I
V
E
colo
gy
22
The Abiotic Environment
1
. Intr
oduc
t
ion
The development and reproduction of insects are greatly influenced by a variety of abioti
c
factors. These factors ma
y
exert their effects on insects either directl
y
or indirectl
y
(throu
g
h
th
e
i
re
ff
ects on ot
h
er or

g
an
i
sms) an
di
nt
h
es
h
ort- or
l
on
g
-term. L
igh
t,
f
or exam
pl
e, ma
y
exer
t
an
i
mme
di
ate e
ff
ect on t

h
eor
i
entat
i
on o
f
an
i
nsect as
i
t searc
h
es
f
or
f
oo
d
,an
d
ma
yi
n
d
uc
e
c
h
anges

i
nan
i
nsect’s p
h
ys
i
o
l
ogy
i
n ant
i
c
i
pat
i
on o
f
a
d
verse con
di
t
i
ons some mont
h
s
i
nt

he
future. Another abiotic factor to which insects are now routinely subjected (deliberately or
otherwise) are
p
esticides. A
p
art from the obvious effect of lethal doses of such chemicals,
p
est
i
c
id
es ma
yh
ave more su
b
t
l
e,
i
n
di
rect e
ff
ects on t
h
e
di
str
ib

ut
i
on an
d
a
b
un
d
ance o
f
s
p
ec
i
es,
f
or exam
pl
e, a
l
terat
i
on o
fp
re
d
ator-
p
re
y

rat
i
os an
d
,
i
nsu
bl
et
h
a
ld
oses, c
h
an
g
es
i
n
f
ecun
di
ty or rates o
fd
eve
l
opment.
Under natural conditions organisms are subject to a combination of environmenta
l
factors, both biotic and abiotic, and it is this combination that ultimatel

y
determines the
di
str
ib
ut
i
on an
d
a
b
un
d
ance o
f
as
p
ec
i
es. Fre
q
uent
ly
,t
h
ee
ff
ect o
f
one

f
actor mo
di
fies t
he
n
orma
l
res
p
onse o
f
an or
g
an
i
sm to anot
h
er
f
actor. For exam
pl
e,
ligh
t,
by i
n
d
uc
i

n
gdi
a
p
aus
e
(
Sect
i
on 3.2.3), may ma
k
ean
i
nsect unrespons
i
ve to (una
ff
ecte
db
y) temperature
fl
uctua
-
t
ions. As a result, an insect is not harmed by abnormally low temperatures, but nor does
i
t become active in temporary periods of warmer weather that may occur in the middle of
wi
nter
.

2. Tem
p
erature
2
.1. Effect on Develo
p
ment Rate
The body temperature of insects, as poikilothermic animals, normally follows closely
t
he tem
p
erature of the surroundin
g
s. Within limits, therefore, metabolic rate is
p
ro
p
ortional
t
oam
bi
ent tem
p
erature. Conse
q
uent
ly
,t
h
e rate o

fd
eve
l
o
p
ment
i
s
i
nverse
ly p
ro
p
ort
i
ona
l
t
o tem
p
erature (F
ig
ure 22.1). Outs
id
et
h
ese tem
p
erature
li

m
i
ts t
h
e rate o
fd
eve
l
o
p
ment
n
o longer bears an inversely linear relationship to temperature, because of the deleteriou
s
e
ffects of extreme temperatures on the enzymes that regulate metabolism, and eventually
t
em
p
eratures are reached (the so-called u
pp
er and lower lethal limits) where death occurs.
65
5
656
CHAPTER
22
F
I
GU

RE 22.1
.
R
elationshi
p
between tem
p
erature and rate of develo
p
ment in e
gg
so
f
D
rosophila melano
g
aster
(Diptera). The two curves represent different ways of expressing this relationship, each being the reciprocal of the
o
t
h
er.
[
A
f
ter H. G. An
d
rewart
h
a, 19

6
1
,
Intro
d
uction to t
h
e Stu
d
y of Anima
l
Popu
l
ation
s
,
Un
i
vers
i
t
y
o
f
C
hi
ca
go
Press. B
yp

ermission of the author.]
W
i
t
hi
nt
h
e range o
fli
near
i
ty t
h
e pro
d
uct o
f
temperature mu
l
t
i
p
li
e
db
yt
i
me requ
i
re

df
o
r
development will be constant. This constant, known as the thermal constant or heat budget,
is commonly measured in units of degree-days. This relationship will hold even when the
tem
p
erature fluctuates,
p
rovided that the fluctuations do not exceed the ran
g
e of linearit
y
.
Th
e tem
p
erature
li
m
i
ts outs
id
ew
hi
c
hd
eve
l
o

p
ment ceases an
d
t
h
e rate o
fd
eve
l
o
p
ment at
ag
iv
e
n temperature vary among spec
i
es, two seem
i
ng
l
yo
b
v
i
ous po
i
nts t
h
at were apparent

l
y
o
verlooked in some early attempts at biological control of insect pests. A predator that, o
n
the basis of laboratory tests and short-term field trials, had good control potential was found
to exert little or no control of the
p
est under natural conditions. Further stud
y
showed thi
s
to
b
ere
l
ate
d
to t
h
e
diff
er
i
n
g
e
ff
ects o
f

tem
p
erature on
d
eve
l
o
p
ment,
h
atc
hi
n
g
,an
d
act
i
v
i
t
y
b
etween t
h
e
p
est an
di
ts

p
re
d
ator
.
A
b
roa
d
corre
l
at
i
on ex
i
sts
b
etween t
h
e temperature
li
m
i
ts
f
or
d
eve
l
opment an

d
t
h
e
habitat occupied by members of a species. For example, many Arctic insects that overwinter
in the e
gg
sta
g
e com
p
lete their entire develo
p
ment (embr
y
onic
+
p
ostembr
y
onic) in th
e
tem
p
erature ran
g
e
0
◦
C

to
4
◦
C
,w
h
ereas
i
nt
h
e Austra
li
an
pl
a
g
ue
g
rass
h
o
pp
er,
A
ustroicete
s
c
ruc
i
ata

,d
ev
e
l
opment ceases
b
e
l
ow 1
6
◦
C
.T
hi
s means t
h
at t
h
e
di
str
ib
ut
i
on o
f
a spec
i
es w
ill

be limited by the range of temperature experienced in different geographic regions, as well
as by other factors. However, the distribution of a species may be significantly greater than
that antici
p
ated on the basis of tem
p
erature data for the followin
g
reasons: (1) tem
p
eratur
e
a
d
a
p
tat
i
on ma
y
occur, t
h
at
i
s,
g
enet
i
ca
lly diff

erent stra
i
ns ma
y
evo
l
ve, eac
h
ca
p
a
bl
eo
f
s
urv
i
v
i
n
g
w
i
t
hi
na
diff
erent tem
p
erature ran

g
e; (2) t
h
e tem
p
erature
li
m
i
ts o
fd
eve
l
o
p
ment
may
diff
er among
d
eve
l
opmenta
l
stages [t
hi
sa
l
so serves as an
i

mportant
d
eve
l
opmenta
l
s
ynchronizer in some species (Section 2.3)]; and (3) the insect may have mechanisms for
s
urvivin
g
extreme tem
p
eratures (Section 2.4).
6
5
7
THE
A
BI
O
TI
C
ENVIR
O
NMEN
T
Because of the ameliorating effects of the water surrounding them, aquatic insect
s
are not normall

y
ex
p
osed to the tem
p
erature extremes ex
p
erienced b
y
terrestrial s
p
ecies
.
F
urt
h
er,
b
ecause
i
ce
i
sa
g
oo
di
nsu
l
ator,
d

eve
l
o
p
ment ma
y
cont
i
nue t
h
rou
gh
t
h
ew
i
nter
in
some a
q
uat
i
cs
p
ec
i
es
i
n tem
p

erate c
li
mates, t
h
ou
gh
a
i
r tem
p
eratures ren
d
er
d
eve
l
o
p
ment
o
f terrestrial species impossible. Indeed, through evolution there has been a trend in som
e
i
nsects (e.g., species of Ephemeroptera and Plecoptera) to restrict their period of growth
t
o the winter,
p
assin
g
the summer as e

gg
sindia
p
ause. Such s
p
ecies, whose develo
p
mental
th
res
h
o
ld i
s usua
lly
on
ly
s
ligh
t
ly
a
b
ove 0
◦
C, a
pp
ear to
g
a

i
nat
l
east two a
d
vanta
g
es
f
ro
m
thi
s arran
g
ement. F
i
rst, t
h
rou
gh
t
h
ew
i
nter t
h
ere
i
sana
b

un
d
ance o
ff
oo
di
nt
h
e
f
orm o
f
r
ott
i
ng vegetat
i
on, yet re
l
at
i
ve
l
y
li
tt
l
e compet
i
t

i
on
f
or
i
t. Secon
d
,t
h
ey are re
l
at
i
ve
l
ysa
f
e
from predators (fish) which are sluggish and feed only occasionally at these temperatures
(
H
y
nes, 1970b). Such a life c
y
cle ma
y
also allow some s
p
ecies to inhabit tem
p

orar
y
or still
b
o
di
es o
f
water t
h
at
d
r
y
u
p
or
b
ecome anaero
bi
c
d
ur
i
n
g
summer.
2
.2. E
ff

ect on Act
i
v
i
ty and D
i
spersa
l
Through its effect on metabolic rate, temperature clearly will affect the activity o
f
i
nsects. Man
y
of the
g
eneralizations made above with re
g
ard to the influence of tem
p
eratur
e
o
n
d
eve
l
o
p
ment
h

ave t
h
e
i
r
p
ara
ll
e
li
nre
l
at
i
on toact
i
v
i
t
y
.T
h
us, t
h
ere
i
s aran
g
eo
f

tem
p
erature
wi
t
hi
nw
hi
c
h
act
i
v
i
ty
i
s norma
l
,t
h
oug
h
t
hi
s range may vary among
diff
erent stra
i
ns o
f

t
h
e
same species. The temperature range for activity is correlated with a species’ habitat; for
e
xample, in the Arctic, chironomid larvae are normally active in water at 0
◦
C, and adult
s
c
an fl
y
at tem
p
eratures as low as 3.5
◦
C
(
Downes, 19
6
4
).
B
y
a
ff
ect
i
n
g

an
i
nsect’s a
bili
t
y
to
fly
tem
p
erature ma
yh
ave a mar
k
e
d
e
ff
ect on a s
p
ec
i
es’
di
spersa
l
an
d
,t
h

ere
f
ore,
i
ts
di
str
ib
ut
i
on. Furt
h
er,
b
ecause
fli
g
h
t
i
so
f
suc
hi
mportance
i
n
f
oo
d

and/or mate location and, ultimately, reproduction, temperature is of great consequence in
d
etermining the abundance of species. Insects use various means of raising their bod
y
t
em
p
erature to that at which fli
g
ht is
p
ossible even when the ambient tem
p
erature is low
.
Fo
r
e
x
am
pl
e, t
h
e
y
ma
yb
e
d
ar

kly
co
l
ore
d
so as to a
b
sor
b
so
l
ar ra
di
at
i
on, or t
h
e
y
ma
yb
as
k
o
n
d
ar
k
sur
f

aces, aga
i
nus
i
ng t
h
e sun’s
h
eat. Some mot
h
san
db
um
bl
e
b
ees
b
eat t
h
e
i
rw
i
ng
s
w
hile at rest and simultaneously reduce hemolymph circulation in order to increase the
t
emperature of the thorax (Chapter 17, Section 3.1). A dense coat of hairs or scales covers

t
he bod
y
of some insects, which, b
y
its insulatin
g
effect, will retard loss of heat
g
enerate
d
o
ra
b
sor
b
e
d.
I
n extreme
l
yco
ld
c
li
mates t
h
ese p
h
ys

i
o
l
og
i
ca
l
,
b
e
h
av
i
ora
l
, or structura
lf
eatures ma
y
n
o longer be sufficient to enable flight to occur, especially in a larger-bodied, egg-carrying
female. Thus, different temperature-adaptation strategies are employed, some of which
are exem
p
lified es
p
eciall
y
well b
y

Arctic black flies (Simuliidae: Di
p
tera). T
yp
ical adult
t
em
p
erate-c
li
mate s
p
ec
i
es are act
i
ve
i
nsects t
h
at mate
i
n
fligh
t, an
df
ema
l
es ma
yfly

cons
id
-
e
ra
bl
e
di
stances
i
n searc
h
o
f
a
bl
oo
d
mea
l
necessar
yf
or e
gg
maturat
i
on. In contrast,
f
ema
l

es
o
f Arctic species seldom fly. Their mouthparts are reduced and eggs mature from nutrients
acquired during larval life. Mating occurs on the ground as a result of chance encounters
close to the site of adult emer
g
ence. In two s
p
ecies
p
artheno
g
enesis has evolved, thereb
y
ov
e
rcom
i
n
g
t
h
e
dif
ficu
l
t
y
o
fb

e
i
n
gf
oun
dby
ama
l
e (Downes, 19
6
4).
Tem
p
erature c
h
an
g
e, t
h
rou
gh i
ts e
ff
ect on t
h
eso
l
u
bili
t

y
o
f
ox
yg
en
i
n water, ma
y
m
ar
k
e
dl
ymo
dif
yt
h
e act
i
v
i
ty an
d
,u
l
t
i
mate
l

y, t
h
e
di
str
ib
ut
i
on an
d
surv
i
va
l
o
f
aquat
i
c
i
n-
sects. Members of many aquatic species are restricted to habitats whose oxygen conten
t
r
emains relativel
y
hi
g
h throu
g

hout the
y
ear. Such habitats include rivers and streams that are
658
CHAPTER
22
normally well oxygenated because of their turbulent flow and lower summer temperature
,
and hi
g
h-altitude or -latitude
p
onds and lakes, which
g
enerall
y
remain cool throu
g
h the
summer. A
l
ternat
i
ve
ly
, as note
di
n Sect
i
on 2.1, t

h
e
lif
ec
y
c
l
eo
f
some s
p
ec
i
es
i
s suc
h
t
h
a
t
t
h
e warmer (ox
yg
en-
d
efic
i
ent) con

di
t
i
ons are s
p
ent
i
n a res
i
stant,
di
a
p
aus
i
n
g
,e
gg
sta
g
e.
2.3. Temperature-
S
ynchronized Development and Emer
g
enc
e
Man
y

s
p
ec
i
es o
fi
nsects
h
ave
highly
s
y
nc
h
ron
i
ze
dl
arva
ld
eve
l
o
p
ment (a
ll l
arvae ar
e
more or
l

ess att
h
e same
d
eve
l
o
p
menta
l
sta
g
e) an
d/
or s
y
nc
h
ron
i
ze
d
ec
l
os
i
on, es
p
ec
i

a
lly
t
h
ose
t
h
at
li
ve
i
n
h
a
bi
tats w
h
ere t
h
ec
li
mate
i
ssu
i
ta
bl
e
f
or growt

h
an
d
repro
d
uct
i
on
f
or a
li
m
i
te
d
p
eriod each year. Synchronized eclosion increases the chances of finding a mate. It may also
increase the
p
robabilit
y
of findin
g
suitable food or ovi
p
osition sites, or of esca
p
in
gp
otentia

l
p
re
d
ators. S
y
nc
h
ron
i
ze
dl
arva
ld
eve
l
o
p
ment a
l
so ma
yb
ere
l
ate
d
to t
h
eava
il

a
bili
t
y
o
ff
oo
d
,
an
di
n some s
i
tuat
i
ons
i
tma
yb
e necessar
yi
nor
d
er to avo
id i
nters
p
ec
i
fic com

p
et
i
t
i
on
f
or t
h
e
same resource. For certa
i
n carn
i
vorous spec
i
es, suc
h
as O
d
onata, sync
h
ron
i
ze
dd
eve
l
opment
may help reduce the incidence of cannibalism among larvae

.
P
erhaps not surprisingly in view of its effects on rate of development and activity,
tem
p
erature
i
san
i
m
p
ortant s
y
nc
h
ron
i
z
i
n
gf
actor
i
nt
h
e
lif
eo
fi
nsects. Its

i
m
p
ortance ma
y
b
e
ill
ustrate
dby
re
f
erence to t
h
e
lif
e
hi
stor
y
o
f
Coenagrion angu
l
atum,w
hi
c
h
,a
l

on
g
w
i
t
h
severa
l
ot
h
er spec
i
es o
fd
amse
lfli
es (O
d
onata: Zygoptera),
i
s
f
oun
di
n or aroun
d
s
h
a
ll

o
w
p
onds on the Canadian prairies (Sawchyn and Gillott, 197
5
). For these insects the seaso
n
f
or growth and reproduction lasts from about mid-May to mid-October. For the remaining
7
months of the
y
ear C
.
angulatum
e
xists as more or less mature larvae
,
which
,
between abou
t
Novem
b
er an
d
A
p
r
il

