23
The Biotic En
v
ironment
1
. Intr
oduc
t
ion
T
his chapter will deal with the biotic environment of insects, which is composed of all other
or
g
anisms that affect insects’ abilit
y
to survive and multipl
y
. In other words, the interaction
s
of insects with other or
g
anisms (of the same and other species) will be discussed. Food i
s
th
e most o
b
v
i
ous an
di
m

p
ortant
bi
ot
i
c
f
actor, an
di
nsects are
i
nvo
l
ve
di
naw
id
es
p
ectrum
o
f
trop
hi
cre
l
at
i
ons
hi

ps w
i
t
h
ot
h
er organ
i
sms,
b
ot
hli
v
i
ng an
dd
ea
d
.Ast
h
ema
j
or
i
ty o
f
i
nsects
f
ee

d
on p
l
ant mater
i
a
li
n one
f
orm or anot
h
er, t
h
e
y
are
k
e
y
components
i
nt
h
e
fl
ow
of ener
gy
throu
g

h the ecos
y
stem. However, other interactions are known that, thou
g
h not
as easil
y
reco
g
nized as feedin
g
, are nonetheless important re
g
ulators of insect distribution
an
d
a
b
un
d
ance
.
2. Food and Tro
p
h
i
c Relat
i
onsh
ip

s
I
nsects have evolved diverse feedin
g
habits that allow them to exploit virtuall
y
ever
y
naturally occurring organic substance. Among their adaptations are specialized ingestiv
e
an
ddi
gest
i
ve systems, t
h
ea
bili
ty to
d
etox
if
yorp
h
ys
i
ca
ll
y avo
id

tox
i
ns pro
d
uce
db
yt
he
h
ost, mutua
li
st
i
cre
l
at
i
ons
hi
ps
b
etween t
h
e
i
nsect an
d
m
i
croor

g
an
i
sms, an
d lif
e-
hi
stor
y
strate
g
ies that result in temporal avoidance of resource-poor situations (includin
g
those
resultin
g
from interspecific competition) or times when the host’s toxins are abundant.
T
hus, insects participate in an array of trophic interactions as herbivores, predators, parasites,
paras
i
to
id
s,
d
etr
i
t
i
vores, an

d
prey
i
n
b
ot
h
terrestr
i
a
l
an
df
res
h
water ecosystems (F
i
gures 23.
1
an
d
23.2). Foo
d
may
b
ean
i
mportant
li
m

i
ter o
fi
nsect popu
l
at
i
on growt
h
;
i
t may a
l
so a
ff
ect
t
he distribution and the dispersal of species over time (Price, 1997)
.
2
.1. Quantitative As
p
ect
s
T
h
oug
h
t
h

e amount o
ff
oo
d
ava
il
a
bl
em
i
g
h
t
b
e cons
id
ere
d
as an
i
mportant regu
l
ator o
f
i
nsect a
b
un
d
ance,

i
t
h
as
b
een
f
oun
di
n natura
l
commun
i
t
i
es t
h
at popu
l
at
i
ons
d
o not norma
ll
y
u
se more t
h
an a sma

ll f
ract
i
on o
f
t
h
e tota
l
ava
il
a
bl
e
f
oo
d
.T
hi
s
i
spr
i
mar
ily b
ecause ot
h
er
6
91

6
9
2
CHAPTER
23
F
I
GU
RE 23.1.
A
n example of a food web in a terrestrial ecosystem, showing the importance of insects. [From
P.
W. Pr
i
ce, T
h
e concept o
f
t
h
e ecosystem,
i
n: Eco
l
ogica
l
Entomo
l
og
y

(C. B. Hu
ff
a
k
er an
d
R. L. Ra
bb
,e
d
s.)
.
C
op
y
r
igh
t

CC
1984
by
Jo
h
nW
il
e
y
an
d

Sons, Inc. Repr
i
nte
dby
perm
i
ss
i
on o
f
Jo
h
nW
il
e
y
an
d
Sons, Inc.]
c
omponents of the environment especiall
y
weather but includin
g
, for example, predators,
parasites, and pathogens, usually have a significant adverse effect on growth and reproduc
-
t
i
on. Ot

h
er
f
eatures o
fi
nsects may,
h
owever,
b
e
i
mportant
i
nt
hi
s regar
d
. Many spec
i
es
,
e
spec
i
a
ll
yp
l
ant
f

ee
d
ers, are po
l
yp
h
agous. T
h
us, w
h
en t
h
e pre
f
erre
df
oo
d
p
l
ant
i
s
i
n
li
m
-
i
ted quantit

y
, alternate choices can be used. Amon
g
endopter
yg
otes, larvae and adults of a
species ma
y
eat quite different kinds of food, and in some species such as mosquitoes the
f
ood of the adult female differs from that of the adult male
.
Two
si
tuat
i
ons may occur
i
nw
hi
c
h
t
h
e quant
i
ty o
ff
oo
dli

m
i
ts
i
nsect
di
str
ib
ut
i
on an
d
a
b
un
d
ance. In t
h
e
fi
rst, t
h
ere
i
snoa
b
so
l
ute s
h

ortage o
ff
oo
d
,
b
ut on
l
y a proport
i
on o
f
t
he
tota
li
sava
il
a
bl
e to a spec
i
es. T
h
us, t
h
ere
i
ssa
id

to
b
e a “re
l
at
i
ve s
h
orta
g
e” o
ff
oo
d
.Var
i
ou
s
reasons ma
y
account for the food not bein
g
available. (1) The food ma
y
be concentrated
6
93
THE BI
O
TI

C
ENVIRONMEN
T
F
IGURE 23.2.
A
n example of a food web in a freshwater ecosystem, showing the importance of insects. [From
P
.W
.
Pr
i
ce, T
h
e concept o
f
t
h
e ecos
y
stem,
i
n
:
E
co
l
ogica
l
Entomo

l
ogy
(
C. B. Hu
ff
a
k
er an
d
R. L. Ra
bb
,e
d
s.
).
Cop
y
ri
g
h
t

CC
1984 b
y
John Wile
y
and Sons, Inc. Reprinted b
y
permission of John Wile

y
and Sons, Inc.
]
w
ithin a small area so that it is available to relativel
y
few insects. As an interestin
g
exampl
e
of this Andrewartha (1961) cited the Shinyanga Game-Extermination Experiment in Eas
t
Africa in which, over the course of about
5
years, the natural hosts of tsetse flies wer
e
v
i
rtua
ll
y exterm
i
nate
d
over an area o
f
a
b
out 800 square m
il

es. At t
h
een
d
o
f
t
hi
s per
i
o
d
on
e
small elephant herd and various small un
g
ulates remained in the
g
ame reserve. However
,
almost no tsetse flies could be found, despite the fact that, collectivel
y
, the mammals tha
t
remained could suppl
y
enou
g
h blood to feed the entire ori
g

