t
h
e compoun
d
eyes an

d
p
roprioceptors strategically distributed over the body, especially on the head, wings, and
l
e
g
s. Res
p
onses to stimuli received b
y
these or
g
ans are usuall
y
mediated via chan
g
es in th
e
nature o
f
t
h
ew
i
n
g
movements (
p
art
i

cu
l
ar
ly
t
h
e
d
e
g
ree o
f
tw
i
st
i
n
g
an
d
w
i
n
g
-
b
eat
f
re
q

uenc
y
).
W
i
n
g
-
b
eat
f
re
q
uenc
y
var
i
es w
id
e
ly
amon
g diff
erent
i
nsects as
h
as
b
een note

d
a
l
rea
dy
i
nt
h
e
i
ntro
d
uct
i
on to t
hi
s
di
scuss
i
on o
ffli
g
h
t. In
fli
ers w
h
ose w
i

ng-
b
eat
f
requency
i
s
l
ow
(e.g., the desert locust, about 1
5
–20 beats/sec) neurogenic (synchronous) control occurs.
T
hat is, there is a 1:1 ratio between win
g
-beat fre
q
uenc
y
and nervous in
p
ut. In such fibers
,
t
h
ere
f
ore, w
i
n

g
-
b
eat
f
re
q
uenc
y
can
b
evar
i
e
dby
a
l
ter
i
n
g
t
h
e rate at w
hi
c
h
nerve
i
m

p
u
l
ses
arr
i
ve at t
h
e musc
l
es. However, t
h
ere are
li
m
i
ts to t
hi
s arran
g
ement (max
i
mum
f
re
q
uenc
y
a
b

out 100
b
eats
/
sec)
b
ecause o
f
t
h
ere
f
ractory per
i
o
d
requ
i
re
d
to return t
h
e musc
l
eto
i
ts
resting state after each contraction. Insects whose wing-beat frequency is high, for example
,
the bee (190 beats/sec) and midg

e
Fo
r
cipomyia
r
r
(up to 1000 beats/sec), use a myogenic
(as
y
nchronous) s
y
stem where the fre
q
uenc
y
of muscle contraction is much
g
reater than tha
t
of nervous in
p
ut (ratios of between 5:1 and 40:1). Such a s
y
stem is
p
ossible onl
y
wher
e
t

h
ere are antagon
i
st
i
c musc
l
es t
h
at contract regu
l
ar
l
yan
d
a
l
ternate
l
y. T
h
ese musc
l
es
h
ave
the property of contracting autonomously when the tension developed in them as a result
of stretching reaches a critical value. In the case of the flight musculature, the alternatin
g
c

ontractions are, in a sense, self-
p
er
p
etuatin
g
, thou
g
h their initiation and cessation are under
nervous contro
l
.T
h
ere
i
sa
l
so ev
id
ence to su
gg
est t
h
at c
h
an
g
es
i
nt

h
e
f
re
q
uenc
y
at w
hi
c
h
nerve
i
m
p
u
l
ses arr
i
ve at t
h
ese musc
l
es can mo
dify
t
h
e
i
r

f
re
q
uenc
y
o
f
contract
i
on. However
,
a
s contract
i
ons are tens
i
on-
d
epen
d
ent, t
h
e
i
r
f
requency can a
l
so
b

ea
l
tere
db
ymo
dif
y
i
ng t
he
elastic resistance in the exoskeleton. In Diptera, for example, this is achieved by contraction
or relaxation of the
p
leurosternal muscles, which serves to move the
p
leural win
gp
rocess
cl
oser to or
f
art
h
er
f
rom t
h
e ter
g
a

lhi
n
g
e(F
ig
ure 14.8)
.
A
s note
d
ear
li
er,
d
ur
i
n
g
a
b
eataw
i
n
gd
oes not ma
k
es
i
m
pl

eu
p
an
dd
own movements
,
b
u
t
rat
h
er tw
i
sts a
b
out t
h
e vert
i
ca
l
ax
i
ssot
h
at
i
ts t
i
p

d
escr
ib
es an e
lli
pse (
S
c
h
istocerca
)
or figure eight (
Ap
is, Musca
(
(
)
.
The size and direction of the twisting force (torque), which
effectively measure the lift and thrust developed, are monitored by campaniform sensilla
a
tt
h
e
b
ase o
f
eac
h
w

i
n
g
(
h
a
l
teres
i
nD
ip
tera—see
b
e
l
ow). In
p
ut
f
rom t
h
e sens
ill
a
i
n
i
t
i
ates