, are encase
di
n
i
ce as t
h
e
p
on
d
s
f
reeze to t
h
e
b
ottom. (T
h
e
l
arvae t
h
em-
se
l
ves
d
o not
f
reeze, as t

h
e
i
ce temperature se
ld
om
f
a
ll
s more t
h
an a
f
ew
d
egrees Ce
l
s
i
u
s
below zero as a result of snow cover.
)
In C.
a
n
g
u
l
atu

m
both larval development and eclosio
n
are synchronized by temperature. Synchronized development is achieved (1) by means of
different tem
p
erature thresholds for develo
p
ment in different instars, that is,
y
oun
g
er larvae
c
an cont
i
nue to
g
row
i
nt
h
e
f
a
ll
a
f
ter t
h

e
g
rowt
h
o
f
o
ld
er
l
arvae
h
as
b
een arreste
dbyd
ecreas-
i
ng water temperatures, an
d
(2)
b
yap
h
otoper
i
o
di
ca
ll

y
i
n
d
uce
ddi
apause. T
h
us, samp
l
e
s
c
ollected in mid-September include larvae of the last seven instars, whereas those from earl
y
O
ctober are composed almost entirely of larvae of the last three instars. Conversely, after the
ice melts the followin
g
A
p
ril,
y
oun
g
er larvae can continue their develo
p
ment earlier tha
n
t

h
e
i
r more mature re
l
at
i
ves, so t
h
at
by
m
id
-Ma
y
more t
h
an 90% o
f
t
h
e
l
arvae are
i
nt
h
e fina
l
i

nstar. A
f
ter t
h
e
i
rre
l
ease
f
rom t
h
e
i
ce
l
arvae m
ig
rate
i
nto s
h
a
ll
ow water at t
h
e
p
on
d

mar
gin
wh
ose temperature para
ll
e
l
st
h
at o
f
t
h
ea
i
r. Emergence occurs w
h
en t
h
ea
i
r temperature
is
2
0
◦
C
to
21
◦

C (and the water temperature is about 1
2
◦
C
). It begins normally during the las
t
week of Ma
y
and reaches a
p
eak within 10 da
y
s. Emer
g
ence of
C
.
angulatum f
o
ll
ows t
h
at
o
f
var
i
ous c
hi
ronom

id
san
d
c
h
ao
b
or
id
s(D
ip
tera), w
hi
c
hf
orm t
h
ema
i
n
f
oo
d
o
f
t
h
ea
d
u

l
t
d
amse
lfli
es
d
ur
i
ng t
h
e per
i
o
d
o
f
sexua
l
maturat
i
on. T
h
e
d
eve
l
opment an
d
emergence o

f
other damselfly species that inhabit the same pond are also highly synchronized but occur
a
t different times of the growing season. This enables the species to occupy the same pond
a
nd make use of the same resources,
y
et avoid inters
p
ecific com
p
etition. This is discussed
f
urt
h
er
i
nC
h
a
p
ter 23 (Sect
i
on 3.2.1).
Th
ou
gh
un
p
re

di
cta
bl
eona
d
a
y
-to-
d
a
yb
as
i
s, tem
p
erature
d
oes
h
aveare
g
u
l
ar seasona
l
p
attern t
h
at contro
l

st
h
e onset an
d
term
i
nat
i
on o
fdi
apause
i
n some spec
i
es. Temperature
i
s
the primary diapause-inducing stimulus for some subterranean species [e.g., some ground
beetles (Carabidae)], wood- and bark-inhabitin
g
s
p
ecies, and
p
ests of stored
p
roducts that
6
5
9

THE
A
BI
O
TI
C
ENVIRONMEN
T
live in darkness. It also is the major cue for diapause induction in some insects living
n
ear the e
q
uator where chan
g
es in
p
hoto
p
eriod are too small to act as si
g
nals of seasona
l
c
h
an
g
e(Tau
b
e
r

et al.
, 198
6
; Den
li
n
g
er, 198
6
). Tem
p
erature can a
l
so exert a stron
gi
n
fl
u-
e
nce on
di
a
p
ause an
d
ot
h
er
ph
oto

p
er
i
o
di
ca
lly
contro
ll
e
dph
enomena, as
i
s
di
scusse
db
e
l
o
w
(
Section 3.2)
.
2
.4.
S
urvival at Extreme Tem
p
eratures

I
n man
y
tro
pi
ca
l
areas c
li
mat
i
c con
di
t
i
ons are su
i
ta
bl
e
f
or
y
ear-roun
dd
eve
l
o
p
ment an

d
r
epro
d
uct
i
on
i
n
i
nsects. In ot
h
er areas o
f
t
h
ewor
ld
,t
h
e year
i
s
di
v
i
s
ibl
e
i

nto
di
st
i
nct seasons
,
i
n some of which growth and/or reproduction is not possible. One reason for this arrest of
g
rowth and/or re
p
roduction ma
y
be the extreme tem
p
eratures that occur at this time and ar
e
p
otent
i
a
lly l
et
h
a
l
to an
i
nsect. In man
yi

nstances s
h
orta
g
eo
ff
oo
d
wou
ld
a
l
so occur un
d
er
th
ese con
di
t
i
ons
.
To
av
o
id
t
h
e
d

etr
i
menta
l
e
ff
ects o
f
per
i
o
d
so
f
mo
d
erate
l
y
l
ow (
d
own to
f
reez
i
ng) or
hi
g
h

t
emperature, and to ensure that development and reproduction occur at favorable times of the
year, insects use an array of behavioral and physiological mechanisms (Danks, 2001, 2002)
.
Fi
rst, t
h
e
lif
e
hi
stor
y
o
f
man
y
s
p
ec
i
es
i
s arran
g
e
d
so t
h
at t

h
e
p
er
i
o
d
o
f
a
d
verse tem
p
eratur
e
i
s
p
asse
d
as t
h
e
i
mmo
bil
e, non-
f
ee
di

n
g
e
gg
or
p
u
p
a. Secon
d
,
p
r
i
or to t
h
ea
d
vent o
f
a
d
verse
con
di
t
i
ons [an
di
ts

h
ou
ld b
e rea
li
ze
d
t
h
at t
h
eto
k
en st
i
mu
l
us t
h
at tr
i
ggers t
hi
s
b
e
h
av
i
or

i
s not,
i
n itself, adverse (see Section 3.2)], an insect may actively seek out a habitat in which the
full effect of the detrimental temperature is not felt. For example, it may burrow or oviposi
t
i
n soil, litter, or
p
lant tissue, which acts as an insulator. Third, it ma
y
enter dia
p
ause wher
e
i
ts
phy
s
i
o
l
o
gi
ca
l
s
y
stems are
l

ar
g
e
ly i
nact
i
ve an
d
res
i
stant to extremes o
f
tem
p
erature
.
2
.4.1.
C
old-Hard
i
ness
C
o
ld
-
h
ar
di
ness re

f
ers to an
i
nsect’s a
bili
t
y
to a
d
a
p
ttoan
d
surv
i
ve
l
ow tem
p
eratures
.
Some
i
nsects are “c
hill
-
i
nto
l
erant,” t

h
at
i
s, su
ff
er
l
et
h
a
li
n
j
ur
y
even at tem
p
eratures a
b
ove
0
◦
C. Ot
h
ers are “c
hill
-to
l
erant,” t
h

oug
h
a per
i
o
d
o
f
gra
d
ua
l
temperature acc
li
mat
i
on (
h
ar
d
-
e
ning) may be required for tolerance to develop (Bale, 1993, 1996; Sømme, 1999). For
i
nsects in environments that experience temperatures below 0
◦
C, an additional problem
p
resents itself, namel
y

, how to avoid bein
g
dama
g
ed b
y
freezin
g
of the bod
y
cells. The
f
ormat
i
on o
fi
ce cr
y
sta
l
sw
i
t
hi
nce
ll
s causes
i
rrevers
ibl

e
d
ama
g
etoan
df
re
q
uent
ly d
eat
h
o
f
an organ
i
sm (1)
b
yp
h
ys
i
ca
ldi
srupt
i
on o
f
t
h

e protop
l
asm an
d
(2)
b
y
d
e
h
y
d
rat
i
on, re
d
uct
i
o
n
o
f the liquid water content that is essential for normal enzyme activity. Insects that sur
-
vive freezing temperatures are described as either freezing-susceptible or freezing-tolerant.
F
reezin
g
-susce
p
tible s

p
ecies are those whose bod
y
fluids have a lower freezin
gp
oint and
m
a
y
un
d
er
g
osu
p
ercoo
li
n
g
. Freez
i
n
g
-to
l
erant
(
=
f
reez

i
n
g
-res
i
stan
t
=
f
rost-res
i
stant) s
p
ec
i
es
are ones w
h
ose extrace
ll
u
l
ar
b
o
dy fl
u
id
s can
f

reeze w
i
t
h
out
d
ama
g
etot
h
e
i
nsect
.
I
n
b
ot
h
groups, two or t
h
ree types o
f
cryoprotectants (su
b
stances t
h
at protect aga
i
ns

t
freezing) are produced. Cryoprotectants identified to date fall into three categories: (1) ice-
nucleatin
g
a
g
ents (
p
roteins),
p
roduced onl
y
in freezin
g
-tolerant s
p
ecies; (2) low-molecular-
w
e
igh
t
p
o
lyhyd
rox
yl
su
b
stances suc
h

as
p
ro
li
ne,
gly
cero
l
, sor
bi
to
l
, mann
i
to
l
,t
h
re
i
to
l
,su
-
c
rose an
d
tre
h
a

l
ose; an
d
(3) t
h
erma
l
-
hy
steres
i
sorant
if
reeze
p
rote
i
ns (Duman an
d
Horwat
h,
1983; Lee, 1991; Ba
l
e, 2002). Typ
i
ca
ll
y,
i
nsects pro

d
uce two or more po
l
y
h
y
d
roxy
l
s. T
his
m
ay be because they are toxic at higher concentrations, an effect that can be avoided by the
use of a multicomponent system
.
660
CHAPTER
22
To
appreciate the mode of action of these cryoprotectants, it is necessary to understand
the
p
rocess of freezin
g
. When water is cooled the s
p
eed at which individual molecules
move
d
ecreases, an

d
t
h
emo
l
ecu
l
es a
gg
re
g
ate. As coo
li
n
g
cont
i
nues t
h
ere
i
san
i
ncrease
d
p
ro
b
a
bili

t
y
t
h
at a num
b
er o
f
a
gg
re
g
ate
d
mo
l
ecu
l
es w
ill b
ecome so or
i
ente
d
w
i
t
h
res
p

ect t
o
each other as to form a minute rigid latticework, that is, a crystal. Immediately this crystal
(nucleator) is formed the rest of the water freezes rapidly as additional molecules bind t
o
the solid frame now available to them. Freezin
g
ofali
q
uid does not alwa
y
sde
p
end on
t
h
e
f
ormat
i
on o
f
a nuc
l
eator,
b
ut can
b
e
i

n
d
uce
dbyf
ore
ig
n nuc
l
eat
i
n
g
a
g
ents suc
h
as
d
ust
p
art
i
c
l
es or,
i
nt
h
e present context, part
i

c
l
es o
ff
oo
di
nt
h
e gut or a roug
h
sur
f
ace suc
h
as
that of the cuticle.
In freezing-susceptible species cold-hardiness is attained in a two-step process (Bale,
2
002). In the first ste
p
behavioral and
p
h
y
siolo
g
ical activities occur that collectivel
y
re
-

d
uce t
h
e
i
nsect’s c
h
ance o
ff
reez
i
n
g
.T
h
ese ma
yi
nc
l
u
d
eem
p
t
yi
n
g
t
h
e

g
ut o
ff
oo
d
an
d
ov
erw
i
nter
i
n
g
as a non-
f
ee
di
n
gp
u
p
a,
hib
ernat
i
n
gi
n
d

r
yl
ocat
i
ons,
b
u
ildi
n
g
structures t
h
at
p
revent contact w
i
t
h
mo
i
sture, re
d
uc
i
ng
b
o
d
y water content, an
di

ncreas
i
ng
f
at content
.
C
ollectively, these processes may lower the supercooling point to –20
◦
C
. In the second step
p
ol
y
h
y
drox
y
ls and antifreeze
p
roteins are
p
roduced. These molecules not onl
y
increase th
e
c
oncentrat
i
on o

f
so
l
utes
i
nt
h
e
b
o
dy fl
u
id
so t
h
at t
h
e
f
reez
i
n
gp
o
i
nt
i
s
d
e

p
resse
d
,
b
ut
by
t
h
e
i
rc
h
em
i
ca
l
nature t
h
e
y
cons
id
era
bly i
m
p
rove t
h
e

i
nsect’s su
p
ercoo
li
n
g
ca
p
ac
i
t
y
;t
h
a
t
i
s, t
h
e
b
o
d
y
fl
u
id
s rema
i

n
li
qu
id
at temperatures muc
hb
e
l
ow t
h
e
i
r norma
lf
reez
i
ng po
i
nt.
B
ecause of their hydroxyl groups, the cryoprotectants are capable of extensive hydroge
n
bondin
g
with the water within the bod
y
. The bindin
g
of the water has two im
p

ortant effect
s
w
i
t
h
res
p
ect to su
p
ercoo
li
n
g
.F
i
rst,
i
t
g
reat
ly
re
d
uces t
h
ea
bili
t
y

o
f
t
h
e water mo
l
ecu
l
es to
agg
re
g
ate an
df
orm a nuc
l
eat
i
n
g
cr
y
sta
l
,an
d
secon
d
,even
if

an
i
ce nuc
l
eus
i
s
f
orme
d
,t
he
rate at w
hi
c
hf
reez
i
ng sprea
d
st
h
roug
h
t
h
e
b
o
d

y
i
s great
l
y retar
d
e
db
ecause o
f
t
h
e
i
ncrease
d
v
iscosity of the fluid
.
A
remarkable degree of supercooling can be achieved through the use of cryoprotec
-
tants. In the overwinterin
g
larva of the
p
arasitic was
p
Bracon ceph
i

,
for exam
p
le,
g
l
y
cero
l
makes u
p
25% of the fresh bod
y
wei
g
ht (re
p
resentin
g
a 5-Mole concentration) and lowers
t
h
e supercoo
li
ng po
i
nt o
f
t
h

e
h
emo
l
ymp
h
t
o
−
47
◦
C. Per
h
aps a
di
sa
d
vantage to t
h
eus
e
of supercooling as a means of overwintering is that the probability of freezing occurring
increases both with duration of exposure and with the degree of supercooling so that, for
exam
p
le, an insect mi
g
ht freeze in 1 minute a
t
−

19
◦
Cb
ut su
r
vive fo
r1m
o
n
th at
−
10
◦
C
.
T
h
us, to ensure surv
i
va
l
an
i
nsect must
h
ave t
h
ea
bili
t

y
to rema
i
nsu
p
ercoo
l
e
d
at extrem
e
temperatures
f
or s
i
gn
i
ficant per
i
o
d
so
f
t
i
me, even t
h
oug
h
t

h
e average temperatures to w
hi
c
h
it is exposed may be 10
◦
C
to 1
5
◦
C
higher. In other words, it may have to produce muc
h
more antifreeze in anticipation of those extremes than would be judged necessary on th
e
basis of the avera
g
e tem
p
erature
.
Th
ea
l
ternat
i
ve met
h
o

d
,em
pl
o
y
e
dbyf
reez
i
n
g
-to
l
erant s
p
ec
i
es,
i
sto
p
erm
i
t(
b
ea
ble
to w
i
t

h
stan
d
)a
li
m
i
te
d
amount o
ff
reez
i
ng w
i
t
hi
nt
h
e
b
o
d
y. Freez
i
ng must
b
e restr
i
cte

d
t
o
the extracellular fluid, as intracellular freezing damages cells. Ice formation in the extracel
-
l
ular fluid, which is accompanied by release of heat (latent heat of fusion), will therefor
e
reduce the rate at which the bod
y
’s tissues cool as the ambient tem
p
erature falls. Thus, it
w
ill b
etoan
i
nsect’s a
d
vanta
g
eto
h
ave a
l
ar
g
evo
l
ume o

fh
emo
ly
m
ph
(an
d
t
h
ere
i
sev
id
enc
e
t
h
at t
hi
s
i
sc
h
aracter
i
st
i
co
fp
u

p
ae) an
d
to
b
ea
bl
etoto
l
erate
f
reez
i
n
g
o
f
a
l
ar
g
e
p
ro
p
ort
i
o
n
of

t
h
e water w
i
t
hi
n
i
t. Two su
b
s
idi
ary pro
bl
ems accompany t
h
e
f
reez
i
ng-to
l
erant strategy
:
it is necessary (1) to prevent freezing from extending to the cell surfaces (and hence into
the cells) and (2) to
p
revent dama
g
e to cells as a result of deh

y
dration. As water in th
e
66
1
THE
A
BI
O
TI
C
ENVIR
O
NMEN
T
e
xtracellular fluid freezes, the osmotic pressure of the remaining liquid will increase, so
t
hat water will be drawn out of the cells b
y
osmosis.
Freez
i
n
g
to
l
erance
i
s

g
enera
lly f
oun
di
n
i
nsects
li
v
i
n
gi
n extreme
ly
co
ld
env
i
ronments
.
T
h
e
g
enera
l
strate
gy
use

dbyf
reez
i
n
g
-to
l
erant s
p
ec
i
es
i
stos
y
nt
h
es
i
ze
i
ce-nuc
l
eat
i
n
gp
ro
-
t

eins in late fall/early winter (i.e., at temperatures above
−
1
0
◦
C) that initiate freezing o
f
e
xtracellular fluids. This early induction of ice formation is advantageous because the rate
o
f ice formation is less than at lower tem
p
eratures, thus allowin
g
water to move out of
c
e
ll
stoma
i
nta
i
n osmot
i
ce
q
u
ilib
r
i

um an
d
re
d
uce t
h
e
lik
e
lih
oo
d
o
fi
ntrace
ll
u
l
ar
f
reez
i
n
g
(
Baust and Ro
j
as, 198
5
). Throu

g
h the winter both intra- and extracellular
p
ol
y
h
y
drox
y
l
s
are generated. With their ability to bind extensively with water the extracellular cryoprotec-
t
ants will retard the rate at which freezing spreads, while the intracellular cryoprotectant
s
w
ill hold water within cells, to counteract the outwardl
yp
ullin
g
osmotic force. It has also
b
een su
gg
este
d
t
h
at t
h

ecr
y
o
p
rotectants ma
ybi
n
d
w
i
t
hpl
asma mem
b
ranes to re
d
uce t
h
e
i
r
p
ermea
bili
t
y
to water. T
h
ero
l

eo
f
t
h
e ant
if
reeze
p
rote
i
ns
i
n
f
reez
i
n
g
-to
l
erant
i
nsects
i
s
l
ess
cl
ear (Ba
l

e, 2002). An ear
l
y suggest
i
on was t
h
at t
h
ey may protect
i
nsects
f
rom
f
reez
i
ng
i
n
e
arly fall, before the ice-nucleating agents have been synthesized. A more likely functio
n
i
s that the
yp
revent “secondar
y
recr
y
stallization” (refreezin

g
) in the s
p
rin
g
, when
p
ol
y
h
y-
d
rox
yl
s are
b
e
i
n
gd
e
g
ra
d
e
d
un
d
er t
h

e
i
n
fl
uence o
f
r
i
s
i
n
g
tem
p
eratures,
y
et t
h
e
i
nsect must
b
esa
f
e
g
uar
d
e
d

a
g
a
i
nst unex
p
ecte
df
reez
i
n
g
tem
p
eratures
.
O
fi
nterest
i
st
h
eevo
l
ut
i
onary se
l
ect
i

on o
f
g
l
ycero
l
as t
h
e
d
om
i
nant cryoprotectant
because in high concentration this molecule is toxic at above-freezing temperatures. Storey
and Storey (1991) suggested that at least three factors have been critical. First, two molecules
o
f
g
l
y
cerol are
p
roduced from each molecule of its
p
recursor hexose
p
hos
p
hate, im
p

ortant
wh
ere co
llig
at
i
ve
p
ro
p
ert
i
es are concerne
d
. Secon
d
,t
h
es
y
nt
h
es
i
so
f
atr
i
o
l