inal population of flies. Th
e
di
str
ib
ut
i
on o
f
t
h
e
f
oo
d
was now so sparse t
h
at t
h
ec
h
ance o
ffli
es o
b
ta
i
n
i
ng a mea

l
wa
s
pract
i
ca
ll
yn
il
. (2) T
h
e
f
oo
d
may
b
e ran
d
om
l
y
di
str
ib
ute
db
ut
diffi
cu

l
tto
l
ocate. T
h
us, on
ly
a
f
ract
i
on o
f
t
h
e
i
n
di
v
id
ua
l
s searc
hi
n
g
ever
fi
n

df
oo
d
. Suc
hi
s pro
b
a
bly
t
h
es
i
tuat
i
on
i
n man
y
parasitic or h
y
perparasitic species whose host is buried within the tissues of plants or othe
r
6
94
CHAPTER
23
animals. (3) A proportion of the food ma
y
occur in areas that for other reasons are no

t
n
ormall
y
visited b
y
the consumer so that, in effect, it is not available.
In the second situation, food ma
y
become a limitin
g
factor in population
g
rowth whe
n
a spec
i
es’ num
b
ers are not
k
ept
i
nc
h
ec
kb
yot
h
er

i
n
fl
uences, espec
i
a
ll
y natura
l
enem
i
es.
T
hi
s may
h
appen,
f
or examp
l
e, w
h
en a spec
i
es
i
s acc
id
enta
ll

y trans
f
erre
d
(o
f
ten as a resu
l
t
o
f human activit
y
) from its ori
g
inal environment to a new
g
eo
g
raphic area where its natural
e
nemies are absent. Under these conditions, the population ma
yg
row unchecked, and its
final size is limited onl
y
b
y
the amount of food available. Occasionall
y
, even in a species

’
n
atura
lh
a
bi
tat,
f
oo
d
may
li
m
i
t popu
l
at
i
on growt
h
,
f
or examp
l
e, w
h
en weat
h
er con
di

t
i
on
s
are
f
avora
bl
e
f
or
d
eve
l
opment o
f
a spec
i
es
b
ut not
f
or
d
eve
l
opment o
f
t
h

ose organ
i
sms t
h
a
t
pre
y
on or paras
i
t
i
ze
i
t.
2.2.
Q
ual
i
tat
i
ve Aspects
T
he nature of the food available ma
y
have strikin
g
effects on the survival, rate of
g
rowth, and reproductive potential of a species, and much work has been done on insect

s
i
nt
hi
s regar
d
. For examp
l
e, o
f
t
h
e
i
nsect
f
auna assoc
i
ate
d
w
i
t
h
store
d
pro
d
ucts, t
h

esaw
-
toot
h
e
d
gra
i
n
b
eet
l
e
,
Or
y
zaep
h
i
l
us surinamensi
s
, can surv
i
ve on
l
yon
f
oo
d

sw
i
t
h
a
hi
g
h
c
ar
b
o
hyd
rate content suc
h
as
fl
our,
b
ran, an
dd
r
i
e
df
ru
i
t, w
h
ereas spec

i
es o
f
sp
id
er
b
eet
l
es
,
Pt
i
nus
spp
., and flour beetles
,
T
r
iboliu
m spp., have no such carboh
y
drate requirement an
d
are consequentl
y
cosmopolitan, occurrin
g
in animal meals and dried
y

east, in addition t
o
p
l
ant pro
d
ucts. For some p
h
ytop
h
agous
i
nsects, a com
bi
nat
i
on o
f
p
l
ants o
f diff
erent
ki
n
ds
appears necessary
f
or surv
i

va
l
an
d
/or norma
l
rates o
fj
uven
il
e
d
eve
l
opment. In t
h
em
i
grator
y
g
rass
h
opper,
M
e
l
anop
l
us san

g
uinipe
s
,
f
or examp
l
e, a sma
ll
er percenta
g
eo
fi
nsects surv
i
ve
f
rom hatchin
g
to adulthood, and the development of those that do survive is slower when
the
g
rasshoppers are fed on wheat (Tr
i
t
i
cum aest
i
vum) alone com
p

ared with wheat
p
lus
fli
xwee
d
(Descurainia Sop
h
ia)o
r
d
an
d
e
li
on
(
T
a
r
axacum officinale
rr
)
(Pickford, 1962)
.
B
ot
h
t
h

e rate o
f
egg pro
d
uct
i
on an
d
t
h
e num
b
er o
f
eggs pro
d
uce
d
may
b
e mar
k
e
dl
y
a
ff
ecte
dby
t

h
e nature o
f
t
h
e
f
oo
d
ava
il
a
bl
e. Man
y
common
fli
es,
f
or examp
l
e, spec
i
es o
f
M
usc
a
,
C

alli
p
hor
a
,
an
d
L
ucilia
,
ma
y
survive as adults for some time on a diet of carbo-
h
y
drate. However, for females to mature e
gg
s a source of protein is essential. Pickfor
d
(
1962) showed that
M
. san
g
u
i
n
i
pe
s

f
ema
l
es
f
e
d
a
di
et t
h
at
i
nc
l
u
d
e
dwh
eat an
d wild
mustar
d
(
Bra
ss
ica
k
a
b

e
r
)
o
r
wheat and flixweed produced far more eggs (
5
79 and 467 eggs pe
r
f
ema
l
e, respect
i
ve
ly
)t
h
an
f
ema
l
es
f
e
d
on w
h
eat (243 e
gg

s
/
Ɋ
), w
ild
mustar
d
(431 e
gg
s/
Ɋ
),
o
r flixweed (249 e
gg
s
/
Ɋ
), alone. These differences in e
gg
production resulted lar
g
el
y
fro
m
v
ariations in the duration of adult life, thou
g
h differences in rate of e

gg
production were
also evident. For exam
p
le,
p
ercent survival of females fed wheat
p
lus mustard after 1, 2
,
and 3 months was 93%,
6
0%, and 13%, respectively. These females produced, on average,
8
.4 e
gg
s/
f
ema
l
e per
d
a
y
.T
h
e correspon
di
n
gfig

ures
f
or
f
ema
l
es
f
e
d
on w
h
eat a
l
one wer
e
8
7%, 27%, and 0% survival over 1, 2, and 3 months, respectivel
y
, and 4.
6
e
gg
s/female per
da
y
. The metabolic basis for these differences was not determined
.
3
.In

sec
t-Pl
a
nt Int
e
r
ac
t
io
n
s
3
.1. Herbivore
s
Th
ou
gh i
nsects
f
ee
d
on p
l
ants
f
rom a
ll
o
f
t

h
ema
j
or taxonom
i
c
g
roups, t
h
e
g
reates
t
n
umber of herbivorous species feed on an
g
iosperms with which the
y
have been coevolvin
g
6
9
5
THE BI
O
TI
C
ENVIRONMEN
T
since the Cretaceous period (Chapter 2, Section 4.2). All parts of a plant ma