re
fl
ex exc
i
tat
i
on o
f
t
h
e
b
asa
l
ar an
d
su
b
a
l
ar musc
l
es, w
hi
c
h
re
g
u
l

ate t
h
e extent to w
hi
c
h
t
he
w
i
ng tw
i
sts. T
hi
s mec
h
an
i
sm
i
s
k
nown as t
h
e
lif
t contro
l
re
fl

ex
.
S
chistocerc
a
e
mp
l
oys suc
h
a
reflex to control the value of lift and, in flight, holds its body at a fairly steady angle to the
horizontal. Other insects vary the angle at which the body is held in flight in order to alter
the lift and thrust com
p
onents.
*
F
ictive flight: The locust preparation is actually a wingless, legless insect pinned in a dish! It is stimulated to
“
fly
”
by g
ent
ly bl
ow
i
n
g
on t

h
e
f
rons.
461
M
U
S
CLE
S
AND
LOCOMOTIO
N
FIGURE 14.15
.
Di
agram s
h
ow
i
ng axes a
b
out w
hi
c
h
a
fl
y
i

ng
i
nsect may rotate.
The direction (and correlated with it, the stability) of flight necessitates the monitorin
g
and re
g
ulation of movement in three dimensions (Fi
g
ure 14.15): movement of the bod
y
i
n
th
e
h
or
i
zonta
l
, transverse ax
i
s
i
s
pi
tc
hi
n
g

; rotat
i
on a
b
out t
h
e vert
i
ca
l
ax
i
s
i
s
y
aw
i
n
g
;an
d
r
otat
i
on aroun
d
t
h
e

l
ong
i
tu
di
na
l
ax
i
s
i
sro
lli
ng
.
I
n
S
c
h
istocerca
g
re
g
aria
p
itching is controlled via the lift control reflex outlined above
.
I
n this species the fore and hind wings beat in antiphase. The hind wings are not capable

,
h
owever, of twistin
g
and, therefore, the value of lift
g
enerated b
y
them is a function of th
e
b
o
dy
an
gl
e(t
h
ean
gl
eatw
hi
c
h
t
h
e
b
o
dy i
s

h
e
ld
re
l
at
i
ve to t
h
e
di
rect
i
on o
f
a
i
r
fl
ow). An
y
c
h
an
g
e
i
n
b
o

dy
an
gl
e, a
l
ter
i
n
g
t
h
e
lif
t
g
enerate
dby
t
h
e
hi
n
d
w
i
n
g
s,
i
s com

p
ensate
df
or
by
appropriate twisting of the fore wings so that the total lift produced remains constant. Other
i
nsects control pitching by varying the amplitude of the wing beat, the stroke plane (the
an
g
le at which the win
g
s move relative to the bod
y
), or the stroke rh
y
thm (b
y
dela
y
in
g
o
r
e
n
h
anc
i
n

g
t
h
e moment at w
hi
c
hp
ronat
i
on o
f
t
h
ew
i
n
g
s occurs
d
ur
i
n
g
t
h
e
b
eat).
T
h

e contro
l
o
fy
aw
i
n
gi
nvo
l
ves sensor
yi
n
p
ut
f
rom
b
ot
h
t
h
e com
p
oun
d
e
y
es an
d

m
ec
h
anoreceptors. As an
i
nsect turns, t
h
ev
i
sua
l
fie
ld
w
ill
rotate. A
l
so,
i
n some
i
nsects
such as Sc
h
istocerc
a
,
this movement results in unequal stimulation of mechanosensory
h
airs at each side of the head. Yawin

g
ma
y
be corrected b
y
var
y
in
g
the an
g
le of attack, th
e
am
pli
tu
d
e, or t
h
e
f
re
q
uenc
y
o
fb
eat,
b
etween t

h
ew
i
n
g
soneac
h
s
id
eo
f
t
h
e
b
o
dy
.A
ll
o
f
th
ese var
i
a
bl
es w
ill
a
l

ter t
h
et
h
rust
g
enerate
d.
Ro
lli
ng
i
s
l
arge
l
y mon
i
tore
d
as a resu
l
to
f
certa
i
nv
i
sua
l

st
i
mu
li
. Common
l
y, t
h
e
h
ea
d
i
s rotated so that the dorsal ommatidia receive maximal illumination, the source of whic
h
i
s normally directly overhead. Early and late in the day, however, when the latter is no
t
t
he case, use is also made of the marked contrast in li
g
ht intensit
y
between the earth and