(3-car
b
on
-
c
onta
i
n
i
ng po
l
yo
l
)
f
rom a
6
-car
b
on precursor conserves t
h
e car
b
on poo
l
compare
d
to syn-
t
hesis of 4- or

5
-carbon polyols (when the extra carbons are lost as carbon dioxide). Third
,
t
he pathways for glycerol synthesis and breakdown already exist in the fat body as part of
li
p
id metabolism. Insects that use
g
l
y
cerol have biochemical
p
athwa
y
s for s
y
nthesizin
g
it
i
n
i
ncreas
i
n
g
amounts as t
h
e tem

p
erature
f
a
ll
s
p
ro
g
ress
i
ve
ly b
e
l
ow 0
◦
Can
d
,e
q
ua
lly
,
f
or
d
egra
di
ng

i
tw
h
en t
h
e temperature
i
ncreases. Suc
hh
as
b
een s
h
own to
b
et
h
e case
in
P
tero
s
-
tic
h
us
b
re
v
icornis,

an
A
rctic carabid beetle that overwinters as a freezing-tolerant adult
.
In
P.
b
revicorni
s
glycerol synthesis begins when an insect is exposed to a fall temperature
o
f0
◦
C
,an
dby
t
h
e
f
o
ll
ow
i
n
g
Decem
b
er-Januar
y

t
h
e concentrat
i
on o
f
t
hi
smo
l
ecu
l
ema
y
r
eac
h
or excee
d
30
g/
100 m
l
,su
f
fic
i
ent to ena
bl
ean

i
nsect to w
i
t
h
stan
d
t
h
e –40
◦
C
t
o
–50
◦
C
t
emperatures to w
hi
c
hi
t may
b
e expose
d
at t
hi
st
i

me. Converse
l
y, as temperatures
i
ncreas
e
t
oward
0
◦
C with the advent of spring, the glycerol concentration falls and the cryoprotectan
t
d
isappears from the hemolymph by about the end of April, coincident with the return of
above-freezin
g
avera
g
e tem
p
eratures (Baust and Morrisse
y
, 1977). A com
p
arable situation
i
so
b
serve
din

E
urosta solidaginis,a
g
all
-
f
orm
i
n
gfly
t
h
at overw
i
nters as a
f
reez
i
n
g
-to
l
eran
t
thi
r
d
-
i
nstar

l
arva. T
h
e
l
arva
h
asat
h
ree-p
h
ase cryoprotectant system t
h
at compr
i
ses g
l
yc-
e
rol, sorbitol, and trehalose. Production of the molecules begins somewhat above 0
◦
C
but
i
s probably triggered by declining temperatures. At temperatures below 0
◦
C, production of
g
l
y

cerol and sorbitol is
g
reatl
y
enhanced. With the return of warm weather in s
p
rin
g
, the
c
oncentrat
i
on o
f
t
h
et
h
ree mo
l
ecu
l
es ra
pidly d
ec
li
nes (Baust an
d
Morr
i

sse
y
, 1977).
Co
ld
-
h
ar
di
ness an
d
overw
i
nter
i
n
gdi
a
p
ause (Sect
i
on 3.2.3)
f
re
q
uent
ly
occur to
g
et

h
er,
and the question of whether the phenomena are physiologically related has been widely de
-
bated (Denlinger, 1991). As noted above, studies have correlated the synthesis of cryopro-
t
ectants with lowered tem
p
eratures, and vice versa. However, onl
y
a handful of exam
p
les are
662
CHAPTER
22
k
nown in which insects exposed to short days (but not low temperatures) develop increase
d
c
old tolerance,
p
resumabl
y
b
y
s
y
nthesizin
g

cr
y
o
p
rotectants (Saunders, 2002). Denlin
g
e
r
(1991) conc
l
u
d
e
d
t
h
at,
gi
ven t
h
e
di
vers
i
t
y
o
f
overw
i

nter
i
n
g
strate
gi
es
f
oun
d
amon
gi
nsects,
genera
li
zat
i
on was not poss
ibl
e. T
h
us,
i
n some spec
i
es co
ld
-
h
ar

di
ness occurs
i
nt
h
ea
b
sence
o
f diapause; in others, diapause and cold-hardiness may occur coincidentally or may b
e
p
hysiologically linked (regulated by the same signals). According to Pullin (1996) there i
s
increasin
g
evidence that the
p
roduction of
p
ol
y
h
y
drox
y
ls is linked to the
g
reat su
pp

ressio
n
of
meta
b
o
li
c rate w
hi
c
h
accom
p
an
i
es
di
a
p
ause.
3. L
i
ght
Ligh
texertsama
j
or
i
n
fl

uence on t
h
ea
bili
t
y
o
f
a
l
most a
ll i
nsects to surv
i
ve an
d
mu
l
t
iply.
A
we
ll
-
d
eve
l
o
p
e

d
v
i
sua
l
s
y
stem ena
bl
es
i
nsects to res
p
on
di
mme
di
ate
ly
an
ddi
rect
ly
to
ligh
t
st
i
mu
li

o
f
var
i
ous
ki
n
d
s
i
nt
h
e
i
r searc
hf
or
f
oo
d
, a mate, a “
h
ome,” or an ov
i
pos
i
t
i
on s
i

te, an
d
in avoidance of danger (Chapter 12, Section 7). But light influences the biology of man
y
insects in another manner which stems from the earth’s rotation about its axis, resultin
g
i
nare
g
u
l
ar
ly
recurr
i
n
g
24-
h
our c
y
c
l
eo
f ligh
tan
dd
ar
k
ness, t

h
e
ph
oto
p
er
i
o
d
.
∗
Because
t
h
e eart
h
’s ax
i
s
i
s not
p
er
p
en
di
cu
l
ar to t
h

e
pl
ane o
f
t
h
e eart
h
’s or
bi
t aroun
d
t
h
e sun, an
d
b
ecause t
h
eor
bi
tvar
i
es t
h
roug
h
out t
h
e year, t

h
ere
l
at
i
ve amounts o
fli
g
h
tan
dd
ar
k
ness
i
n
the photoperiod change seasonally and from point to point over the earth’s surface.
P
hoto
p
eriod influences or
g
anisms in two wa
y
s: it ma
y
either induce short-term (diurnal
)
b
e

h
av
i
ora
l
res
p
onses w
hi
c
h
occur at s
p
ec
i
fie
d
t
i
mes
i
nt
h
e 24-
h
our c
y
c
l
e, or

b
r
i
n
g
a
b
out
l
on
g
-term (seasona
l
)
phy
s
i
o
l
o
gi
ca
l
res
p
onses w
hi
c
hk
ee

p
or
g
an
i
sms
i
n tune w
i
t
h
c
h
an
gi
n
g
env
i
ronmenta
l
con
di
t
i
ons. In
b
ot
h
s

i
tuat
i
ons,
h
owever, a
k
ey
f
eature
i
st
h
at t
h
e organ
i
sm
s
that respond have the ability to measure time. In short-term responses the time interva
l
b
etween the onset of li
g
ht or darkness and commencement of the activit
y
is im
p
ortant. For
s

easona
l
res
p
onses, t
h
ea
b
so
l
ute
d
a
yl
en
g
t
h
(num
b
er o
fh
ours o
f ligh
t
i
n a 24-
h
our
p

er
i
o
d
)
i
s
u
sua
lly
cr
i
t
i
ca
l
,t
h
ou
gh i
n some s
p
ec
i
es
i
t
i
st
h

e
d
a
y
-to-
d
a
yi
ncrease or
d
ecrease
i
nt
h
e
ligh
t
per
i
o
d
t
h
at
i
s measure
d
.Inot
h
er wor

d
s, organ
i
sms t
h
at ex
hibi
tp
h
otoper
i
o
di
c responses ar
e
s
aid to possess a “biological clock,” the nature of which is unknown, though its effects i
n
a
nimals are fre
q
uentl
y
manifest throu
g
h chan
g
es in endocrine activit
y
.

3.1. Dail
y
Influences of Photo
p
eriod
V
arious advantages may accrue to members of a species through the performance o
f
p
articular activities at set times of the
p
hoto
p
eriod. It ma
y
be advanta
g
eous for some insects
to
b
ecome act
i
ve at
d
awn,
d
us
k
,ort
h

rou
gh
t
h
en
igh
tw
h
en am
bi
ent tem
p
eratures are
b
e
l
ow
t
h
eu
pp
er
l
et
h
a
lli
m
i
t, c

h
ances o
fp
re
d
at
i
on are re
d
uce
d
,an
d
t
h
e rate o
f
water
l
oss t
h
rou
gh
t
h
e cut
i
c
l
e

i
s
l
essene
db
yt
h
e genera
ll
y greater re
l
at
i
ve
h
um
idi
ty t
h
at occurs at t
h
ese t
i
mes.
For
o
ther insects, in which visual stimuli are important, activity during specific daylight
h
ours may be advantageous; for example, food may be available for only a limited part o
f

t
h
e
d
a
y
, or converse
ly
,ot
h
er,
d
etr
i
menta
lf
actors ma
y
restr
i
ct
f
ee
di
n
g
toas
p
ec
i

fic
p
er
i
o
d
.
F
o
r
m
an
y
s
p
ec
i
es
i
t
i
sc
l
ear
ly b
enefic
i
a
lf
or t

h
e
i
r mem
b
ers to s
h
ow s
y
nc
h
ronous act
i
v
i
t
y,
a
st
hi
sw
ill i
ncrease t
h
ec
h
ance o
f
contact
b

etween sexes. “Act
i
v
i
ty”
i
nt
hi
s sense
i
s not
∗
A
s Bec
k
(1980) note
d
, some aut
h
ors use t
hi
s term to
d
escr
ib
et
h
e
li
g

h
t port
i
on o
f
a
li
g
h
t-
d
ar
k
cyc
l
e(
i
.e.
,
sy
non
y
mousl
y
with da
y
len
g
th).
663

THE
A
BI
O
TI
C
ENVIR
O
NMEN
T
r
estricted to locomotion, however. For example, in many species of moths, it is by and larg
e
onl
y
the males that exhibit dail
y
rh
y
thms of locomotor activit
y
. The females are sedentar
y,
b
ut,
i
nt
h
e
i

rv
i
r
gi
n con
di
t
i
on,
h
ave
d
a
ily
r
hy
t
h
ms o
f
ca
lli
n
g
(secret
i
on o
f
ma
l

e-attract
i
n
g
ph
eromones) t
h
at ena
bl
ema
l
es to
l
ocate t
h
em
.
3.1.1.
Ci
rcad
i
an Rhythms
I
na
f
ew s
p
ec
i
es

d
a
ily
r
hy
t
h
ms o
f
act
i
v
i
t
y
are tr
igg
ere
dby
env
i
ronmenta
l
cues an
d
are t
h
ere
f
ore o

f
exo
g
enous or
igi
n. For exam
pl
e, t
h
e act
i
v
i
t
y
o
f
t
h
est
i
c
ki
nsect
C
arausius
m
oro
s
u

s
i
s
di
rect
l
y provo
k
e
db
y
d
a
il
yc
h
anges
i
n
li
g
h
t
i
ntens
i
ty. However,
i
n most spec
i

e
s
t
hese rhythms are not simply a response to the onset of daylight or darkness; that is, daw
n
o
r dusk do not act as a tri
gg
er that switches the activit
y
on or off. Rather, the rh
y
thms ar
e
e
n
d
o
g
enous (or
igi
nate w
i
t
hi
nt
h
eor
g
an

i
sm
i
tse
lf
)
b
ut are su
bj
ect to mo
di
ficat
i
on (re
g
u
l
a
-
ti
on)
by ph
oto
p
er
i
o
d
an
d

ot
h
er env
i
ronmenta
lf
actors. T
h
at t
h
er
hy
t
h
mor
igi
nates
i
nterna
lly
m
ay
b
e
d
emonstrate
db
yp
l
ac

i
ng t
h
e organ
i
sm
i
n constant
li
g
h
tor
d
ar
k
ness. T
h
e organ
i
s
m
continues to begin its activity at approximately the same time of the 24-hour cycle, as i
t
d
id when subject to alternating periods of light and darkness. Because the rhythm has a
n
a
pp
rox
i

mate
ly
24-
h
our c
y
c
l
e,
i
t
i
s
d
escr
ib
e
d
as a c
i
rca
di
an r
hy
t
h
m. W
h
en t
h

er
hy
t
h
m
i
sno
t
i
n
fl
uence
dby
t
h
eenv
i
ronment, t
h
at
i
s, w
h
en env
i
ronmenta
l
con
di
t

i
ons are
k
e
p
t constant
,
th
er
h
yt
h
m
i
s
d
escr
ib
e
d
as “
f
ree-runn
i
ng.” W
h
en env
i
ronmenta
l

con
di
t
i
ons vary regu
l
ar
l
y
in
e
ach 24-hour cycle, and the beginning of the activity occurs at precisely the same time in the
c
y
cle, the rhythm is “entrained.” For example, if a cockroach begins its locomotor activit
y
2
hours after darkness, this activit
y
is said to be
p
hoto
p
eriodicall
y
entrained. The role o
f
ph
oto
p

er
i
o
di
st
h
ere
f
ore to a
dj
ust (
ph
ase set) t
h
een
d
o
g
enous r
hy
t
h
msot
h
at t
h
e act
i
v
i

t
y
o
ccurs eac
hd
a
y
at t
h
e same t
i
me
i
nre
l
at
i
on to t
h
e onset o
fd
a
yligh
tor
d
ar
k
ness. T
h
ou

gh
photoperiod is probably the most important regulator of circadian rhythms in insects, othe
r
e
nvironmental factors such as temperature, humidity, and light intensity, as well as physio
-
lo
g
ical variables such as a
g
e, re
p
roductive state, and de
g
ree of desiccation or starvation ma
y
m
o
dify b
e
h
av
i
or
p
atterns. P
h
oto
p
er

i
o
di
ca
lly
entra
i
ne
dd
a
ily
r
hy
t
h
ms are
k
nown to occur
in
r
e
l
at
i
on to
l
ocomotor act
i
v
i

t
y
,
f
ee
di
n
g
, mat
i
n
gb
e
h
av
i
or (
i
nc
l
u
di
n
g
swarm
i
n
g
), ov
ip

os
i
t
i
on,
an
d
ec
l
os
i
on, examp
l
es o
f
w
hi
c
h
are g
i
ven
b
e
l
ow.
M
any examples are known of insects that actively run, swim, or fly during a charac-
t
eristic period of the 24-hour cycle, this activity usually occurring in relation to some other

rhy
t
h
m suc
h
as
f
ee
di
n
g
or mate
l
ocat
i
on. I
n
P
eriplaneta
a
n
d
ot
h
er coc
k
roac
h
es act
i

v
i
t
y
b
e
gi
ns s
h
ort
ly b
e
f
ore t
h
e ant
i
c
ip
ate
d
onset o
fd
ar
k
ness, reac
h
es a
p
ea

k
some 2–3
h
ours a
f
ter
d
ar
k
,an
dd
ec
li
nes to a
l
ow
l
eve
lf
or t
h
e rema
i
n
i
ng per
i
o
d
o

fd
ar
k
ness an
dd
ur
i
ng most o
f
t
he
light period (Figure 22.2A).
D
roso
ph
i
l
aro
b
usta (Figure 22.2B) flies actively during the las
t
3
hours of the light phase but is virtually inactive for the rest of the 24-hour period. Male
ants of the s
p
ecies Camponotus clarithora
x
are most active durin
g
the first few hours of

th
e
ligh
t
p
er
i
o
db
ut s
h
ow
li
tt
l
e act
i
v
i
t
y
at ot
h
er t
i
mes (F
ig
ure 22.2C). T
h
ea

b
ove exam
pl
es
s
h
owawe
ll
-
d
efine
d
s
i
ng
l
e pea
k
(un
i
mo
d
a
l
r
h
yt
h
m) o
f

act
i
v
i
ty. Ot
h
er spec
i
es,
h
owever
,
h
ave bimodal or trimodal rhythms. For example, females of the silver-spotted tiger moth
,
Ha
l
isi
d
ota ar
g
entata
,
show two peaks of flight activity during darkness, the first shortl
y
after darkness be
g
ins, the second about midwa
y
throu

g
h the dark
p
eriod (Fi
g
ure 22.3A).
Ma
l
es o
f
t
hi
ss
p
ec
i
es,
i
n contrast,
h
aveatr
i
mo
d
a
l
r
hy
t
h

mo
f fligh
t act
i
v
i
t
y
(F
ig
ure 22.3B
)
(
Bec
k
, 1980)
.
R
h
yt
h
m
i
c
f
ee
di
ng act
i
v

i
ty
i
s apparent
i
n
l
arvae o
f
some Lep
id
optera,
f
or examp
l
e
,
H. ar
g
entata
,
which feed almost exclusively during darkness. Female mosquitoes, too
,
66
4
CHAPTER
22
F
I
GU