y
be exploite
d
as a result of the activities of
g
razin
g
, suckin
g
, and borin
g
insects. As mi
g
ht be anticipated
in view of the len
g
th of time over which this coevolution has occurred, some of the rela
-
ti
ons
hi
ps
b
etween
h
er
bi
vorous
i
nsects an

d
ang
i
osperms are extreme
l
y
i
nt
i
mate an
d
re
fi
ne
d
,
th
oug
h
essent
i
a
ll
yt
h
ere
l
at
i
ons

hi
ps
h
ave a common t
h
eme. Insects ga
i
n energy (
f
oo
d
)a
t
th
e expense o
f
p
l
ants, w
h
ereas p
l
ants attempt to
d
e
f
en
d
t
h

emse
l
ves (conserve t
h
e
i
r ener
gy
)
or at least to obtain somethin
g
in return for the ener
gy
that insects take from them. Thou
g
h
t
he theme remains constant throu
g
h time, the relationships themselves are alwa
y
s chan
g
in
g
as a resu
l
to
f
natura

l
se
l
ect
i
on. Insects str
i
ve to
i
mprove t
h
e
i
r energy-gat
h
er
i
ng e
ffi
c
i
enc
y
(most o
f
ten
b
y concentrat
i
ng on energy

i
n a part
i
cu
l
ar
f
orm an
df
rom a restr
i
cte
d
sourc
e
an
db
y spec
i
a
li
zat
i
on o
f
t
h
e met
h
o

d
use
d
to co
ll
ect t
h
e energy) w
hil
ep
l
ants concurrent
l
y
improve their defenses. Most authors, for example, Price (1997) view this relationship as
“constant warfare” between insects and
p
lants, which forms the basis of their coevolu-
t
ion. Other authors such as Owen and Wiegert (1987) believe that herbivory is a form of
mutua
li
sm. T
h
ey po
i
nt out t
h
at,
i

n ana
l
ogy w
i
t
h
prun
i
ng, mow
i
ng, an
d
s
i
m
il
ar act
i
v
i
t
i
e
s
carr
i
e
d
out
b

y
h
umans, a
f
requent e
ff
ect o
fi
nsects graz
i
ng on new
l
y
f
orme
d
p
l
ant t
i
ssues
i
s
t
o stimulate the plant to produce more branches and, eventuall
y
, more reproductive struc-
t
ures and seed; in other words, the plant is makin
g

an adaptive, mutualistic response to th
e
h
erbi
v
ore.
T
h
e most common met
h
o
d
use
db
yp
l
ants as
d
e
f
ense aga
i
nst
i
nsects (an
d
ot
h
er
h

er
-
bi
vorous an
i
ma
l
s)
i
s pro
d
uct
i
on o
f
tox
i
c meta
b
o
li
tes. P
l
ants pro
d
uceaw
id
e array o
f
suc

h
chemicals in secondar
y
metabolic pathwa
y
s (i.e., those not used for
g
eneration of ma
-
j
or components such as proteins, nucleic acids, and carboh
y
drates). Particular t
y
pes o
f
secondar
y
plant compounds are commonl
y
restricted to specific plant families, for exam-
p
l
e, g
l
ucos
i
no
l
ates

i
n Brass
i
caceae (cruc
if
ers), car
d
eno
lid
es (ma
i
n
l
y car
di
ac g
l
ycos
id
es)
in
Asclepiadaceae (milkweeds), and cucurbitacins in Cucurbitaceae (Panda and Khush, 199
5
;
Sc
h
oon
h
ove
n

et al.
, 1998). Moreover, t
h
e compoun
d
so
f
ten accumu
l
ate w
i
t
hi
n spec
ifi
ct
i
s-
sues or areas of the plant, for example, trichomes (terpenes), the wax la
y
er (phenolics)
,
vacuoles (alkaloids), and seeds (non-protein amino acids) (Berna
y
s and Chapman, 1994)
.
Th
e repro
d
uct

i
ve parts o
f
p
l
ants, w
hi
c
h
represent concentrate
d
stores o
f
energy, are es
-
pec
i
a
ll
y attract
i
ve to
h
er
bi
vores an
d
o
f
ten serve as a s

i
n
kf
or secon
d
ary meta
b
o
li
tes. For
examp
l
e, Hypericum per
f
oratum
(
K
l
amat
h
wee
d
) pro
d
uces t
h
e tox
i
cqu
i

none
h
yper
i
c
i
n
.
T
he concentration of h
y
pericin is 3
0
µ
g
/
g
wet wei
g
ht in the lower stem, 70
µ
g
/
g
in the
upp
er stem, and 500
µ
g
/

g
in the flower (Price, 1997). T
y
picall
y
, the toxins are chemicall
y
combined with sugars, salts, or proteins to render them inactive while in storage. When th
e
p
l
ant t
i
ssue
i
s
d
amage
d
, enzymes re
l
ease t
h
e tox
i
n
f
rom
i
ts con

j
ugate, a
ll
ow
i
ng a
l
oca
li
ze
d
e
ff
ect at t
h
es
i
te o
f
t
h
e woun
d
(Bernays an
d
C
h
apman, 1994).
The evolutionar
y

ori
g
in of these secondar
y
metabolites remains a matter of specula-
t
ion. An earl
y
view was that the chemicals arose as waste products of a plant’s primar
y
metabolism, and the plant, being unable to excrete the molecules, simply retained them
wi
t
hi
n
i
ts t
i
ssues. T
hi
s
id
ea
i
s now cons
id
ere
d
un
lik

e
l
yg
i
ven t
h
e
hi
g
hl
y comp
l
ex nature o
f
some o
f
t
h
ese compoun
d
san
d
,t
h
ere
f
ore, t
h
e amount o
f

energy requ
i
re
df
or t
h
e
i
r synt
h
es
i
s
.
A more
lik
e
ly
poss
ibili
t
yi
st
h
at or
igi
na
lly
t
h

e meta
b
o
li
tes were s
i
mp
ly
s
h
ort-
li
ve
di
nterme-
d
iates in normal biochemical pathwa
y
s within plants and/or provided a means of storin
g
chemical ener
gy
for later use b
y
the plant. In other words, the ori
g
inal function(s) of these
compoun
d
s may

h
ave
b
een unre
l
ate
d
to t
h
e occurrence o
fh
er
bi
vores. An examp
l
eo
f
suc
ha
compoun
d
m
i
g
h
t
b
en
i
cot

i
ne pro
d
uce
db
yt
h
eto
b
acco p
l
an
t
(
Nicotian
a
spp.). Ra
di
o
i
sotope
stu
di
es
h
ave s
h
own t
h
at, a

l
t
h
ou
gh
a
b
out 12% o
f
t
h
e ener
gy
trappe
di
np
h
otos
y
nt
h
es
i
s
i
s use
d
6
9
6