RE 22.2. Locomotor act
i
v
i
t
y
r
hy
t
h
ms
i
n
i
nsects,
ill
ustrat
i
n
gph
oto
p
er
i
o
di
c entra
i
nment. (A
)

Perip
l
aneta
;
(B
)
D
roso
p
hil
a
; and (C)
C
am
p
onotus
.
[From S. D. Beck, 1968
,
I
nsect Photo
p
eriodism
.
By permission of Academi
c
P
ress, Inc., an
d
t

h
e aut
h
or.
]
F
I
GU
RE 22.3. P
h
oto
p
er
i
o
di
ca
lly
entra
i
ne
d fligh
t act
i
v
i
t
yin
H
a

l
isi
d
ota argentat
a
(
Le
pid
o
p
tera). [From D. K.
Edwards, 1962, Laboratory determinations of the daily flight times of separate sexes of some moths in naturally
ch
ang
i
ng
li
g
h
t
,
C
an. J. Zoo
l
.
40
:511–530. By permission of the National Research Council of Canada.
]
665
THE

A
BI
O
TI
C
ENVIR
O
NMEN
T
show peaks of feeding activity either at dawn or dusk, or during both of these periods
,
t
hou
g
h there is some ar
g
ument with re
g
ard to whether feedin
g
activit
y
is endo
g
enous o
r
s
i
m
ply

a
di
rect res
p
onse to a
p
art
i
cu
l
ar
ligh
t
i
ntens
i
t
y
.
S
evera
lg
oo
d
exam
pl
es ma
yb
ec
i

te
d
to
ill
ustrate t
h
e
i
m
p
ortance o
fph
oto
p
er
i
o
di
n
e
ntraining daily endogenous rhythms of mating behavior. Many virgin female Lepidopter
a
b
egin to secrete male-attracting pheromones shortly after the onset of darkness and ar
e
m
aximall
y
rece
p

tive to males about midwa
y
throu
g
h the dark
p
eriod. E
q
uall
y
, males sho
w
m
ax
i
mum exc
i
ta
bili
t
y
to t
h
ese
ph
eromones
i
nt
h
e ear

ly p
art o
f
t
h
e
d
ar
kp
er
i
o
d
.T
h
ema
l
es
o
f
certa
i
n ant spec
i
es un
d
erta
k
e mat
i

ng
fli
g
h
ts at c
h
aracter
i
st
i
ct
i
mes w
i
t
hi
nt
h
e
li
g
h
t per
i
o
d,
t
ypically near dawn or dusk. Mosquitoes and other Nematocera form all-male swarms that
females enter for insemination. Formation of these swarms, which occurs both at dawn and
at dusk, is an endo

g
enous rh
y
thm, entrained b
yp
hoto
p
eriod, thou
g
h tem
p
erature and li
g
h
t
i
ntens
i
t
y
are a
l
so
i
nvo
l
ve
d
(Bec
k

, 1980).
F
or
some
i
nsect s
p
ec
i
es, e
gg l
a
yi
n
gh
as
b
een s
h
own to
b
ea
ph
oto
p
er
i
o
di
ca

lly
entra
i
ne
d
e
n
d
ogenous r
h
yt
h
m. In t
h
e mosqu
i
toe
s
A
e
d
es ae
gy
pt
i
a
n
d
Taenior
h

ync
h
us
f
uscopennatus
,
for example, oviposition is concentrated in the period immediately after sunset and before
d
awn, res
p
ectivel
y
. In other mos
q
uitoes, however, no ovi
p
osition rh
y
thm exists and e
gg
l
a
yi
n
g
a
pp
ears to
b
e

d
e
p
en
d
ent on
ligh
t
i
ntens
i
t
y.
M
an
y
exam
pl
es are
k
nown o
fi
nsects t
h
at mo
l
ttoa
d
u
l

ts
d
ur
i
n
g
ac
h
aracter
i
st
i
c
p
er
i
o
d
o
f
t
h
e
d
ay. Many trop
i
ca
l
O
d

onata ex
hibi
t mass ec
l
os
i
on
d
ur
i
ng t
h
e ear
l
yeven
i
ng an
d
are
able to fly by the following morning. Corbet (1963) suggested that this minimizes the effects
of predators such as birds and other dragonflies that hunt by sight. In temperate climates
wh
ere n
igh
tt
i
me tem
p
eratures are
g

enera
lly
too
l
ow
f
or emer
g
ence, t
h
ere ma
yb
easw
i
tc
h
t
o emer
g
ence
d
ur
i
n
g
certa
i
n
d
a

yligh
t
h
ours. In more r
ig
orous c
li
mates tem
p
erature a
pp
ear
s
t
o overr
id
ep
h
otoper
i
o
d
∗
a
sa
f
actor regu
l
at
i

ng emergence, w
hi
c
h
occurs opportun
i
st
i
ca
ll
y
at any time of the day provided the ambient temperature is suitable (Section 2.3). Species of
E
phemeroptera and Diptera also have daily emergence patterns, which may be associated
w
ith immediate matin
g
and ovi
p
osition. Thou
g
h man
y
insect s
p
ecies are known that have a
d
a
ily
emer

g
ence r
hy
t
h
m,
f
or on
ly
a
f
ew o
f
t
h
ese, ma
i
n
ly
D
ip
tera,
i
sex
p
er
i
menta
l
ev

id
enc
e
av
ail
a
bl
et
h
at proves t
h
een
d
ogenous nature o
f
t
h
er
h
yt
h
m. In contrast to t
h
e prev
i
ous
ly
d
escribed rhythmic processes, emergence occurs but once in the life of an insect and result
s

i
n the appearance of a very different developmental stage, the adult. Nevertheless, this singl
e
ev
e
nt, like dail
y
re
p
eated
p
rocesses, is an endo
g
enous rh
y
thm, entrained b
y
environmenta
l
st
i
mu
li
,es
p
ec
i
a
lly ph
oto

p
er
i
o
d
,t
h
at exert t
h
e
i
re
ff
ect
i
n ear
li
er
d
eve
l
o
p
menta
l
sta
g
es. For
e
xam

pl
e,
p
o
p
u
l
at
i
ons o
f
man
y
D
rosop
h
i
la
sp
ec
i
es emer
g
eatmax
i
mum rates 1–2
h
our
s
a

f
ter
d
awnont
h
e
b
as
i
so
f
p
h
otoper
i
o
di
c entra
i
nment e
i
t
h
er
i
nt
h
e
l
arva

l
or pupa
l
stage.
Thus, if a culture o
f
Droso
ph
i
l
a larvae of variable ages is maintained in darkness from the
egg
s
ta
g
e exce
p
t for one brief
p
eriod of li
g
ht (a flash lastin
g
as little as 1/2000 of a second
i
ssu
f
fic
i
ent) t

h
ea
d
u
l
ts w
ill
emer
g
eatre
g
u
l
ar 24-
h
our
i
nterva
l
s,
b
ase
d
on t
h
e onset o
f
t
he
ligh

t
p
er
i
o
db
e
i
n
g
e
q
u
i
va
l
ent to
d
awn; t
h
at
i
s, t
h
e
b
e
gi
nn
i

n
g
o
f
t
h
e
ligh
t
p
er
i
o
d
serves as t
h
e
r
e
f
erence po
i
nt
f
or entra
i
n
i
ng t
h

e
i
nsects’ emergence r
h
yt
h
m (Bec
k
, 1980)
.
Physiological and molecular studies of light-regulated circadian rhythms have reveale
d
t
hat, althou
g
h there is a basic o
p
eratin
g
s
y
stem, this ma
y
occur in a variet
y
of form
s
(
Saun
d

ers, 2002). T
h
e
b
as
i
cs
y
stem com
p
r
i
ses t
h
ree com
p
onents: an
i
n
p
ut
p
at
h
wa
y
,w
hi
c
h

i
nc
l
u
d
es a
ph
otorece
p
tor; an osc
ill
ator (“c
l
oc
k
”or
p
acema
k
er) t
h
at rece
i
ves t
h
e entra
i
n
i
n

g
∗
In t
h
e Arct
i
c summer t
h
ere are, o
f
course, 24
h
ours o
fli
g
h
t per
d
ay, an
d
p
h
otoper
i
o
d
cannot serve as an entra
i
n
i

n
g
f
actor for diurnal rhythms.
f
f
666
CHAPTER
22
signal from the photoreceptor; and the output pathway that connects the clock to the effector
structures for the rh
y
thms
.
In coc
k
roac
h
es, cr
i
c
k
ets an
d
some
b
eet
l
es t
h

e com
p
oun
d
e
y
es are t
h
e
ph
otorece
p
tors
,
and a clock is located near the medulla re
g
ions of each o
p
tic lobe (Fi
g
ure 13.
5
). However,
in flies, moths and other beetles neither the compound eyes nor the ocelli are essential as
p
hotoreceptors for circadian rhythms. These insects may use several photoreceptors fo
r
entrainment, includin
gg
rou

p
s of neurons within the central brain re
g
ion. In flies the clock
i
s
l
ocate
di
nt
h
e
l
atera
l
neurons (
l
ocate
d
near t
h
e
b
or
d
er o
f
t
h
eo

p
t
i
c
l
o
b
ean
db
ra
i
n) o
r
t
h
e
i
r equ
i
va
l
ent, w
hil
e
i
n mot
h
st
h
ec

l
oc
kli
es
d
eep
i
nt
h
e centra
l
part o
f
t
h
e
b
ra
i
n. Outpu
t
p
athways vary in their nature, depending on the rhythmic activity that is being controlled
.
Fo
re
xample, in cockroaches the clock connects with interneurons that run to the thoracic
g
an
g

lia where locomotor activit
y
is re
g
ulated. B
y
contrast, the eclosion rh
y
thm in moths i
s
tr
igg
ere
dby
ec
l
os
i
on
h
ormone w
h
ose re
l
ease
i
s contro
ll
e
dby

t
h
ec
l
oc
ki
nt
h
e
b
ra
i
n.
Th
ou
gh b
e
h
av
i
ora
l
r
hy
t
h
ms suc
h
as
l

ocomotor act
i
v
i
t
y
an
d
ec
l
os
i
on are re
g
u
l
ate
dby
a
centra
l
c
l
oc
k
,
i
t
i
sev

id
ent t
h
at many ot
h
er c
i
rca
di
an r
h
yt
h
ms operate
i
n
d
epen
d
ent
l
y
;
that is, many organs and tissues possess their own clock (Giebultowicz, 2000, 2001). This
is readil
y
shown b
y
se
p

aratin
g
a structure from the rest of the bod
y
and observin
g
that i
t
reta
i
ns
i
ts r
hy
t
h
m
i
c
i
t
y
o
ff
unct
i
on. To
d
ate,
p

er
iph
era
l
c
l
oc
k
s
h
ave
b
een re
p
orte
df
or
g
ona
d
s
,
M
a
lpighi
an tu
b
u
l
es, en

d
ocr
i
ne
gl
an
d
s, e
pid
erm
i
s, an
d
some sense or
g
ans
.
Mo
l
ecu
l
ar stu
di
es, ma
i
n
l
yus
i
ng Droso

ph
i
l
a mutants,
h
ave
id
ent
i
fie
d
at
l
east 10 gene
s
in the central brain oscillator that are involved in circadian locomotor and eclosion rhythms
.
T
wo of these genes,
p
eriod
a
nd timeless, and their protein products (PER and TIM, respec-
t
i
ve
ly
) are res
p
ons

ibl
e
f
or t
h
e actua
l
t
i
m
i
n
g
mec
h
an
i
sm, s
h
ow
i
n
g
c
i
rca
di
an act
i
v

i
t
y
an
d
p
ro
d
uct
i
on, res
p
ect
i
ve
ly
.At
hi
r
dg
ene
,
cryptochrome,co
d
es
f
or a
ph
otosens
i

t
i
ve
p
rote
in
t
h
at mo
d
u
l
ates t
h
e act
i
on o
f
PER an
d
TIM, t
h
ere
b
y resett
i
ng t
h
ec
l

oc
k
.Ot
h
er genes are
o
n the output pathway (i.e., downstream of the clock), and their gene products induce
manifestation of the circadian rhythm. Homologous genes t
o
p
eriod have been detected
in the central oscillators of moths and cockroaches, as well as in or
g
ans with
p
eri
p
hera
l
cl
oc
k
s(G
i
e
b
u
l
tow
i

cz, 2000),
i
n
di
cat
i
n
g
t
h
at t
h
ere ma
yb
e a common mo
l
ecu
l
ar
b
as
i
s
f
or
a
ll
c
i
rca

di
an c
l
oc
k
s. For
f
urt
h
er
d
eta
il
so
f
t
h
emo
l
ecu
l
ar components o
f
c
i
rca
di
an c
l
oc

k
s,
see Giebultowicz (2000, 2001), Stanewsky (2002), and Zorda
n
e
ta
l
. (2003).
3
.2. Seasonal Influences of Photo
p
eriod
P
hotoperiod affects a variety of long-term physiological processes in insects and, i
n
doing so, allows a species to (1) exploit suitable environmental conditions and (2) survive
p
eriods when climatic conditions are adverse. Some of the wa
y
s in which s
p
ecies are enabled
to ex
pl
o
i
tasu
i
ta
bl

eenv
i
ronment
i
nc
l
u
d
e
b
e
i
n
gi
nana
pp
ro
p
r
i
ate
d
eve
l
o
p
menta
l
sta
g

eassoo
n
as t
h
esu
i
ta
bl
e con
di
t
i
ons appear, an
d
grow
i
ng or repro
d
uc
i
ng at t
h
e max
i
mum rate w
hil
e
c
onditions last. Obviously, to survive adverse conditions, members of a species must already
be in an appropriate physiological state when the conditions develop. In other words, th

e
p
h
y
siolo
g
ical or behavioral chan
g
es are induced b
y
cues that are not in themselves adverse
.
Th
us, amon
g
t
h
e
p
rocesses
k
nown to
b
ea
ff
ecte
dbyph
oto
p
er

i
o
d
are t
h
e nature (
q
ua
li
tat
i
ve
ex
p
ress
i
on) an
d
rate o
fd
eve
l
o
p
ment, re
p
ro
d
uct
i

ve a
bili
t
y
an
d
ca
p
ac
i
t
y
,s
y
nc
h
ron
i
ze
d
a
d
u
lt
emergence, induction of diapause, and possibly cold-hardiness. Several of these processes
are closely related and are therefore affected simultaneously. Other environmental factors,
es
p
eciall
y

tem
p
erature, ma
y
modif
y
the effects of
p
hoto
p
eriod.
667
THE
A
BI
O
TI
C
ENVIR
O
NMEN
T
3.2.1. Nature and Rate of Develo
p
ment
I
n some species larval growth rates are affected by photoperiod. For some species
g
rowth is accelerated under long-day conditions (when there are 16 or more hours of light
i

n each 24-hour c
y
cle) and inhibited in
p
hoto
p
eriods that contain 12 or fewer hours of li
g
ht;
f
or ot
h
er s
p
ec
i
es, t
h
e converse
i
s true. O
f
ten t
h
ee
ff
ect o
fph
oto
p

er
i
o
d
on
g
rowt
h
rate
i
s
corre
l
ate
d
w
i
t
h
t
h
e nature o
fdi
a
p
ause
i
n
d
uct

i
on; t
h
at
i
s, s
p
ec
i
es t
h
at
g
row more s
l
ow
ly
u
n
d
er s
h
ort-
d
ay con
di
t
i
ons ten
d

a
l
so to enter
di
apause as a resu
l
to
f
s
h
ort
d
ays. However,
i
t
should be noted thatthe growth rateof many species that enter a photoperiodicallycontrolle
d
d
ia
p
ause is not affected b
yp
hoto
p
eriod.
Ex
p
osure to
diff
erent

ph
oto
p
er
i
o
d
s suc
h
as occur
i
n
diff
erent seasons ma
y
resu
l
t
in
th
e
d
eve
l
o
p
ment o
fdi
st
i

nct
f
orms o
f
as
p
ec
i
es, t
h
at
i
s,
p
o
lyph
en
i
sm. T
h
e
phy
s
i
o
l
o
gi
ca
l

(
en
d
ocr
i
ne)
b
as
i
so
f
po
l
yp
h
en
i
sm
h
as
b
een out
li
ne
di
nC
h
apter 21 (Sect
i
on 7), an

d
t
h
e
present discussion is restricted to aconsideration of its induction by photoperiod. Sometimes
t
he forms that develop are so strikingly different that they were described originally as
se
p
arate s
p
ec
i
es. Bec
k
(1980) c
i
te
d
as an exam
pl
et
h
e Euro
p
ean
b
utter
fly
A

raschnia levana
,
d
escr
ib
e
d
or
igi
na
lly
as two s
p
ec
i
es
,
A
.le
v
an
a
an
d
A
.prors
a
,b
ut which is
n

ow k
n
ow
n
to be a
seasona
ll
y
di
morp
hi
c spec
i
es. Caterp
ill
ars reare
d
un
d
er
l
ong-
d
ay con
di
t
i
ons metamorp
h
ose

i
nto the non-diapausing, black-winged (prorsa) form; when they have developed at short day
lengths the caterpillars emerge as red-winged (levana) adults that overwinter in diapause.
This exam
p
le shows a t
yp
ical feature of most dimor
p
hic Le
p
ido
p
tera, namel
y
, that one form
i
sc
h
aracter
i
st
i
ca
lly f
oun
di
n summer an
di
s non-

di
a
p
aus
i
n
g
,w
h
ereas t
h
ea
l
ternate
f
orm
is
th
e
di
apaus
i
ng, overw
i
nter
i
ng stage
.
Photoperiodically influenced polyphenism is also seen in the seasonal occurrence
o

f normal-winged, brachypterous, and/or apterous forms of species of Orthoptera an
d
Hemi
p
tera. But
p
erha
p
s the best-known exam
p
le of the effects of
p
hoto
p
eriod on develo
p
-
m
ent
i
st
h
at o
fp
o
lyph
en
i
sm
i

na
phid
s. T
h
e
lif
ec
y
c
l
eo
f
a
phid
s
p
ec
i
es (see F
ig
ure 8.8)
is
com
pl
ex an
d
var
i
e
db

ut s
h
ows
b
eaut
if
u
lly h
ow an
i
nsect ta
k
es
f
u
ll
a
d
vanta
g
eo
f
su
i
ta
bl
e con-
di
t
i

ons
f
or growt
h
an
d
repro
d
uct
i
on. A
k
ey
f
eature o
f
t
h
e
lif
ecyc
l
e
i
st
h
e occurrence w
i
t
hi

n
it
o
f wingless, neotenic females that reproduce viviparously and parthenogenetically. In man
y
s
p
ecies the offs
p
rin
g
are entirel
y
female. This combination of features enables a
p
hids to
r
e
p
ro
d
uce ra
pidly
an
db
u
ild
u
p
mass

i
ve
p
o
p
u
l
at
i
ons
i
nt
h
es
p
r
i
n
g
an
d
summer w
h
en weat
h
e
r
con
di
t

i
ons are
g
oo
d
an
df
oo
di
sa
b
un
d
ant. As a resu
l
to
f
t
h
e crow
di
n
g
t
h
at resu
l
ts
f
rom t

hi
s
r
epro
d
uct
i
ve act
i
v
i
ty, w
i
nge
d
m
i
gratory
f
orms
d
eve
l
op, an
d
a part o
f
t
h
e popu

l
at
i
on moves
o
n to alternate host plants. From these migratory forms several more generations of female
aphids (alienicolae) are produced (again through viviparity and parthenogenesis), whic
h
m
a
yb
ew
i
n
g
e
d
or a
p
terous. Eventua
lly
t
h
ea
li
en
i
co
l
ae

gi
ve r
i
se to w
i
n
g
e
d
sexu
p
arae (a
ll f
e-
m
a
l
e) t
h
at m
ig
rate
b
ac
k
to t
h
eor
igi
na

lh
ost
pl
ant, an
d
w
h
ose
p
ro
g
en
y
ma
yb
ee
i
t
h
er w
i
n
g
e
d
m
a
l
es or w
i

ng
l
ess
f
ema
l
es (ov
i
parae). T
h
ese repro
d
uce sexua
ll
yan
dl
ay eggs t
h
at pass t
h
e
w
inter in diapause on the host plant. The following spring each egg gives rise to a female in
-
d
ividual, the “stem mother” or fundatrix, normally wingless, that reproduces asexually, and
from which several
g
enerations of neotenic females (fundatri
g

eniae) arise. There are man
y
var
i
ants o
f
t
hi
s
g
enera
li
ze
d lif
ec
y
c
l
e, most o
f
ten t
h
rou
gh i
ts s
i
m
pli
ficat
i

on; t
h
at
i
s, one o
r
m
ore o
f
t
h
e
lif
e stages
i
som
i
tte
d
as,
f
or examp
l
e,
i
n spec
i
es t
h
at

d
o not a
l
ternate
h
osts w
h
en
m
igrants and whose offspring do not appear as distinct forms. Indeed, in some species sexual
forms have never been described and reproduction appears to be strictly parthenogenetic.
The develo
p
ment of these seasonall
y
occurrin
g
a
p
hid forms is influenced b
y
a variet
y
of
env
i
ronmenta
lf
actors,
i

nc
l
u
di
n
gd
a
yl
en
g
t
h
. Crow
di
n
gi
st
h
ema
j
or
f
actor t
h
at
i
n
fl
uences
668

CHAPTER
22
p
roduction of summer migrants, whereas the shorter days of late summer and early fall
induce develo
p
ment of sexu
p
arae and ovi
p
arae. For some s
p
ecies there is a critical da
y
l
en
g
t
hf
or
i
n
d
uct
i
on o
f
ov
ip
arous

f
orms. In Megoura v
i
c
i
ae (Fi
g
ure 21.15), for exam
p
le
,
whi
c
hd
oes not a
l
ternate
h
ost
pl
ants (
i
.e.,
i
t
h
as no m
ig
rant
f

orm, an
d
t
h
eov
ip
arae are
p
roduced directly from fundatrigeniae), the critical day length is 14 hours
55
minutes at
15
◦
C. At greater day lengths continuous production of viviparous, parthenogenetic females
o
ccurs; when the da
y
len
g
th is below this critical value ovi
p
arae are
p
roduced.
In some s
p
ec
i
es
p

ro
d
uct
i
on o
f
ma
l
es a
l
so
i
s
i
n
d
uce
dby
s
h
ort
d
a
y
s, t
h
ou
gh
tem
p

erature
an
d
materna
l
a
g
e exert a stron
gi
n
fl
uence. For exam
pl
e,
i
nt
h
e
p
ea a
phid
Ac
y
rt
h
osip
h
o
n
p

isu
m
ma
l
eo
ff
spr
i
ng are not pro
d
uce
db
y young
f
ema
l
es or
b
y
f
ema
l
es reare
d
un
d
er
l
ong-
day conditions. Old females reared at short day lengths and temperatures from 1

3
◦
C
to
20
◦
C
p
roduce a lar
g
e
p
ro
p
ortion of males. Outside this tem
p
erature ran
g
e the
p
ro
p
ortion o
f
ma
l
es
d
ec
li

nes
.
3
.2.2. Reproduct
i
ve Ab
i
l
i
ty and
C
apac
i
ty
T
he effects of
p
hoto
p
eriod on re
p
roductive
p
rocesses are almost all indirect, that is,
resu
l
t
f
rom ot
h

er
ph
oto
p
er
i
o
di
ca
lly i
n
d
uce
dph
enomena, es
p
ec
i
a
lly
a
d
u
l
t
di
a
p
ause (see
b

e-
l
ow). B
yi
ts e
ff
ect on t
h
e nature o
fd
eve
l
o
p
ment, as
i
na
phid
s,
ph
oto
p
er
i
o
d
ma
yi
n
di

rect
ly
mo
dif
yt
h
e
f
ecun
di
ty o
f
a spec
i
es. Bec
k
(1980) note
d
one examp
l
eo
f
an apparent
l
y
di
rec
t
effect of photoperiod on fecundity. In
Pl

ute
ll
ax
yl
oste
lla
, the diamondback moth, egg pro-
duction in individuals reared under long-day photoperiods averaged 74 eggs/moth, whereas
e
gg
p
ro
d
uct
i
on un
d
er s
h
ort-
d
a
y
con
di
t
i
ons was on
ly h
a

lf
t
hi
sva
l
ue.
3
.2.3. D
i
a
p
ause
B
eck (1980, p. 119) described diapause as “a genetically determined state of suppressed
develo
p
ment, the ex
p
ression of which ma
y
be controlled b
y
environmental factors.” It is
a
p
hy
s
i
o
l

o
gi
ca
l
state
i
nw
hi
c
hi
nsects can surv
i
ve c
y
c
li
c, usua
lly l
on
g
,
p
er
i
o
d
so
f
a
d

vers
e
c
on
di
t
i
ons, unsu
i
te
d
to
g
rowt
h
an
d
re
p
ro
d
uct
i
on,
i
nc
l
u
di
n

g high
summer or
l
ow w
i
nte
r
temperatures,
d
roug
h
t, an
d
a
b
sence o
ff
oo
d
.Inot
h
er wor
d
s,
i
t
i
nc
l
u

d
es
b
ot
h hib
ernat
i
on
(overwintering) and estivation (summer dormancy). Insects enter diapause usually some
time in advance of the adverse conditions and terminate diapause after the condition
s
h
ave en
d
e
d
.Inot
h
er wor
d
s, natura
l
se
l
ect
i
on
h
as
f

avore
d
t
h
e
d
eve
l
o
p
ment o
f
asa
f
et
y
mar
gi
na
g
a
i
nst
p
remature
ly
unseasona
l
con
di

t
i
ons. Furt
h
ermore, t
h
e
f
actor t
h
at
l
ea
d
stot
he
i
n
d
uct
i
on o
fdi
apause (most o
f
ten p
h
otoper
i
o

d
)
i
s not
i
n
i
tse
lf
an a
d
verse con
di
t
i
on. T
h
us
,
diapause differs markedly from quiescence, which is a temporary form of dormancy, usually
induced directly by the arrival of adverse conditions.
O
ccurrence and Nature. D
i
a
p
ause ma
y
occur at an
y

sta
g
eo
f
t
h
e
lif
e
hi
stor
y
,e
gg,
l
arva,
p
u
p
a, or a
d
u
l
t, t
h
ou
gh
t
hi
s sta

g
e
i
s usua
lly
s
p
ec
i
es-s
p
ec
i
fic. On
ly
rare
ly d
oes
di
a
p
ause
o
ccur at more t
h
an one stage
i
nt
h
e

lif
e
hi
story o
f
a spec
i
es. Suc
hi
s typ
i
ca
ll
yt
h
e case
in
species that require 2 or more years in which to complete their development. For example,
in the cockroac
h
Ectobius la
pp
onicu
s
,
which has a 2-
y
ear life histor
y
, the first winter i

s
p
asse
d
as a
di
a
p
aus
i
n
g
e
gg
,t
h
e secon
d
as a
q
u
i
escent secon
d
-ort
hi
r
d
-
i

nstar
l
arvaorasa
di
a
p
aus
i
n
gf
ourt
h
-
i
nstar
l
arva.
Ant
i
c
i
pat
i
on o
f
t
h
e arr
i
va

l
o
f
a
d
verse con
di
t
i
ons means t
h
at t
h
eenv
i
ronmenta
l
st
i
mu
li
that induce diapause must exert their influence at an earlier stage in development. Thus,
egg diapause is the result of stimuli that affect the parental generation. These stimuli act on
669
THE
A
BI
O
TI
C

ENVIRONMEN
T
t
he female parent either in the adult stage or, more often, during her embryonic or larval
d
evelo
p
ment. I
n
B
ombyx mor
i
,
for exam
p
le, the da
y
len
g
th ex
p
erienced b
y
develo
p
in
g
f
ema
l

eem
b
r
y
os
d
eterm
i
nes w
h
et
h
er or not t
h
ese
i
nsects w
ill l
a
y
e
gg
st
h
at enter
di
a
p
ause.
S

p
ec
i
fica
lly
,ex
p
osure o
f
em
b
r
y
os to
l
on
gd
a
yl
en
g
t
h
s resu
l
ts
i
n
f
ema

l
es t
h
at
l
a
ydi
a
p
aus
i
n
g
e
ggs, and vice versa. Fo
r
B. mori good evidence exists for the production of a diapause
h
ormone by females exposed during embryogenesis to long-day conditions. This hormone
,
s
y
nthesized in the subeso
p
ha
g
eal
g
an
g

lion, has as its tar
g
et or
g
an the ovar
y
, which is cause
d
t
o
p
ro
d
uce
di
a
p
ause e
gg
s. W
h
et
h
er t
hi
ssc
h
eme
i
sa

ppli
ca
bl
etot
h
e
i
n
d
uct
i
on o
f
e
gg di
a
p
ause
i
not
h
er spec
i
es
i
s not
k
nown
.
Diapause may occur at any larval stage, though the instar in which it is present is usually

characteristic fora species. In many species it occurs in the final instar and, upon termination,
i
s immediatel
y
followed b
yp
u
p
ation. In this situation it is referred to as
p
re
p
u
p
al dia
p
ause
.
I
nt
h
e
i
n
d
uct
i
on o
fl
arva

ldi
a
p
ause env
i
ronmenta
l
st
i
mu
li
norma
lly
exert t
h
e
i
r
i
n
fl
uence a
t
an ear
li
er
l
arva
l
sta

g
e, t
h
ou
gh
s
p
ec
i
es are
k
nown
i
nw
hi
c
h
t
h
eenv
i
ronmenta
l
st
i
mu
l
us
is
gi

ven
i
nt
h
e egg stage or
d
ur
i
ng t
h
e prev
i
ous generat
i
on. For examp
l
e,
i
nt
h
ep
i
n
kb
o
ll
worm
,
P
ectinop

h
ora
g
oss
y
pie
lla
, the photoperiod experienced by the eggs, as well as that during
larval life, is im
p
ortant in determinin
g
whether or not
p
re
p
u
p
al dia
p
ause occurs. I
n
N
asoni
a
vi
tr
i
penn
is

,
a
p
aras
i
t
i
c
hy
meno
p
teran,
i
n
d
uct
i
on o
fl
arva
ldi
a
p
ause
i
s
d
e
p
en

d
ent on t
h
ea
ge
of
t
h
e
f
ema
l
e
p
arent at ov
ip
os
i
t
i
on, as we
ll
as on t
h
e
ph
oto
p
er
i

o
d
an
d
tem
p
erature to w
hi
c
h
s
h
e
i
s expose
d
ear
l
y
i
na
d
u
l
t
lif
e.
The pupa is the stage in which a large number of species enter diapause. The environ-
m
ental signal that induces diapause is generally given during larval development, though

f
or some s
p
ec
i
es t
h
e
i
n
fl
uence
i
s exerte
di
nt
h
e
p
arenta
lg
enerat
i
on. In t
h
eC
hi
nese oa
k
s

ilk
worm
,
Antheraea pernyi,
f
or exam
pl
e, t
h
e
l
ast two
l
arva
li
nstars are sens
i
t
i
ve to
ph
o-
t
oper
i
o
d
,w
h
ereas

i
nt
h
e
h
orn
fl
y
,
Haemato
b
ia irritan
s
, pupa
ldi
apause resu
l
ts w
h
en t
h
e
female parent has been exposed to short day lengths
.
Diapause may also occur in adult insects when it is known as reproductive diapause
.
E
ither
y
oun

g
adults or larval instars are the sta
g
es sensitive to environmental stimuli. Newl
y
e
mer
g
e
d
a
d
u
l
tCo
l
ora
d
o
p
otato
b
eet
l
es (Leptinotarsa decemlineata), w
h
en su
bj
ecte
d

t
o
s
h
ort
d
ay
l
engt
h
s, w
ill
enter
di
apause. In t
h
e
b
o
ll
weev
il,
A
nt
h
onomus
g
ran
d
i

s
,s
h
ort-
d
ay
conditions experienced by larvae will induce diapause in the adult stage.
Af
ew e
ff
xamples of intraspecific variation in the diapausing instar are known, especiall
y
i
ns
p
ecies that occu
py
a wide
g
eo
g
ra
p
hic ran
g
e. In the
p
itcher-
p
lant mos

q
uito,
W
yeomy
ia
smithii, nort
h
ern Nort
h
Amer
i
can
p
o
p
u
l
at
i
ons overw
i
nter as t
hi
r
d
-
i
nstar
l
arvae w

h
ereas
th
ose
i
nt
h
e sout
h
ern Un
i
te
d
States
di
a
p
ause one
i
nstar
l
ater.
M
ans
i
ng
h
(1971) su
bdi
v

id
e
ddi
apause an
d
t
h
e events surroun
di
ng
i
t
i
nto a num
b
er o
f
phases (Figure 22.4). This arrangement is convenient for a description of the sequence in
w
hich various
p
rocesses occur, thou
g
h it must be realized that these
p
hases normall
y
ar
e
n

ot c
l
ear
ly
se
p
arate
di
nt
i
me
b
ut mer
g
e
g
ra
d
ua
lly
w
i
t
h
one anot
h
er.Int
h
e
p

re
p
arator
yph
as
e
e
nv
i
ronmenta
lf
actors
i
n
d
uce c
h
an
g
es
i
n meta
b
o
li
c act
i
v
i
t

yi
n ant
i
c
ip
at
i
on o
fdi
a
p
ause, re
-
su
l
t
i
ng genera
ll
y
i
n accumu
l
at
i
on o
f
reserves, espec
i
a

ll
y
f
ats,
b
ut
i
nc
l
u
di
ng car
b
o
h
y
d
rate
s
and in some hibernating species cryoprotectants. During this phase the metabolic rate re
-
m
ains normal. Entry into the first phase (induction phase) of diapause is signaled by grea
t
d
ec
li
nes
i
n meta

b
o
li
c rate an
d
,
i
n
p
ostem
b
r
y
on
i
c sta
g
es, act
i
v
i
t
y
o
f
t
h
een
d
ocr

i
ne s
y
stem.
Fo
r
e
xam
pl
e,
i
n
di
a
p
aus
i
n
g
Hyalophora cecropi
a
,
a saturn
iid
mot
h
,t
h
e rate o
f

ox
yg
e
n
consumpt
i
on (a measure o
f
meta
b
o
li
c rate)
i
son
l
ya
b
out 2% o
f
t
h
e pre
di
apause va
l
ue;
i
n
larval European corn borers