CHAPTER
23
f
or nicotine production, the nicotine has a relativel
y
short half-life, 40% of it bein
g
converted
to other metabolites (possibl
y
su
g
ars, amino acids, and or
g
anic acids) within 10 hours
.
T
hus, animals adapted to feedin
g
on plants that produce toxins will be at a consid-
e
ra
bl
ea
d
vantage over an
i
ma
l
st

h
at are not. Among
h
er
bi
vores,
i
nsects s
h
ow t
h
e greatest
a
bili
ty to cope w
i
t
h
t
h
e tox
i
ns. In part, t
hi
sar
i
ses
f
rom t
h

e enormous per
i
o
d
o
f
t
i
me ove
r
whi
c
h
coevo
l
ut
i
on o
fi
nsects an
d
p
l
ants
h
as occurre
d
,
b
ut

i
t
i
sa
l
so re
l
ate
d
to
i
nsects’
high
reproductive rate and short
g
eneration time, which facilitate rapid adaptation to chan
g
es i
n
the host plant. Throu
g
h evolution, man
y
insect species have not onl
y
developed increas-
i
ng to
l
erance to a

h
ost p
l
ant’s tox
i
ns
b
ut are now attracte
db
yt
h
em. In ot
h
er wor
d
s, suc
h
i
nsects
l
ocate
f
oo
d
p
l
ants
b
yt
h

e scent or taste o
f
t
h
e
i
r tox
i
csu
b
stance an
df
requent
l
yar
e
restr
i
cte
d
to
f
ee
di
ng on suc
h
p
l
ants. For examp
l

e, certa
i
n
fl
ea
b
eet
l
es,
Phyll
otreta spp., an
d
c
abba
g
e worms
,
Pieris spp., feed exclusivel
y
on plants such as Cruciferae that produce
g
lucosinolates (mustard oil). Colorado potato beetles,
L
eptinotarsa decemlineata, and var-
i
ous hornworms,
M
anduca spp., feed only on Solanaceae, the family that includes potato
(
S

o
l
anum tu
b
erosum) (pro
d
uces so
l
an
i
ne), to
b
acco
(
N
i
cot
i
an
a
s
pp.) (n
i
cot
i
ne), an
dd
ea
dly
nightshade (

Atropa belladonna
(
(
) (atrop
i
ne) (Pr
i
ce, 1997)
.
T
he method most often used to overcome the potentiall
y
harmful effects of thes
e
c
hemicals is to convert them into non-toxic or less toxic products. Especiall
y
important in
such conversions is a group of enzymes known as mixed-function oxidases (polysubstrate
m
onooxygenases), w
hi
c
h
,ast
h
e
i
r name
i

n
di
cates, cata
l
yze a var
i
ety o
f
ox
id
at
i
on react
i
ons
(
Sc
h
oon
h
oven et a
l
., 1998). T
h
e enzymes are
l
ocate
di
nt
h

em
i
crosome
f
ract
i
on
∗
of
ce
ll
san
d
o
ccur in particularl
y
hi
g
h concentrations in fat bod
y
and mid
g
ut. Perhaps unsurprisin
g
l
y
,it
is these same enz
y
mes that are often responsible for the resistance of insects to s

y
nthetic
insecticides (Cha
p
ter 1
6
,
S
ection 5.5.)
.
Some
i
nsects are a
bl
eto
f
ee
d
on potent
i
a
ll
y
d
angerous p
l
ants as a resu
l
to
f

e
i
t
h
er
tempora
l
or spat
i
a
l
avo
id
ance o
f
t
h
e tox
i
c mater
i
a
l
s. For examp
l
e, t
h
e
lif
e

hi
story o
f
t
he
winter moth
,
Op
ero
p
htera brumata
,
is such that the caterpillars hatch in the earl
y
sprin
g
a
nd feed on
y
oun
g
leaves of oak
(
Q
uercu
s
spp.), which have onl
y
low concentrations of
tannins, molecules that complex with proteins to reduce their digestibility. Though weather

c
on
di
t
i
ons are su
i
ta
bl
ean
df
oo
di
sst
ill
apparent
l
yp
l
ent
if
u
ll
ater
i
nt
h
e season, a secon
d
g

enerat
i
on o
f
w
i
nter mot
h
s
d
oes not
d
eve
l
op
b
ecause
b
yt
hi
st
i
me
l
arge quant
i
t
i
es o
f

tann
i
ns
a
re present in the leaves. Spatial avoidance is possible for man
y
Hemiptera whose delicate
s
uctorial mouthparts can b
y
pass localized concentrations of toxin in the host plant. Some
a
phids feed on senescent foliage where the concentration of toxin is less than that of younger,
meta
b
o
li
ca
ll
y act
i
ve t
i
ssue (Pr
i
ce, 1997)
.
P
r
i

ce (1997) propose
d
t
h
at at
l
east
f
our a
d
vantages may accrue to an
i
nsect a
bl
eto
f
eed on potentiall
y
toxic plants. First, competition with other herbivores for food will be
much reduced. Second, the food plant can be located easil
y
. Related to this, as member
s
o
f a species will tend to a
gg
re
g
ate on or near the food plant, the chances of findin
ga

mate w
ill b
e
i
ncrease
d
.T
hi
r
d
,
if
an
i
nsect
i
sa
bl
e to store t
h
e
i
ngeste
d
tox
i
nw
i
t
hi

n
i
ts
t
i
ssues,
i
t may ga
i
n protect
i
on
f
rom wou
ld
-
b
e pre
d
ators. Many examp
l
es o
f
t
hi
sa
bili
t
y
a

re
k
nown, espec
i
a
lly
amon
g
Lep
id
optera (B
l
um, 1981; N
i
s
hid
a, 2002). T
h
us, most o
f
t
h
e
insect fauna associated with milkweeds are able to store the cardenolides produced b
y
these
p
lants. These substances, at sublethal levels, induce vomitin
g
in vertebrates. Other well-

k
nown examp
l
es are pyrro
li
z
idi
ne a
lk
a
l
o
id
s sequestere
db
y arct
iid
mot
h
s, an
d
cucur
bi
tac
i
ns
∗
Th
em
i

crosome
f
ract
i
on
i
so
b
ta
i
ne
db
y
diff
erent
i
a
lhi
g
h
-spee
d
centr
if
ugat
i
on o
fh
omogen
i

ze
d
ce
ll
san
d
cons
i
sts
o
ff
ra
g
mente
d
mem
b
ranes o
f
en
d
op
l
asm
i
c ret
i
cu
l
um, r

ib
onuc
l
eoprote
i
ns, an
d
ves
i
c
l
es.
6
9
7
THE BI
O
TI
C
ENVIRONMEN
T
accumulated b
y
cucumber beetles. In Lepidoptera the chemicals are accumulated b
y
the
caterpillar sta
g
e and are transferred at metamorphosis to the adult. Further, in some species
t