(
O
strinia nu
b
i
l
a
l
is), which have a “weak” diapause (see below)
,
t
he rate of oxygen consumption falls to about one-quarter of the prediapause level. In the
6
70
CHAPTER
22
F
IGURE 22.4. P
h
ases
b
e
f
ore,
d
ur
i
ng, an
d
a

f
ter
di
apause
i
n overw
i
nter
i
ng
i
nsects. Pro
b
a
bl
e (so
lid
arrows)
an
dp
oss
ibl
e(
b
ro
k
en arrows) re
l
at
i

ons
hip
s
b
etween t
h
eenv
i
ronment, en
d
ocr
i
ne s
y
stem, an
d
t
h
evar
i
ous
ph
ase
s
are indicated. [From A. Mansin
g
h, 1971, Ph
y
siolo
g

ical classification of dormancies in insects
,
C
an. Entomol
.
1
0
3
:983–1009. By perm
i
ss
i
on o
f
t
h
e Entomo
l
og
i
ca
l
Soc
i
ety o
f
Cana
d
a.]
i

n
d
uct
i
on
ph
ase cont
i
nue
dp
ro
d
uct
i
on o
f
certa
i
n reserves, nota
bly
cr
y
o
p
rotectants
i
n over
-
wi
nter

i
n
g
s
p
ec
i
es,
p
ro
b
a
bly
occurs. W
h
at causes t
h
e
d
ec
li
ne
i
n meta
b
o
li
c rate assoc
i
ate

d
wi
t
h
t
h
e
b
eg
i
nn
i
ng o
fdi
apause
i
s uncerta
i
n. It may
b
ere
l
ate
d
to t
h
e cont
i
nue
d

e
ff
ects o
f
en-
v
ironmental stimuli, or it may result from the changed metabolism of an insect. Collectively
,
the behavioral and physiological changes that occur during the preparatory and inductio
n
p
hases make u
p
the so-called “dia
p
ause s
y
ndrome.” The refractor
yp
hase (
p
hase of dia-
p
ause
d
eve
l
o
p
ment), w

hi
c
hf
o
ll
ows
i
n
d
uct
i
on,
i
s
p
er
h
a
p
st
h
e
l
east un
d
erstoo
d
as
p
ect o

f
t
h
e
di
apause con
di
t
i
on. Or
i
g
i
na
ll
y,
i
t was propose
d
t
h
at
f
or overw
i
nter
i
ng
i
nsects

di
apause
d
e-
v
elopment would occur only during a period of exposure to low temperature. Such chillin
g
w
as
t
hought to be necessary for breakdown of the diapause-inducing or growth-inhibiting
substances
p
roduced earlier, or for reactivation of s
p
ecific s
y
stems (e.
g
., the endocrin
e
s
y
stem)
i
m
p
ortant
i
n

p
ost
di
a
p
ause
d
eve
l
o
p
ment. Tau
b
er
et al.
(
198
6
)an
d
Ho
d
e
k
(2002)
summar
i
ze
d
t

h
eev
id
ence t
h
at,
i
n
f
act, no suc
h
c
hilli
ng
i
s requ
i
re
d
; rat
h
er, t
h
ere
f
ractor
y
p
hase, like other phases of diapause, is maintained as a result of species-specific tempera
-

ture and/or photoperiod requirements. Of course, under natural conditions, species may b
e
sub
j
ect to low winter tem
p
eratures, but these serve onl
y
to
p
revent
p
remature develo
p
ment,
to
p
revent
b
rea
kd
own o
f
meta
b
o
li
tes
i
m

p
ortant
i
nco
ld
-
h
ar
di
ness an
d
to s
y
nc
h
ron
i
ze
p
ost-
di
a
p
ause
d
eve
l
o
p
ment. T

h
ere
f
ractor
yph
ase
i
s
f
o
ll
owe
dby
t
h
e act
i
vate
dph
ase, a
p
er
i
o
d
in which insects are capable of terminating diapause but do not do so because of prevail
-
ing environmental conditions (especially low temperature). Certain authors (e.g., Hodek,
2
002) consider that once insects reach this sta

g
e, when their dormanc
y
is (often) sim
p
l
y
tem
p
erature-
d
e
p
en
d
ent, t
h
e
y
must
b
e cons
id
ere
d
as
b
e
i
n

gq
u
i
escent, t
h
at
i
s, no
l
on
g
er
in
di
a
p
ause. Mans
i
n
gh
(1971),
h
owev er,
p
o
i
nte
d
out t
h

at, a
l
t
h
ou
gh i
nsects
i
nt
hi
s
ph
ase are
c
apa
bl
eo
f
cont
i
nue
dd
eve
l
opment, severa
l
aspects o
f
t
h

e
i
rp
h
ys
i
o
l
ogy are s
i
m
il
ar to t
h
ose o
f
the refractory phase, for example, the greatly depressed respiratory rate and presence of cry
-
op
rotectants. He believed therefore that activated insects should be considered to be still in
6
71
THE
A
BI
O
TI
C
ENVIR
O

NMEN
T
d
iapause. In Mansingh’s scheme the final phase of diapause is the termination phase, whic
h
occurs when environmental conditions become favorable for develo
p
ment. In this
p
hase the
m
eta
b
o
li
c rate returns to norma
l
,t
h
een
d
ocr
i
ne s
y
stem once more
b
ecomes act
i
ve,

b
o
dy
ti
ssues a
g
a
i
n
b
ecome ca
p
a
bl
eo
f
nuc
l
e
i
cac
id
an
dp
rote
i
ns
y
nt
h

es
i
s, an
d
an
y
cr
y
o
p
rotectant
s
present gradually disappear. As a result of these changes postdiapause development can
b
egin
.
I
n view of the var
y
in
g
de
g
rees of severit
y
of climatic conditions that insects in different
g
eo
g
ra

phi
cre
gi
ons ma
y
encounter,
i
t
i
s
p
er
h
a
p
s not sur
p
r
i
s
i
n
g
to fin
d
t
h
at t
h
e

i
ntens
i
t
y
(d
urat
i
on an
d
sta
bili
ty) o
fdi
apause var
i
es. T
hi
svar
i
a
bili
ty, w
hi
c
hi
s
b
ot
hi

nterspec
i
fic
and intraspecific, is manifest as a broad spectrum of dormancy that ranges from a stat
e
virtually indistinguishable from quiescence (“weak” or “shallow” diapause) to one of grea
t
stabilit
y
(“stron
g
” or “intense” dia
p
ause) in which an insect can resist extremel
y
unfavorabl
e
con
di
t
i
ons. In eac
h
s
i
tuat
i
on t
h
e stren

g
t
h
o
fdi
a
p
ause
i
s
p
rec
i
se
ly
a
dj
uste
d
t
h
rou
gh
natura
l
se
l
ect
i
on to

p
rov
id
ean
i
nsect w
i
t
h
a
d
e
q
uate
p
rotect
i
on a
g
a
i
nst t
h
ea
d
verse con
di
t
i
ons

,
yet to cont
i
nue growt
h
an
d
repro
d
uct
i
on as soon as an amena
bl
ec
li
mate returns. Broa
dl
y
speaking, insects from less extreme climates show weak diapause [called oligopause b
y
Mansin
g
h (1971)], in which develo
p
ment ma
y
not be com
p
letel
y

su
pp
ressed; the insects
m
a
y
cont
i
nue to
g
row s
l
ow
ly
(an
d
even mo
l
t) an
df
ee
d
w
h
en con
di
t
i
ons
p

erm
i
t
d
ur
i
n
g
th
e
p
er
i
o
d
o
fg
enera
lly
a
d
verse c
li
mate. In wea
kdi
a
p
ause t
h
e

i
n
d
uct
i
on
ph
ase
i
sre
l
at
i
ve
ly
s
h
ort, s
i
nce t
h
e
bi
oc
h
em
i
ca
l
a

dj
ustments t
h
at an
i
nsect ma
k
es
i
nor
d
er to cope w
i
t
h
t
h
e
adverse conditions are relatively simple. As a corollary of this, insects that overwinter in
w
eak diapause are not, for example, very cold-tolerant. The refractory phase is short so
th
at t
h
e act
i
vate
dph
ase
i

s entere
d
re
l
at
i
ve
ly
soon a
f
ter
di
a
p
ause
h
as
b
e
g
un, an
ddi
a
p
ause
i
s
q
u
i

c
kly
term
i
nate
d
w
h
en env
i
ronmenta
l
con
di
t
i
ons return to norma
l
. Converse
ly
,
i
n stron
g
di
apause, w
hi
c
hi
st

h
eru
l
e
i
n
i
nsects
f
rom severe c
li
mates, t
h
ere
i
sa
l
engt
h
y
i
n
d
uct
i
o
n
phase, after which development is fully suppressed. The refractory phase usually lasts for
several weeks or months, and the activated phase usually does not begin until diapaus
e

i
s more than half over. The termination
p
hase is relativel
y
slow, normall
y
s
p
annin
g
2or
3
wee
k
sa
f
ter t
h
e return o
f
su
i
ta
bl
ec
li
mat
i
c con

di
t
i
ons. Fre
q
uent
ly i
nsects t
h
at overw
i
nte
r
i
n strong
di
apause are very co
ld
-
h
ar
d
y.
Diapause was formerly subdivided into facultative and obligate diapause. Facultativ
e
d
iapause described the environmentally controlled diapause of bivoltine and multivoltine
s
p
ecies (havin

g
two or more
g
enerations
p
er
y
ear) in which the members of certain
g
enera-
ti
ons
h
a
d
no
di
a
p
ause
i
nt
h
e
i
r
lif
e
hi
stor

y
.O
blig
ate
di
a
p
ause re
f
erre
d
to t
h
e
di
a
p
ause
f
oun
d
i
nun
i
vo
l
t
i
ne s
p

ec
i
es (t
h
ose w
i
t
h
one
g
enerat
i
on
p
er
y
ear)
i
nw
hi
c
h
ever
y
mem
b
er o
f
t
he

spec
i
es un
d
ergoes
di
apause. It was
i
ncorrect
l
y assume
d
t
h
at
i
nun
i
vo
l
t
i
ne spec
i
es
di
apaus
e
was
not induced by environmental factors. However, experimental work on a number of

u
nivoltine s
p
ecies has revealed that in these s
p
ecies dia
p
ause is environmentall
y
controlled
.
F
urt
h
er stu
dy
ma
y
we
ll d
emonstrate t
h
at t
hi
s
i
sa
l
wa
y

st
h
e case an
d
ren
d
er
i
nva
lid
t
he
di
st
i
nct
i
on
b
etween o
blig
ate an
df
acu
l
tat
i
ve
di
a

p
ause
.
Induction, Maintenance, and Termination.
V
arious factors may influence the
course of dia
p
ause. Photo
p
eriod is es
p
eciall
y
im
p
ortant in the induction of dia
p
ause, thou
g
h
am
bi
ent tem
p
eratures,
p
o
p
u

l
at
i
on
d
ens
i
t
y
,an
ddi
et
d
ur
i
n
g
t
h
e
p
re
p
arator
y
an
di
n
d
uct

i
on
ph
ases ma
yi
n
fl
uence t
h
e
i
nc
id
ence (
p
ro
p
ort
i
on o
fi
n
di
v
id
ua
l
s enter
i
n

gdi
a
p
ause) an
di
n
-
t
ens
i
ty o
fd
ormancy. For many spec
i
es p
h
otoper
i
o
di
sa
l
so
i
mportant, t
h
oug
h
temperature
plays an increasing role, either alone or in combination with photoperiod, in diapaus

e
m
aintenance. Exam
p
les of both hibernatin
g
and estivatin
g
s
p
ecies that re
q
uire a s
p
ecific
ph
oto
p
er
i
o
d
to term
i
nate
di
a
p
ause are a
l

so
k
nown.
6
7
2
CHAPTER
22
T
emperature and moisture have also been suggested as key factors in the termination
o
f dia
p
ause, es
p
eciall
y
for some overwinterin
g
forms. However, it is often unclear whether
t
h
ese
f
actors are serv
i
n
g
as to
k

en st
i
mu
li f
or term
i
nat
i
n
gdi
a
p
ause or are ena
bli
n
gp
ost
di-
a
p
ause
d
eve
l
o
p
ment to
b
e
gi

n (Den
li
n
g
er, 198
6
;Tau
b
e
r
et a
l
.
,
198
6
). Accor
di
n
g
to Ho
d
e
k
(2002) and others, diapause typically terminates naturally simply by the passage of time;
that is, no specific temperature or moisture stimulus is required and any effects of thes
e
f
actors is exerted on the
q

uiescent
p
hase that follows dia
p
ause
.
In contrast to c
i
rca
di
an c
l
oc
k
s
f
or w
hi
c
h,
as note
d
ear
li
er
,
t
h
ere
i

s now a reasona
ble
un
d
erstan
di
ng o
f
t
h
e
i
r mec
h
an
i
sm, t
h
ep
h
otoper
i
o
di
cc
l
oc
k
t
h

at regu
l
ates
i
nsect seasona
li
t
y
remains largely a “black box.” Despite extensive study no single hypothesis predominates
;
rather, a series of complex models have been proposed, details of which are beyond the scope
o
f this text. Most of the models incor
p
orate two interde
p
endent com
p
onents: a circadian-
t
yp
ec
l
oc
k
s
y
stem t
h
at measures t

h
e num
b
er o
fh
ours o
f ligh
t (or
d
ar
k
ness)
i
n eac
hd
a
y,
an
d
a counter t
h
at sums t
h
e num
b
er o
f
c
y
c

l
es. A
dj
ustments are ma
d
e
f
or var
i
at
i
ons
in
temperature,
l
at
i
tu
d
e,
f
oo
d
, etc. T
h
e
i
n
f
ormat

i
on gat
h
ere
di
s store
di
n a “memory
li
n
k
” unt
il
a “critical value” is reached, at which point an effector (e.g., the neuroendocrine system)
is activated. For further information, refer to Takeda and Sko
p
ik (1997), Vaz Nunes and
S
aun
d
ers (1999), Tau
b
er an
d
K
y
r
i
acou (2001), an
d

Saun
d
ers (2002).
Fo
rt
h
e
g
reat ma
j
or
i
t
y
o
fi
nsects t
h
at ex
hibi
ta
ph
oto
p
er
i
o
di
ca
lly i

n
d
uce
ddi
a
p
ause
i
t
i
s
t
h
ea
b
so
l
ute
d
ay
l
engt
h
t
h
at
i
scr
i
t

i
ca
l
rat
h
er t
h
an
d
a
il
yc
h
anges
i
n
d
ay
l
engt
h
. Most
i
nsects
s
tudied to date show a long-day response to photoperiod (Figure 22.
5
A). That is, whe
n
reared under long-day conditions, they show continuous development, whereas at short da

y
l
en
g
t
h
s
di
a
p
ause
i
s
i
n
d
uce
d
. Between t
h
ese extremes
i
sacr
i
t
i
ca
ld
a
yl

en
g
t
h
at w
hi
c
h
t
h
e
i
nc
id
ence o
fdi
a
p
ause c
h
an
g
es a
b
ru
p
t
ly
. Exam
pl

es o
fi
nsects t
h
at s
h
ow a
l
on
g
-
d
a
y
res
p
onse
are t
h
eCo
l
ora
d
o potato
b
eet
l
e, L.
d
ecem

l
ineat
a
,an
d
t
h
ep
i
n
kb
o
ll
worm
,
P
.
g
oss
y
pie
lla
.
I
n
FI
GU
RE 22.5. D
iff
erent t

yp
es o
fdi
a
p
ause
incidence-da
y
len
g
th relationshi
p
s in insects. (A)
L
ong-
d
ay; (B) s
h
ort-
d
ay; (C) s
h
ort-
d
ay-
l
ong-
d
ay
;

a
n
d
(D)
l
on
g
-
d
a
y
-s
h
ort-
d
a
y
.T
h
e
h
atc
h
e
dli
ne
in
F
igure 22.5A indicates that in some long-day
s

pec
i
es
di
apause
i
nc
id
ence
i
s
l
ess t
h
an 100% at very
sh
ort
d
a
yl
en
g
t
h
s. [From S. D. Bec
k
,19
6
8,
I

nsect
P
hoto
p
eriodism.
B
y permission of Academic Press,
Inc., an
d
t
h
e aut
h
or.
]
6
73
THE
A
BI
O
TI
C
ENVIR
O
NMEN
T
F
IGURE 22.6.
E

ffect of photoperiod on di
-
apause
i
nc
id
ence
in
A
cronycta rumicis
(
Lep-
ido
p
tera)
p
o
p
ulations from different norther
n
latitudes.
[
From S. D. Beck, 1968, In
s
ect Pho
-
t
operio
d
ism.