he female endows her e
gg
s with the toxin so that the
y
, too, are protected (Blum and Hilker,
2002). Most
i
nsect spec
i
es t
h
at sequester tox
i
ns
f
rom t
h
e
i
r
h
ost p
l
ant are aposemat
i
ca
ll
y
(
b

r
i
g
h
t
l
yan
ddi
st
i
nct
l
y) co
l
ore
d
,a
f
eature common
l
y
i
n
di
cat
i
ve o
f
a
di

staste
f
u
l
organ
i
s
m
an
d
one t
h
at ma
k
es t
h
em stan
d
out a
g
a
i
nst t
h
e
b
ac
kg
roun
d

o
f
t
h
e
i
r
h
ost p
l
ant. On samp
li
n
g
such insects, a would-be vertebrate predator discovers their unpalatabilit
y
and quickl
y
learns to avoid insects havin
g
a particular color pattern. Remarkabl
y
, a few insect predators
h
ave evo
l
ve
d
to
l

erance to t
h
ep
l
ant-pro
d
uce
d
tox
i
ns store
db
yt
h
e
i
r
i
nsect prey an
d
are
,
th
emse
l
ves, unpa
l
ata
bl
etopre

d
ators
f
urt
h
er up t
h
e
f
oo
d
c
h
a
i
n(E
i
sner
e
ta
l
., 1997). T
h
e
f
ourt
h
a
d
vantage to

b
ega
i
ne
db
yto
l
erance to t
h
ese p
l
ant pro
d
ucts
i
s protect
i
on aga
i
ns
t
patho
g
enic microor
g
anisms. For example, cardiac
g
l
y
cosides in the hemol

y
mph of the lar
ge
milkweed bu
g
,
O
ncopeltus fasciatus,h
av
ea
s
tron
g
antibacterial effect. Also, cucurbitacin
s
sequestered by the adult female cucumber beetle,
D
iabrotica undecimpunctata howardi
,
prov
id
e ant
if
unga
l
protect
i
on
f
or

h
er eggs an
d
o
ff
spr
i
ng (Ta
ll
am
y
e
ta
l.
,
1998).
T
h
ec
h
anne
li
ng o
f
energy
i
nto pro
d
uct
i

on o
f
tox
i
c or repe
ll
ent su
b
stances
i
st
h
e mos
t
often used method b
y
which plants ma
y
obtain protection, thou
g
h others are known.
A
few plants expend this “ener
gy
of protection” on formation of structures that prevent or
d
eter feeding, or even harm would-be feeders. For example, passion flowers (Passi
fl
or
a

ad
enopo
d
a
)h
av
em
i
nute
h
oo
k
e
dh
a
i
rs t
h
at gr
i
pt
h
e
i
ntegument o
f
caterp
ill
ars attempt
i

n
g
t
o
f
ee
d
on t
h
em. T
h
e
h
a
i
rs
b
ot
hi
mpe
d
e movement an
d
tear t
h
e
i
ntegument as t
h
e caterp

il
-
lars stru
gg
le to free themselves so that the insects die from starvation and/or desiccation
(Gilbert, 1971). Le
g
uminous plants have evolved a variet
y
of ph
y
sical (as well as chemical
)
mechanisms to
p
rotect their seeds from Bruchidae (
p
ea and bean weevils). These includ
e
pro
d
uct
i
on o
f
gum as a
l
arva penetrates t
h
e see

d
po
d
so t
h
at t
h
e
i
nsect
i
s
d
rowne
d
or
i
ts
movements
hi
n
d
ere
d
, pro
d
uct
i
on o
f

a
fl
a
k
ypo
d
sur
f
ace t
h
at
i
ss
h
e
d
, carry
i
ng t
h
e weev
il
’s
e
gg
sw
i
t
hi
t, as t

h
epo
db
rea
k
s open to expose
i
ts see
d
s, an
d
pro
d
uct
i
on o
f
po
d
st
h
at open
explosivel
y
so that seeds are immediatel
y
dispersed and, therefore, not available to females
t
hat oviposit directl
y

on seeds (Center and Johnson, 1974)
.
3
.2. In
sec
t-Pl
a
nt M
u
t
ua
l
is
m
Not all insect-plant relationships are of the “constant warfare” t
y
pe
j
ust discussed. For a
lar
g
e number of insect and plant species, an interaction of mutual benefit has evolved. Thus
,
some insects live in close association with plants, protecting them in return for food. For
example, the bull’s-horn acacias (
A
cacia
(
(
s

pp.) are
h
ost to co
l
on
i
es o
f
ants (Pseu
d
om
y
rme
x
spp.) t
h
at
li
ve w
i
t
hi
nt
h
eswo
ll
en,
h
o
ll

ow st
i
pu
l
ar t
h
orns an
df
ee
d
on nectar (pro
d
uce
din
petioles) and protein (in Beltian bodies at the tips of new leaves) (Fi
g
ure 23.3). In return,
t
he a
gg
ressive ants
g
uard the plants a
g
ainst herbivores and suppress the
g
rowth of nearb
y,
potentially competitive plants by chewing their growing tips (H¨olldobler and Wilson, 1990).
A mutua

li
st
i
cre
l
at
i
ons
hi
po
f
a very
diff
erent
ki
n
di
st
h
at
i
nw
hi
c
h
t
h
e
h
ost supp

li
e
s
f
oo
d
to
i
nsects,
i
n return
f
or w
hi
c
h
t
h
e
i
nsects prov
id
et
h
e transport system
f
or
di
spersa
l

o
f
po
ll
en, see
d
s, an
d
spores. T
h
ou
gh
t
h
e
i
r
i
mportance as po
lli
nators
f
or
high
er p
l
ants
h
as
b

ee
n
extensivel
y
studied (
K
evan and Baker, 1983, 1999; Schoonhove
n
et al.
, 1998
)
, it must be
emphasized that some insects are essential for spore dispersal in some mosses and man
y
fungi (see Chapter 16, Section 4.2.4), as well as transporting seeds of angiosperms. The
success (
i
mportance) o
fi
nsects as po
lli
nators compare
d
w
i
t
h
po
lli
nators

f
rom ot
h
er group
s
suc
h
as
bi
r
d
san
db
ats
i
s presuma
bly
a resu
l
to
f
t
h
e
i
r muc
hl
on
g
er evo

l
ut
i
onar
y
assoc
i
at
i
o
n
6
98
CHAPTER
23
F
IGURE 23.3
.
Mutua
li
sm
b
etween
b
u
ll
’s-
h
orn acac
i

aan
d
ants. (A) Acac
i
a
l
ea
f
an
d
tw
i
gs
h
ow
i
ng extra
fl
ora
l
n
ectar
y
,
h
o
ll
ow t
h
orns, an

dl
ea
fl
ets w
i
t
h
Be
l
t
i
an
b
o
di
es at t
i
ps; (B) en
l
ar
g
e
d
v
i
ew o
fh
o
ll
ow t

h
orn w
i
t
h
entrance
hole of ant nest; and (C) close-up view of Beltian bodies and ant visitor. [A, redrawn from W. M. Wheeler, 1910,
A
nts. T
h
eir Structure, Deve
l
opment an
d
Be
h
aviour.Co
l
um
bi
aUn
i
vers
i
ty Press. B, C, p
h
otograp
h
s courtesy o
f

D
an L. Per
l
man.]
w
ith plants. Most of the modern insect orders were well established b
y
the time the earliest
flowerin
g
plants appeared about 225 million
y
ears a
g
o. Thus, insects were able to
g
ai
n
a cons
id
era
bl
e
h
ea
d
start as
p
o
lli

nators over
bi
r
d
san
db
ats, t
h
e ear
li
est
f
oss
il
recor
d
s
f
or
w
hich date back about 1
5
0 and 60 million years, respectively (Price, 1997).
To
a
c
hi
eve e
ff
ect

i
ve cross-po
lli
nat
i
on, two
i
mportant
f
actors must
b
eta
k
en
i
nto con-
sideration in an evolutionar
y
sense. First, plants must produce precisel
y
the ri
g
ht amount o
f
6
9
9
THE BI
O
TI

C
ENVIRONMEN
T
F
IGURE 23.3.
(
Continue
d
)
nectar to ma
k
ean
i
nsect’s v
i
s
i
t energet
i
ca
ll
y wort
h
w
hil
e, yet st
i
mu
l
ate v

i
s
i
ts to ot
h
er p
l
ants
,
an
d
secon
d
,p
l
ants o
f
t
h
e same spec
i
es must
b
e eas
il
y recogn
i
ze
db
yan

i
nsect. I
f
too muc
h
ener
gy i
sma
d
eava
il
a
bl
e
by
eac
h
p
l
ant, t
h
en
i
nsects nee
d
v
i
s
i
t

f
ewer p
l
ants an
d
t
h
e extent o
f
cross-pollination is reduced. If a plant produces too little food (to ensure that an insect will
visit man
y
plants), there is a risk that the insect will seek more accessible sources of food,
N
atural selection determines the precise amount of energy that each plant must offer to a
n
i
nsect, an
d
t
hi
s amount
d
epen
d
sonanum
b
er o
ff
actors. T

h
e amount o
f
energy ga
i
ne
db
ya
n
i
nsect
d
ur
i
ng eac
h
v
i
s
i
ttoa
fl
ower
i
sre
l
ate
d
to
b

ot
h
quant
i
ty an
d
qua
li
ty o
f
ava
il
a
bl
e
f
oo
d
.
T
hus, until recentl
y
, it was considered that man
y
adult insects obtained their carboh
y
drat
e
re
q

uirements from nectar and their
p
rotein re
q
uirements from other sources such as
p
ollen
,
v
e
g
etative parts of the plant (as a result of larval feeding), or other animals. Baker an
d
B
a
k
er (1973) s
h
owe
d
,
h
owever, t
h
at t
h
e nectar o
f
many p
l

ants conta
i
ns s
i
gn
ifi
cant amount
s
o
f
am
i
no ac
id
s
,
so t
h
at
i
nsects can concentrate t
h
e
i
re
ff
orts on nectar co
ll
ect
i

on. T
hi
s not
onl
y
increases the extent of cross-pollination b
y
inducin
g
more visits to flowers, but ma
y
also lead to econom
y
in pollen production, as pollen becomes less important as food for
t
he insects. The amount of nectar
p
roduced is a function of the number of flowers
p
er
p
lant
.
Hence,
f
or p
l
ants w
i
t

h
a num
b
er o
ffl
owers
bl
oom
i
ng sync
h
ronous
l
y,
i
t
i
s
i
mportant t
h
at
eac
hfl
ower pro
d
uces on
l
y a sma
ll

amount o
f
nectar an
d
po
ll
en, so t
h
at an
i
nsect must v
i
s
i
t
other plants to satisf
y
its requirements
.
More nectar is produced b
y
plant species whose members t
y
picall
yg
row some distanc
e
apart, so that it is still ener
g
eticall

y
worthwhile for an insect species to concentrate on these
p
l
ants. Re
l
ate
d
to t
hi
s,
i
nsects t
h
at
f
orage over greater
di
stances are
l
arger spec
i
es suc
h
as
b
ees, mot
h
s, an
db

utter
fli
es w
h
ose energy requ
i
rements are
hi
g
h
.W
h
en nectar
i
s pro
d
uce
d
i
n
l
ar
g
e amounts,
i
t
i
st
y
p

i
ca
lly
access
ibl
eon
ly
to
l
ar
g
er
i
nsects t
h
at are stron
g
enou
gh
to
g
ain entr
y
into the nectar-producin
g
area or have sufficientl
y
elon
g
ate mouthparts. Thi

s
ensures that nectar is not wasted on smaller insects lackin
g
the abilit
y
to carr
y
pollen t
o
ot
h
er mem
b
ers o
f
t
h
e
pl
ant s
p
ec
i
es.
Temperature a
l
so a
ff
ects t
h

e amount o
f
nectar pro
d
uce
d
,as
i
t
i
sre
l
ate
d
to t
h
e energ
y
expen
d
e
dbyi
nsects
i
n
fligh
tan
d
to t
h

et
i
me o
fd
a
y
an
d
/or season. For examp
l
e,
i
n temperate
re
g
ions and/or at hi
g
h altitudes, flowers that bloom earl
y
in the da
y
or at ni
g
ht, or earl
y
7
00
CHAPTER
23
o

r late in the season, when temperatures ma
y
not be much above freezin
g
, must provide
a lar
g
e enou
g
h reward to make fora
g
in
g
profitable at these temperatures. An alternative to
production of lar
g
e amounts of nectar b
y
individual flowers is for plants that bloom at lowe
r
temperatures to grow
i
n
hi
g
hd
ens
i
ty an
dfl

ower sync
h
ronous
l
y (He
i
nr
i
c
h
an
d
Raven, 1972)
.
B
eyon
d
a certa
i
n
di
stance
b
etween p
l
ants,
h
owever, t
h
e amount o

f
nectar t
h
at an
i
nsect
requ
i
res to co
ll
ect at eac
h
p
l
ant (
i
nor
d
er to rema
i
n“
i
ntereste
d
”
i
nt
h
at spec
i

es) excee
d
st
h
e
m
aximum amount that the
p
lant is able to
p
roduce. Thus, the
p
lant must ado
p
t a differen
t
strate
gy
. Amon
g
orchids, for example, about one half of the species produce no nectar,
but
r
e
l
yonot
h
er met
h
o