B
y perm
i
ss
i
on o
f
Aca
d
em
i
c Press,
Inc., and the author.
]
a num
b
er o
f
spec
i
es,
i
nc
l
u
di
ng t
h
es
ilk

worm, Bom
by
x mori,
di
apause
i
s
i
n
d
uce
d
w
h
en t
h
e
d
ay length is long, while at short day lengths development is continuous. Such insects are
said to show a short-da
y
res
p
onse (Fi
g
ure 22.5B). The Euro
p
ean corn borer,
O
. nubilali

s
,
an
d
t
h
e
i
m
p
orte
d
ca
bb
a
g
e worm,
P
ieris brassica
e
,h
av
ea
s
h
ort-
d
a
y
-

l
on
g
-
d
a
y
res
p
onse
t
o
ph
oto
p
er
i
o
d
;t
h
at
i
s, t
h
e
i
nc
id
ence o

fdi
a
p
ause
i
s
l
ow at s
h
ort an
dl
on
gd
a
yl
en
g
t
h
s
,
b
ut
h
igh at intermediate day lengths (14–16 hours of light per day) (Figure 22.
5
C). Th
e
e
cological significance of such a response is unclear, since under natural conditions, insects

w
ould already be hibernating when the day length was short. A few northern species of
L
e
p
ido
p
tera behave in the o
pp
osite manner, namel
y
, show a lon
g
-da
y
-short-da
y
res
p
onse
t
o
p
hoto
p
eriod (Fi
g
ure 22.5D). All
p
hoto

p
eriods exce
p
t those with 16–20 hours of li
g
ht
p
er
d
ay
i
n
d
uce
di
apause. Aga
i
n,
h
owev er, t
h
e eco
l
og
i
ca
l
va
l
ue o

f
suc
h
a response
i
s uncerta
i
n
.
The precise value of the critical day length for a species varies with latitude
(
Figure 22.6). For example, the sorrel dagger moth,
A
cronycta rumici
s
, studied in Russia by
Danilevskii (1961), is a lon
g
-da
y
insect which, near Lenin
g
rad (latitude about 6
0
◦
N
)
,
h
as a

c
r
i
t
i
ca
ld
a
yl
en
g
t
h
o
f
a
b
out 19
h
ours. In more sout
h
er
ly p
o
p
u
l
at
i
ons t

h
ecr
i
t
i
ca
ld
a
yl
en
g
t
h
i
s gradually reduced and is, for example, only 1
5
hours on the Black Sea coast (4
3
◦
N
).
I
n the dragonfly Anax im
p
erator
a
nd perhaps a few other insects, diapause is induced by
d
aily changes in day length rather than by absolute number of hours of light per day
.

A
n
ax
l
arvae that have entered the final instar b
y
the be
g
innin
g
of June are able to metamor
p
hos
e
th
e same
y
ear. T
h
ose t
h
at reac
h
t
h
e fina
li
nstar a
f
ter t

hi
s
d
ate enter
di
a
p
ause an
dd
o not
e
merge unt
il
t
h
e
f
o
ll
ow
i
ng spr
i
ng. It seems t
h
at
l
arvae are a
bl
eto

d
eterm
i
ne t
h
e extent
b
y
w
hich the day length increases. When the daily increment is 2 minutes or more per day
l
arvae can develop directly, whereas at smaller increases or decreases in day length diapause
i
s induced
(
Corbet, 1963
)
.
Tem
p
erature ma
yp
ro
f
oun
dly
mo
dify
or overru
l

et
h
e norma
l
e
ff
ect o
fph
oto
p
er
i
o
d
o
n
di
apause
i
n
d
uct
i
on. For examp
l
e, t
h
ecr
i
t

i
ca
l
p
h
otoper
i
o
dd
epen
d
sont
h
e part
i
cu
l
ar
(
constant) temperature at which insects are maintained: in A. rumici
s
a5
◦
C difference in
t
emperature results in a 1-hour difference in the critical day length. At extreme value
s
t
he effects of tem
p

erature ma
y
overcome those of
p
hoto
p
eriod with reference to induction
of di
a
p
ause. In
l
on
g
-
d
a
yi
nsects ex
p
osure to constant
high
tem
p
erature ma
y
com
pl
ete
ly

p
revent
di
a
p
ause
i
n
d
uct
i
on re
g
ar
dl
ess o
fph
oto
p
er
i
o
d
. Converse
ly
,
i
ns
h
ort-

d
a
yi
nsects
high
t
emperature induces diapause, even under long-day conditions.
I
n nature temperatures normally fluctuate daily about a mean value. This daily fluctu
-
ation (thermo
p
eriod) also ma
y
modif
y
the influence of
p
hoto
p
eriod accordin
g
to whether
6
74
CHAPTER
22
o
r not it is in phase with the light-dark cycle. For example, i
n

A. rumici
s
t
he inci
d
ence o
f
dia
p
ause is increased b
y
low ni
g
httime tem
p
eratures and vice versa, thou
g
hatver
y
lon
g
d
a
yl
en
g
t
h
s (18
h

ours or more) tem
p
erature
h
as
li
tt
l
ee
ff
ect.
In most spec
i
es stu
di
e
ddi
et
i
n
fl
uences t
h
e
i
n
d
uct
i
on o

fdi
apause on
l
ys
li
g
h
t
l
y or not
at all. In P.
g
oss
y
pie
ll
a
,
for example, the incidence of diapause induction may be increased
by feeding the larvae on cotton seeds whose water content is low and/or oil content high,
p
rovided that the da
y
len
g
th is not much
g
reater than the critical value. Host-
p
lant maturit

y
c
an
b
e corre
l
ate
d
w
i
t
h
t
h
e onset o
fdi
a
p
ause
i
n a num
b
er o
f
s
p
ec
i
es t
h

ou
gh
t
h
ec
h
em
i
ca
lb
as
is
f
or t
hi
s rema
i
ns un
k
nown. For some pre
d
aceous spec
i
es (e.g., t
h
e convergent
l
a
d
y

b
eet
l
e
,
H
ippo
d
amia conver
g
ens), prey density is inversely correlatedwith the incidenceof diapause.
F
or
m
ost insects termination of hibernation or estivation is not under photoperiodic
c
ontrol but occurs, under natural conditions, with the return of suitable tem
p
eratures for
d
eve
l
o
p
ment. Ina
f
ew s
p
ec
i

es,
h
owev er, ex
p
osure toa
pp
ro
p
r
i
ate
ph
oto
p
er
i
o
d
sw
ill
term
i
nat
e
di
a
p
ause. For exam
pl
e,

i
na
d
u
lt
Leptinotarsa
d
ecem
l
ineat
a
a
n
dp
u
p
ae o
f
H
. cecrop
ia
a
n
d
P
.
g
oss
y
pie

lla
l
ong-
d
ay con
di
t
i
ons term
i
nate
di
apause. Converse
l
y,
i
n some
L
imne
ph
i
l
us
species (Trichoptera) that estivate as adults, diapause is ended by short day lengths
.
In some s
p
ecies, es
p
eciall

y
those that overwinter in the e
gg
sta
g
eorina
p
artiall
y
d
e
hyd
rate
d
con
di
t
i
on, contact w
i
t
h liq
u
id
water
i
s necessar
yf
or cont
i

nue
d
(
i
.e.,
p
ost
di
a
-
p
ause)
d
eve
l
o
p
ment an
d
act
i
v
i
t
y
.In
di
a
p
aus

i
n
gl
arvae o
f
O
.nu
b
i
l
a
l
is,
f
or exam
pl
e, w
h
ose
w
ater content falls by midwinter to about
5
0% of the prediapause level, uptake of wate
r
(by drinking) is essential before the insect can continue its development (Beck, 1980)
.
L
estes congener
,a
d

amselfly found on the Canadian prairies, oviposits in late summer in
d
r
y
,
d
ea
d
stems o
f
S
cirpus
(b
u
l
rus
h
). T
h
ee
gg
s
b
e
gi
nto
d
eve
l
o

pi
mme
di
ate
ly b
ut on
ly
t
o
t
h
een
d
o
f
anatre
p
s
i
san
d
t
h
en enter
di
a
p
ause. Cont
i
nue

dd
eve
l
o
p
ment
i
nt
h
es
p
r
i
n
g
w
ill
not
b
eg
i
n unt
il
t
h
e eggs are wette
d
, regar
dl
ess o

f
temperature. Wett
i
ng
i
sac
hi
eve
d
un
d
e
r
natural conditions as the level of the water rises during snow melt and also as a result o
f
w
ind action, which causes ice movements and subsequent breaking and submersion of the
p
lant stems (Sawch
y
n and Gillott, 1974a). As a result of such observations, it has fre
q
uentl
y
b
een c
l
a
i
me

d
t
h
at water
/
mo
i
sture
i
sa
f
actor t
h
at term
i
nates
di
a
p
ause. However, as note
d
a
b
ove,
i
n most
i
nstances
i
t

i
s unc
l
ear w
h
et
h
er t
hi
s
i
s correct or w
h
et
h
er
i
n
f
act
di
apaus
e
has already ended; in other words, the insect is now quiescent but requires water for it
s
c
ontinued development (Hodek, 2003).
4
. Water
W

ater, an essential constituent of living organisms, is obviously an important determi-
WW
nant of their distribution and abundance. Active or
g
anisms must retain within their bod
ya
c
erta
i
n
p
ro
p
ort
i
on o
f
water
i
nor
d
er
f
or meta
b
o
li
sm to occur norma
lly
.Dev

i
at
i
on
f
rom t
his
p
roport
i
on
f
or any
l
engt
h
o
f
t
i
me may resu
l
t
i
n
i
n
j
ury or
d

eat
h
. For some terrestr
i
a
li
nsects,
especially those from regions with striking dry and wet seasons, moisture may also serve
as a token stimulus for seasonally regulated processes (but see below)
.
4
.1. Terrestrial Insect
s
F
or terrestrial organisms, the problem generally is to reduce water loss from the body
,
w
hich occurs as a result of surface evaporation and during excretion of metabolic wastes.
S
urface eva
p
oration is es
p
eciall
y
im
p
ortant in small or
g
anisms, includin

g
insects whos
e
6
7
5
THE
A
BI
O
TI
C
ENVIR
O
NMEN
T
surface area is relatively large in relation to body volume. That insects have been able to
solve this
p
roblem is one of the main reasons for their success as a terrestrial
g
rou
p
. Not onl
y
d
o
i
nsects
g

enera
lly p
ossess a
highly i
m
p
ermea
bl
e cut
i
c
l
e(C
h
a
p
ter 11, Sect
i
on 4.2) an
d
various devices for reducin
g
water loss from the res
p
irator
y
s
y
stem (Cha
p

ter 1
5
, Section 3),
b
ut they also have an efficient method of excretion, that is, one that uses a minimum of water
for urine production (Chapter 18, Section 4.1). Such water loss as does occur is normally
m
ade u
p
b
y
drinkin
g
or from water in the food, thou
g
h active members of a few s
p
ecies
f
rom ver
yd
r
yh
a
bi
tats are a
bl
etota
k
eu

p
water
f
rom mo
i
st a
i
rs
h
ou
ld
t
h
eo
pp
ortun
i
t
y
ar
i
se
,
or use water pro
d
uce
di
n meta
b
o

li
sm.
As dormant insects are largely unable to acquire water from their surroundings, the
y
t
ypically have a “prevention is better than cure” strategy; that is, they use behavioral or
p
h
y
siolo
g
ical mechanisms to reduce water loss (Danks, 2000). Behavioral means includ
e
s
p
en
di
n
g
t
h
e
d
ormant
p
er
i
o
di
n cocoons,

i
nso
il
or
l
ea
fli
tter, un
d
er
b
ar
k
,an
di
n
g
rou
ps
(
e.
g
.,
l
a
dybi
r
db
eet
l

es). Exam
pl
es o
f phy
s
i
o
l
o
gi
ca
l
strate
gi
es are re
d
uc
i
n
g
t
h
es
i
ze o
f
t
he
sp
i

racu
l
ar open
i
ng,
i
ncreas
i
ng t
h
et
hi
c
k
ness o
f
t
h
e cut
i
c
l
e, espec
i
a
ll
yt
h
ewax
l

ayer, a
l
ter
i
ng
t
he composition of the wax to raise the transition temperature (Chapter 11, Section 4.2),
i
ncreasin
g
the osmotic
p
ressure of the hemol
y
m
p
hb
y
s
y
nthesizin
g
cr
y
o
p
rotectants, and b
y
s
ig

n
i
ficant
ly
re
d
uc
i
n
g
meta
b
o
li
c rate. Some
i
nsects, nevert
h
e
l
ess,
l
ose cons
id
era
bl
e
b
o
dy

w
ater
d
ur
i
n
gdi
a
p
ause, an
di
n
hib
ernat
i
n
g
s
p
ec
i
es t
hi
s
i
so
f
ten corre
l
ate

d
w
i
t
h
t
h
e
p
ro
d
uc-
ti
on o
f
cryoprotectants (Sect
i
on 2.4.1) (B
l
oc
k
, 199
6
). For examp
l
e, ye
ll
ow woo
ll
y

b
ear
caterpillars
(
D
iacrisia vir
g
inica) enter diapause as mature larvae weighing about 600 mg.
During diapause their weight falls to about 200 mg, mainly as a result of the loss of wa
-
t
er. However, t
h
e water
l
oss
i
sac
hi
eve
dbyd
ecreas
i
n
g
t
h
e
h
emo

ly
m
ph
vo
l
ume, ena
bli
n
g
i
ntrace
ll
u
l
ar water to
b
e
k
e
p
tata
phy
s
i
o
l
o
gi
ca
lly

su
i
ta
bl
e
l
eve
l.
Fo
r
e
st
i
vat
i
ng
i
nsects, espec
i
a
ll
yt
h
ose t
h
at
li
ve
i
n areas w

i
t
hdi
st
i
nct wet an
dd
r
y
seasons, moisture may act as an important stimulus for continued development and activity
,
i
n much the same manner as photoperiod and temperature regulate the seasonal ecology
of man
y
tem
p
erate s
p
ecies (Tauber
et al.
,
1998; Hodek, 2003). Thou
g
h there is currentl
y
a
l
ac
k

o
f
ev
id
ence
f
or t
h
e
i
m
p
ortance o
f
mo
i
sture as a seasona
l
re
g
u
l
ator, Tau
b
er
et al.
(
1998)
h
ypot

h
es
i
ze t
h
at mo
i
sture may a
ff
ect
lif
ecyc
l
es
i
nt
h
ree ways: (1)
i
t may serv
e
t
o induce, maintain, or terminate diapause; (2) it may be a developmental modulator, fo
r
e
xample, by controlling rates of growth, maturation, and reproduction, as well as feedin
g
and locomotion; and (3) It ma
y
be an im

p
ortant behavioral cue for such
p
rocesses as moltin
g
,
m
at
i
n
g
,an
d
e
gg l
a
yi
n
g
.
T
h
e
i
m
p
ortance o
f
water
i

s not restr
i
cte
d
to
p
ostem
b
r
y
on
i
c sta
g
es. Dur
i
n
g
em
b
r
y
o
g
en-
e
s
i
s, a
l

so, t
h
e correct proport
i
on o
f
water must
b
e present w
i
t
hi
nt
h
e egg. Aga
i
n, t
h
epr
i
mar
y
problem is to prevent water loss (unlike postembryonic stages of most species, eggs cannot
m
ove in search of water or into habitats where loss is reduced!
)
. To facilitate this a female
m
a
yl

a
y
e
gg
s
i
n
b
atc
h
es rat
h
er t
h
an s
i
n
gly
,ov
ip
os
i
t
i
namo
i
st me
di
um, an
d

surroun
d
t
h
e
egg
sw
i
t
hp
rotect
i
ve mater
i
a
l
(C
h
a
p
ter 19, Sect
i
on 7). In a
ddi
t
i
on, t
h
ee
gg

s
h
e
ll
(c
h
or
i
on)
i
s
hi
g
hl
y
i
mpermea
bl
e to water. As a resu
l
tt
h
eegg
i
s very res
i
stant to
d
es
i

ccat
i
on an
di
s
frequently the stage in which periods of drought are overcome. Moisture may also be an
i
mportant cue that triggers postdiapause embryonic development and hatching, as described
i
n Sect
i
on 3.2.3
.
I
nv
i
ew o
f
t
h
e
i
m
p
ortance o
f
water,
i
t
i

s not sur
p
r
i
s
i
n
g
to fin
d
t
h
at man
y
terrestr
i
a
l
i
nsects
b
e
h
ave
i
nac
h
aracter
i
st

i
c manner w
i
t
h
respect to mo
i
sture
i
nt
h
e surroun
di
ng a
i
ror
substrate. The response may have immediate survival value for the individual concerned
or may confer a long-term advantage on the individual and, ultimately, on the species. Th
e
6
7
6
CHAPTER
22
ability to recognize and respond to slight differences in relative humidity enables an insect
to move into a re
g
ion of
p
referred humidit

y
. Not onl
y
does this have immediate survival
v
a
l
ue,
b
ut
b
ecause ot
h
er
i
n
di
v
id
ua
l
so
f
t
h
es
p
ec
i
es w

ill
ten
d
to res
p
on
d
s
i
m
il
ar
ly i
tma
y
a
l
so
i
ncrease t
h
ec
h
ances
f
or
p
er
p
etuat

i
on o
f
t
h
es
p
ec
i
es. Some
i
nsects see
k
out s
i
tes w
i
t
h
a preferred humidity, in which to enter diapause. Though this behavior is of no immediate
v
alue to the insect, it increases the chances of survival of the dormant stage. Similarly,
f
emale
g
rassho
pp
ers about to ovi
p
osit di

g
“test holes” with their ovi
p
ositor to determin
e
t
h
emo
i
sture content (an
dp
ro
b
a
bly
ot
h
er
phy
s
i
ca
l
an
d
c
h
em
i
ca

lf
eatures) o
f
t
h
eso
il
.E
ggs
are norma
ll
y
l
a
id i
nmo
i
st so
il
,an
d
a
f
ema
l
e may reta
i
nt
h
e eggs

i
nt
h
eov
id
ucts
f
or som
e
time if she does not immediately find a suitable site. Again, this behavior has no immediat
e
v
alue to the female but certainly increases the eggs’ chances of survival
.
T
hus far, the discussion has em
p
hasized the harmful effects of too little water and th
e
mec
h
an
i
sms
by
w
hi
c
h
terrestr

i
a
li
nsects avo
id
t
hi
s
p
ro
bl
em. On occas
i
ons,
h
owever, too
muc
h
mo
i
sture ma
yb
ee
q
ua
lly d
etr
i
menta
l

to
i
nsects’ surv
i
va
l
.T
h
ee
ff
ects o
f
excess
i
ve
mo
i
sture may
b
e
di
rect (name
l
y, caus
i
ng
d
rown
i
ng)

b
ut more o
f
ten are
i
n
di
rect. For exam
-
p
le, insects that normally develop cold-hardiness partially as a result of dehydration ma
y
be less cold-hard
y
and therefore less ca
p
able of survivin
g
low tem
p
eratures of winter i
f
t
hi
s
h
as
b
een
p

rece
d
e
dby
a wet
f
a
ll
. Wet con
di
t
i
ons ma
y
a
l
so a
ff
ect a s
p
ec
i
es’
f
oo
d
su
pply.
H
owev er, t

h
e most
i
m
p
ortant wa
yi
nw
hi
c
h
excess
i
ve mo
i
sture a
ff
ects
i
nsect
p
o
p
u
l
at
i
ons
i
s

b
yst
i
mu
l
at
i
ng t
h
e
d
eve
l
opment an
d
sprea
d
o
f
pat
h
ogen
i
cm
i
croorgan
i
sms (
b
acter

i
a, proto
-
z
oa, fungi, and viruses). For example, in the summer of 1963 in Saskatchewan (Canada) th
e
w
eather was abnormally humid, with above-average rainfall in some areas of the province.
Th
ese con
di
t
i
ons a
pp
eare
did
ea
lf
or t
h
e
f
un
g
u
s
E
ntomophthora gryll
i