d
s to attract
i
nsects, espec
i
a
ll
y
d
ecept
i
on
b
ym
i
m
i
cry. T
h
e
fl
ower
s
m
ay resem
bl
e (1) ot
h
er nectar-pro
d

uc
i
ng
fl
owers, (2)
f
ema
l
e
i
nsects so t
h
at ma
l
es ar
e
attracte
d
an
d
attempt pseu
d
ocopu
l
at
i
on, (3)
h
osts o
fi

nsect paras
i
to
id
s, or (4)
i
nsects t
h
a
t
are subsequentl
y
attacked b
y
other territorial insects. These somewhat risk
y
methods of
attractin
g
insects are offset b
y
the evolution of hi
g
hl
y
specific pollen receptors (so that onl
y
pollen from the correct species is acquired) and a high degree of seed set for each pollination
(
Pr

i
ce, 1997)
.
It
i
s
i
mportant
f
or
b
ot
h
p
l
ants an
di
nsects t
h
at
i
nsects v
i
s
i
t mem
b
ers o
f
t

h
e same p
l
ant
species. The chances of this occurrin
g
are
g
reatl
y
increased (1) when the plant species has a
restricted period of bloom, in terms of both season and/or time of da
y
; (2) where members
o
f a species grow in aggregations, though this is counterbalanced by a restriction of gen
e
fl
ow
if
po
lli
nators wor
k
w
i
t
hi
n a part
i

cu
l
ar p
l
ant popu
l
at
i
on; an
d
(3) w
h
en t
h
e
fl
owers ar
e
e
as
il
y recogn
i
ze
db
yan
i
nsect w
hi
c

hl
earns to assoc
i
ateag
i
ven p
l
ant spec
i
es w
i
t
hf
oo
d
.
Reco
g
nition is achieved as a result of flower morpholo
gy
(and related to this is accessibilit
y
o
f the nectar and pollen), color, and scent. The advanta
g
e to an insect species when its
m
embers can reco
g
nize particular flowers is that, throu

g
h natural selection, the species wil
l
b
ecome more e
ffi
c
i
ent at gat
h
er
i
ng an
d
ut
ili
z
i
ng t
h
e
f
oo
d
pro
d
uce
db
yt
h

ose
fl
owers
.
Th
e
d
egree o
fi
n
fl
uence t
h
at t
h
ese var
i
a
bl
es exert
i
s man
if
est as a spectrum o
fi
nt
i
macy
b
etween p

l
ants an
d
t
h
e
i
r
i
nsect po
lli
nators. At one en
d
o
f
t
h
e spectrum, t
h
ep
l
ant-
i
nsec
t
relationship is non-specific; that is, a variet
y
of insect species serve as pollinators for a variet
y
o

f plants. Neither insects nor flowers are especiall
y
modified structurall
y
or ph
y
siolo
g
icall
y.
A
tt
h
e oppos
i
te extreme, t
h
ere
l
at
i
ons
hi
p
i
s suc
h
t
h
atap

l
ant spec
i
es
i
spo
lli
nate
db
ya
s
i
ng
l
e
i
nsect spec
i
es. Structura
lf
eatures o
f
t
h
epo
lli
nator prec
i
se
l

y comp
l
ement
fl
ower
m
orp
h
o
l
ogy; t
h
ep
l
ant’s
bl
oom
i
ng per
i
o
di
s sync
h
ron
i
ze
d
w
i

t
h
t
h
e
lif
e
hi
story an
ddi
urna
l
activit
y
of the insect; and, where present, nectar is produced in exactl
y
the ri
g
ht quantit
y
and qualit
y
to satisf
y
the insect’s requirements
.
Harvester ants (those that use seeds as food) are important seed dispersers, resulting
f
rom acc
id

enta
ll
oss o
f
t
h
e see
d
sast
h
ey transport t
h
em
b
ac
k
to t
h
e nest or
b
y
f
a
il
ure to use t
h
e
see
d
s

b
e
f
ore t
h
ey germ
i
nate. T
hi
s act
i
v
i
ty part
i
a
ll
y compensates
f
or t
h
e
d
amage cause
d
to
the plant b
y
the ants’ seed predation. This mutualistic relationship has been taken to a new
l

evel of sophistication b
y
m
y
rmecochorous plants, which produce attractive appenda
g
es
(
elaiosomes) on their seeds and chemicals to induce the ants to trans
p
ort the seeds without
d
amag
i
ng t
h
em (F
i
gure 23.4). T
h
ee
l
a
i
osomes are r
i
c
hi
n nutr
i

ents an
df
orm t
h
e
f
oo
d
o
f
t
h
e ants, w
hil
et
h
e see
di
tse
lf i
s
di
scar
d
e
d
.T
h
oug
h

examp
l
es o
f
myrmecoc
h
ory are
k
nown
w
or
ld
w
id
e,
i
t seems to
b
eap
h
enomenon o
fh
a
bi
tats t
h
at are nutr
i
ent-poor (espec
i

a
lly
t
h
os
e
deficient in phosphorus and potassium), notabl
y
the dr
y
schleroph
y
ll re
g
ions of Australia an
d
S
outh Africa where more than 90% of the 3100 known species of m
y
rmecochorous plant
s
are
f
oun
d
.It
h
as
b
een specu

l
ate
d
t
h
at p
l
ants
i
nt
h
ese
h
a
bi
tats use myrmecoc
h
ory
b
ecause
e
nerget
i
ca
ll
y
i
t
i
s

f
ar
l
ess expens
i
ve t
h
an t
h
e pro
d
uct
i
on o
f
t
h
e
l
arger
f
ru
i
ts pre
f
erre
db
y
v
ertebrates

(
Beattie, 198
5
;H¨olldobler and Wilson, 1990
)
.
7
01
THE BI
O
TI
C
ENVIR
O
NMEN
T
F
IGURE 23.4.
W
orkers of Formica
p
odzolic
a
fr
o
m
t
h
e
n

ort
h
ern Un
i
te
d
States
g
at
h
er
i
n
g
v
i
o
l
et
(
Vio
l
a nutta
ll
ii
)
see
d
s
.