,
w
hi
c
h
un
d
erwent
a
wid
es
p
rea
d
e
pi
zoot
i
c, caus
i
n
g high
morta
li
t
yi
n
p
o
p

u
l
at
i
ons o
f
severa
l
s
p
ec
i
es o
fg
rass
h
o
p
-
p
ers, espec
i
a
ll
y Camnu
l
ape
ll
uci
da

,t
h
ec
l
ear-w
i
nge
d
grass
h
opper, an
d
to a
l
esser exten
t
Me
l
ano
pl
us
b
ivittatus
(
two-striped grasshopper) an
d
M.
p
ac
k

ar
d
ii
(
Packard’s grasshopper).
S
uch was the effect of the fungus on
C
.
p
ellucida that by the fall of 1963 its proportion in
the
g
rassho
pp
er s
p
ecies com
p
lex had fallen to 7% com
p
ared with 64% the
p
revious
y
ear
(P
i
c
kf

or
d
an
d
R
i
e
g
ert, 19
6
4).
Fi
na
ll
y, t
h
e
b
enefic
i
a
l
e
ff
ects o
f
snowont
h
e surv
i

va
l
o
fi
nsects must
b
e note
d
. Snow
is an excellent insulator and in extremely cold climates serves to reduce considerably th
e
rate of heat loss from the substrate. Thus, the substrate remains considerably warmer than
the air above the snow. For exam
p
le, with an air tem
p
erature of –30
◦
C
an
d
a snow
d
e
p
t
h
o
f
10 cm, t

h
e tem
p
erature o
f
so
il
a
b
out3cm
b
e
l
ow
i
ts sur
f
ace
i
sa
b
out –
9
◦
C.
In t
h
e
ab
sence o

f
snow t
h
eso
il
temperature at t
hi
s
d
ept
hi
son
l
ya
d
egree or two
hi
g
h
er t
h
a
n
that of the air. This means that species with only limited cold-hardiness may be able t
o
s
urvive the winter in cold climates provided that there is ample snow cover. In other words
,
because of snow a s
p

ecies ma
y
be able to extend its
g
eo
g
ra
p
hical ran
g
e into areas with low
w
i
nter tem
p
eratures. In Sas
k
atc
h
ewan,
f
or exam
pl
e, t
h
e
d
amse
lfli
e

s
L
estes dis
j
unctus
a
n
d
L
.un
g
uicu
l
atus
ov
e
rw
i
nter as e
gg
s(
i
n
di
a
p
ause)
l
a
id i

n emer
g
ent stems o
f
S
cirpus. T
he
eggs can tolerate exposure to temperatures as low as –2
0
◦
C
and remain viable. Below this
temperature mortality increases significantly (Sawchyn and Gillott, 1974b). At Saskatoon
,
where thisstud
y
was carried out, the
mean
tem
p
erature forJanuar
y
is, however, about –22
◦
C,
t
h
ou
gh
t

h
e tem
p
erature
f
re
q
uent
ly f
a
ll
swe
ll b
e
l
ow t
hi
sva
l
ue (t
h
e recor
dl
ow
b
e
i
n
g
a

b
out
–4
8
◦
C!). F
i
e
ld
co
ll
ect
i
on o
f
eggs t
h
roug
h
out t
h
ew
i
nter s
h
owe
d
t
h
at, w

h
ereas t
h
ev
i
a
bili
ty
o
f eggs from beneath the snow remained near 100%, no eggs collected from exposed stems
survived. Thus, the insulating effect of snow is essential to the survival of these species i
n
this re
g
ion of Canada. In addition, the snow cover ma
y
also
p
revent desiccation.
6
7
7
THE
A
BI
O
TI
C
ENVIR
O

NMEN
T
4.2. A
q
uatic Insects
The most important features of the surrounding medium that affect the distribution and
abundance of aquatic insects appear to be its temperature, oxygen content, ionic content
,
and rate of flow. The influence of tem
p
erature on develo
p
ment and activit
y
(throu
g
h its
eff
ect on ox
yg
en content)
h
as a
l
rea
dy b
een out
li
ne
di

n Sect
i
ons 2.1 an
d
2.2.
T
h
ea
bili
t
y
o
fi
nsects to re
g
u
l
ate
b
ot
h
t
h
e tota
li
on
i
c concentrat
i
on an

d
t
h
e
l
eve
l
o
f
i
n
di
v
id
ua
li
ons
i
nt
h
e
h
emo
l
ymp
hi
sama
j
or
d

eterm
i
nant o
f
t
h
e
i
r
di
str
ib
ut
i
on. Typ
i
ca
l
freshwater insects are restricted to waters of low ionic content because, although they are
ca
p
able ofexcretin
g
excess water thatenters their bod
y
osmoticall
y
, the
y
have nomechanism

f
or remov
i
n
g
excess
i
ons t
h
at enter t
h
e
b
o
dy
w
h
en t
h
e
i
nsect
i
s
i
nasa
li
ne me
di
um; t

h
a
t
i
s, t
h
e
y
cannot
p
ro
d
uce a
hyp
erosmot
i
cur
i
ne (C
h
a
p
ter 18, Sect
i
on 4.2). Furt
h
er, mem
b
ers
o

f
some spec
i
es may
b
e una
bl
etoco
l
on
i
ze some
f
res
h
water
h
a
bi
tats
b
ecause t
h
ese conta
i
n
certain ions such as Mg
2
+
a

nd Ca
2
+
in too high a concentration.
I
n contrast, members of man
y
s
p
ecies that normall
y
inhabit saline environments a
pp
ear
t
o
b
ea
bl
etore
g
u
l
ate t
h
e
i
r
h
emo

ly
m
ph
osmot
i
c
p
ressure an
di
on
i
c content over a w
id
e ran
g
e
of
externa
l
sa
l
t concentrat
i
ons. In ot
h
er wor
d
s, t
h
e

y
can
p
ro
d
uce
hyp
erosmot
i
cur
i
ne w
h
e
n
i
t
i
s necessary,
i
nasa
li
ne me
di
um, to excrete excess
i
ons, or
h
ypoosmot
i

cur
i
ne, w
h
en
in
fresh water, to remove excess water from the body (Chapter 18, Section 4.3). As they are
normally found only in saline habitats, it must be assumed that their distribution is governe
d
by
ot
h
er env
i
ronmenta
lf
actors.
T
h
e
i
nsect
f
auna o
f
an a
q
uat
i
c

h
a
bi
tat ma
yb
e corre
l
ate
d
w
i
t
h
t
h
es
p
ee
d
at w
hi
c
h
t
h
e
w
ater
i
smov

i
ng. Insects
i
nst
ill
or s
l
ow
l
ymov
i
ng water are not prevente
df
rom mov
i
ng,
f
or
e
xample, in search of food or to the surface for gaseous exchange. In contrast, rheophili
c
species (those that live in swiftly moving streams or rivers) have evolved structural, be-
havioral, and
p
h
y
siolo
g
ical ada
p

tations to survive in these habitats. Amon
g
the structura
l
a
d
a
p
tat
i
ons t
h
at ma
yb
e
f
oun
di
nr
h
eo
phili
c
i
nsects are
fl
atten
i
n
g

or stream
li
n
i
n
g
o
f
t
h
e
b
o
dy,
an
d
t
h
e
d
eve
l
opment o
ff
r
i
ct
i
on
di

scs or
h
y
d
rau
li
c suc
k
ers (Hynes, 1970a,
b
). F
l
atten
i
ng ma
y
t
ake on differing significance among species, though ultimately its function is to enable in
-
sects to avoid being washed downstream by the current. In members of some species, whic
h
live on ex
p
osed surfaces, flattenin
g
enables them to remain within the boundar
y
la
y
er, a

thi
n
l
a
y
er o
f
a
l
most stat
i
c water cover
i
n
g
t
h
esu
b
strate. For mem
b
ers o
f
most s
p
ec
i
es
fl
at-

t
en
i
ng
i
s assoc
i
ate
d
w
i
t
h
t
h
e
i
r crypt
i
c
h
a
bi
t, perm
i
tt
i
ng t
h
em to

li
ve un
d
er stones,
i
n crac
k
s
,
crevices, etc. Streamlining, too, is a modification mainly used by insects to avoid currents
by burrowing into the substrate, though members of a few streamlined species, for example
,
m
ost s
p
ecies o
f
B
aet
i
s
a
n
d
Centro
p
tilu
m
(
ma

y
flies), do live on ex
p
osed surfaces and ar
e
a
bl
etosw
i
ma
g
a
i
nst
q
u
i
te stron
g
currents (H
y
nes, 1970a,
b
)
.
T
h
ema
j
or

phy
s
i
o
l
o
gi
ca
l
a
d
a
p
tat
i
on o
f
r
h
eo
phili
cs
p
ec
i
es
i
sre
l
ate

d
to
g
as exc
h
an
g
e
.
Because o
f
t
h
e
d
anger o
fb
e
i
ng was
h
e
dd
ownstream,
i
nsects
i
nmov
i
ng water cannot come

t
o the surface to obtain oxygen; they rely on oxygen dissolved in the medium. Throug
h
ev
olution, members of rheo
p
hilic s
p
ecies have become ada
p
ted to a medium with hi
gh
o
x
yg
en content an
d
con
d
uct most or a
ll g
as exc
h
an
g
e
di
rect
ly
across t

h
e
b
o
dy
wa
ll
. Furt
h
er
,
th
e
yd
e
p
en
d
on t
h
e water current to renew t
h
eox
yg
en su
pply
at t
h
e
i

r
b
o
dy
sur
f
ace. As a
r
esu
l
t,
i
n many spec
i
es, g
ill
s,
if
present, are re
d
uce
d
,an
d
t
h
ea
bili
ty to vent
il

ate,
b
y
fl
app
i
n
g
t
he gills or undulating the abdomen, has been lost.
Their relative inability to move because of the current has been paralleled, in many
rh
eo
phili
c
i
nsects,
by
t
h
eevo
l
ut
i
on o
fd
ev
i
ces t
h

at ena
bl
et
h
em to o
b
ta
i
n
f
oo
dp
ass
i
ve
ly;
th
at
i
s, t
h
e
yd
e
p
en
d
on t
h
e current to

b
r
i
n
gf
oo
d
(es
p
ec
i
a
lly
m
i
croor
g
an
i
sms an
dd
etr
i
tus
)
6
78
CHAPTER
22
to them. These devices include the nets built by many trichopteran larvae, fringes of hairs

o
n the forele
g
s and/or mandibles of some larval Pleco
p
tera, the fans on the
p
remandibles of
bl
ac
kflyl
arvae, an
d
t
h
est
i
c
ky
str
i
n
g
so
f
sa
li
va
p
ro

d
uce
dby
t
h
ec
hi
ronom
id
Rheotanytarsu
s
(Hynes, 1970a,
b
)
.
An important factor in the distribution of aquatic insects, and one that is related to the
extent of water movement, is the substratum. Many species of stream insects are character-
isticall
y
associated with
p
articular t
yp
es of substratum. For some insects the si
g
nificance
of
t
hi
s assoc

i
at
i
on
i
s eas
ily
un
d
erstoo
d
. For exam
pl
e, water
p
enn
i
es [
l
arvae o
f
Pse
ph
en
id
ae
(Co
l
eoptera)],
f

oun
di
n
f
ast-mov
i
ng waters, requ
i
re
l
arg
i
s
h
roc
k
stow
hi
c
h
t
h
ey can
b
ecome
attached. Similarly, larval Blepharoceridae (Diptera) need smooth rocks, not covered with
silt or algal growth, to which to attach their suckers. And some Leuctridae (Plecoptera
)
re
q

uire
g
ravel of the correct texture in which to burrow.
5. Weathe
r
B
ecause of their wei
g
ht and relativel
y
lar
g
e surface area/volume ratio, insects ma
y
b
e
p
ro
f
oun
dly
a
ff
ecte
dby
weat
h
er, es
p
ec

i
a
lly by
tem
p
erature, w
i
n
d
,an
d
ra
i
n. Weat
h
er
i
sa
ma
j
or
f
actor
li
m
i
t
i
n
g

t
h
ea
b
un
d
ance o
f
man
yi
nsect s
p
ec
i
es, es
p
ec
i
a
lly
c
l
ose to t
h
ee
dg
eo
f
t
h

e
i
r range. Its e
ff
ect may
b
e
b
ot
hdi
rect an
di
n
di
rect. For examp
l
e,
b
ya
l
ter
i
ng t
h
e rate o
f
ev
aporation of water from the body surface wind may be important in the water relation
s
o

f the insect. Flight activity (whether or not flight occurs, the direction of movement, and
t
h
e
di
stance trave
l
e
d
)
i
sa
l
so
di
rect
ly
re
l
ate
d
to t
h
e stren
g
t
h
an
ddi
rect

i
on o
f
t
h
ew
i
n
d
.W
i
n
d
act
i
on ma
y
a
l
so exert
i
n
di
rect e
ff
ects on
i
nsects,
f
or exam

pl
e,
by
caus
i
n
g
eros
i
on o
f
so
il
or
snowsot
h
at t
h
e
i
nsects (or t
h
e
i
r eggs) are expose
d
to pre
d
ators, extremes o
f

temperature, or
desiccation. Temperature has both obvious direct effects on development rate (Section 2.1
)
and less easily quantified indirect effects, for example, on a species’ host plants, pathogens,
and
p
arasitoids, and is thus a ke
y
factor in insect
p
o
p
ulation d
y
namics. Rain
p
robabl
y
exerts
i
ts
i
n
fl
uence on most
i
nsect
p
o
p

u
l
at
i
ons on
ly i
n
di
rect
ly
, nota
bly by
a
ff
ect
i
n
g
t
h
eava
il
a
bili
t
y
an
d
qua
li

ty o
ff
oo
d
or t
h
e
i
nc
id
ence o
fdi
sease. However,
i
t can occas
i
ona
ll
y
h
ave spec
i
fic
,
direct effects. For example, through the formation of temporary pools it provides egg-layin
g
sites for some mosquitoes and it is an important factor in termination of larval diapause
f
or some s
p

ecies in semiarid, tro
p
ical climates. In other tro
p
ical s
p
ecies, for exam
p
le, the
d
esert
l
ocust
,
Schistocerca gregari
a
,w
hi
c
hh
as an a
d
u
l
t (re
p
ro
d
uct
i

ve)
di
a
p
ause t
h
rou
gh
t
h
e
d
r
y
season, t
h
e arr
i
va
l
o
f
ra
i
n serves as a cue
f
or co
p
u
l

at
i
on,
di
s
p
ersa
l
,an
d
ov
ip
os
i
t
i
on
(Den
li
nger, 198
6
).
T
hrough its effect on the flight activity of winged insects and because insects by virtu
e
o
f their wei
g
ht are easil
y

trans
p
orted on wind currents, wind is an im
p
ortant factor in
di
s
p
ersa
l
,t
h
e movement awa
yf
rom a crow
d
e
dh
a
bi
tat so t
h
at scatter
i
n
g
o
f
a
p

o
p
u
l
at
i
o
n
resu
l
ts. T
h
ou
gh
a
g
oo
dd
ea
l
o
fi
nsect
di
s
p
ersa
li
so
f

no o
b
v
i
ous
b
enefit,
f
or some s
p
ec
i
es t
h
e
di
spersa
li
sa
d
apt
i
ve, t
h
at
i
s, con
f
ers a
l

ong-term a
d
vantage on t
h
e spec
i
es
b
y trans
f
err
i
n
g
some adult members to new breeding sites. Because of its advantageous nature, physiolog
-
ical, structural, and behavioral features that facilitate adaptive dispersal (
=
m
igration) will
b
ecome fixe
di
na
p
o
p
u
l
at

i
on t
h
rou
gh
natura
l
se
l
ect
i
on.
5.1.
W
eather and Insect
A
bundance
To
i
llustrate the key role of weather, especially temperature, as a limiter of insect
p
o
p
ulations, it will be useful to refer to two s
p
ecific exam
p
les, both im
p
ortant forest

p
est
s