N
ote the elaiosomes that will later be eaten b
y
colon
y
mem-
b
ers.
[
From A. J. Beattie. 1985, The Evolutionary Theory o
f
Ant-P
l
ant Mutua
l
isms
.
B
y
perm
i
ss
i
on o
f
Cam
b
r
idg
eUn

i
ver
-
s
it
y
Press.]
3.3. Detritivores
Fee
di
ng on
d
etr
i
tus, essent
i
a
ll
yt
h
e rema
i
ns o
fd
ea
d
an
i
ma
l

san
d
p
l
ants toget
h
er w
i
t
h
th
em
i
croor
g
an
i
sms t
h
at
b
r
i
n
g
a
b
out t
h
e

i
r
d
eca
y
,
i
saver
y
o
ld h
a
bi
t amon
g
Insecta, an
d
mos
t
orders include some detritivorous species (Southwood, 1972). Detritus-feedin
g
insects are
especiall
y
si
g
nificant in aquatic ecos
y
stems where lar
g

e quantities of dead plant matter ma
y
accumu
l
ate annua
ll
y. In streams an
d
r
i
vers t
h
e source o
f
t
hi
s mater
i
a
li
s
l
arge
l
y over
h
ang
i
ng
v

e
g
etat
i
on. In st
ill
waters t
h
ema
j
or contr
ib
utor to
d
etr
i
tus
i
sp
h
ytop
l
an
k
ton, t
h
oug
hi
ns
h

a
l
-
l
ow areas emergent vegetat
i
on may ma
k
eas
i
gn
ifi
cant contr
ib
ut
i
on. In terrestr
i
a
l
ecosystems
insects are
g
enerall
y
unimportant as detritivores, this role fallin
g
predominantl
y
to other

arthropods, notabl
y
Collembola and oribatid mites. Two notable exceptions are termites
,
t
he majority of which feed on wood litter, and the Australian Oecophoridae and Tortricidae
(Lep
id
optera) many o
f
w
h
ose
l
arvae
f
ee
d
on euca
l
yptus
li
tter (Common, 1980). T
h
e
f
o
li
ag
e

o
f
euca
l
yptus conta
i
ns su
b
stant
i
a
l
amounts o
f
p
h
eno
li
cs (
i
nc
l
u
di
ng tann
i
ns) an
d
essent
i

a
l
oils, renderin
g
it unpalatable to man
y
herbivores, and is also extremel
y
deficient in nitro
g
en
.
T
hus, the abilit
y
of these moth larvae to utilize this resource
g
ives them a ke
y
role in ener
gy
fl
ow and matter rec
y
clin
g
in this specialized ecos
y
stem.
According to Anderson and Cargill (1987), some 4

5
% of an estimated 10,000 specie
s
o
f
aquat
i
c
i
nsects
i
n Nort
h
Amer
i
ca
i
ngest some
d
etr
i
tus. T
h
ema
j
or groups o
fd
etr
i
t

i
vores
are
i
nt
h
eor
d
ers Tr
i
c
h
optera, D
i
ptera, Ep
h
emeroptera, P
l
ecoptera, an
d
Co
l
eoptera, an
d
t
h
e
ir
eatin
g

habits ma
y
be cate
g
orized as shreddin
g
and
g
ou
g
in
g
, scrapin
g
, filter feedin
g
,an
d
d
eposit collection (Fi
g
ure 23.2). The shredders,
g
ou
g
ers, and scrapers inevitabl
y
will in
g
es

t
th
e
li
v
i
ng saprop
h
yt
i
cm
i
croorgan
i
sms on t
h
e sur
f
ace o
f
t
h
e
d
ea
d
vegetat
i
on, as we
ll

a
s
th
ep
l
ant t
i
ssue
i
tse
lf
,an
d
a
k
ey quest
i
on
i
st
h
ere
l
at
i
ve
i
mportance o
f
t

h
ese as
f
oo
d
.For
some
d
etr
i
t
i
vores, t
h
ere
i
sev
id
ence t
h
at t
h
em
i
croor
g
an
i
sms prov
id

ea
ll
o
f
t
h
e nutr
i
ent
s
w
ith the relativel
y
indi
g
estible plant tissue simpl
y
passin
g
unchan
g
ed throu
g
h the
g
ut. I
n
other species, dead plant tissues are the main source of ener
gy
thou

g
h microor
g
anisms ma
y
supply some essential components. Generally, only about 10% of the ingested material is
ass
i
m
il
ate
d
,t
h
e rest
b
e
i
ng
d
e
f
ecate
d
. However, t
h
e
b
rea
ki

ng up o
f
t
h
e mater
i
a
li
nto sma
ll
er
part
i
c
l
es as
i
t passes a
l
ong t
h
ea
li
mentary tract
i
s
i
n
i
tse

lf i
mportant, t
h
e
i
ncrease
i
n sur
f
ace
area facilitatin
g
microbial activit
y
.
Detritus ma
y
var
y
considerabl
y
in its nutrient availabilit
y
and in its content of feed
-
ing deterrents, and a major role of the microorganisms is to “condition” the material, fo
r
examp
l
e,

b
yso
f
ten
i
ng t
h
et
i
ssues,
b
yc
h
em
i
ca
ll
y convert
i
ng t
h
e contents
i
nto a
f
orm t
h
a
t
can

b
e use
db
yt
h
e
i
nsects, an
db
y
d
etox
if
y
i
ng t
h
e
d
eterrent compoun
d
s. T
h
eava
il
a
bili
ty o
f
d

etr
i
tus as
f
oo
d
ma
y
a
l
so var
y
seasona
lly
,t
y
p
i
ca
lly b
ecom
i
n
g
max
i
ma
li
nt
h

e
f
a
ll f
o
ll
ow
i
n
g
7
02
CHAPTER
23
l
eaf drop and the death of emer
g
ent ve
g
etation and ph
y
toplankton and a
g
ain in sprin
g
a
s
temperatures rise permittin
g
renewed microbial activit

y
. Thus, man
y
detritivores (especiall
y
shredders) exhibit their
g
reatest
g
rowth rates in the fall and earl
y
winter, before enterin
ga
p
h
ase o
f
arreste
dd
eve
l
opment unt
il
spr
i
ng.
4
. Interactions between Insects and
O
ther Animal

s
Interact
i
ons
b
etween
i
nsects an
d
ot
h
er an
i
ma
l
s(
i
nc
l
u
di
ng ot
h
er mem
b
ers o
f
t
h
e sam

e
spec
i
es) ta
k
e many
f
orms, t
h
oug
h
most are
f
oo
d
-re
l
ate
d
. Insects may
b
e pre
d
ators (w
hi
c
h
requ
i
re more t

h
an one pre
yi
n
di
v
id
ua
li
nor
d
er to comp
l
ete
d
eve
l
opment), paras
i
to
id
s, or par
-
asites (which need onl
y
one host to complete development). Parasitoids differ from parasites
i
n that the
y
ultimatel

y
kill their host, which is t
y
picall
y
another arthropod. Alternativel
y
,
i
nsects may serve as prey or
h
ost
f
or ot
h
er an
i
ma
l
s. Insects may a
l
so enter
i
nto mutua
li
st
ic
re
l
at

i
ons
hi
ps w
i
t
h
ot
h
er spec
i
es. In anot
h
er
f
orm o
fi
nteract
i
on,
i
nsects may compete e
i
t
h
er
wi
t
h
ot

h
er mem
b
ers o
f
t
h
e spec
i
es or w
i
t
h
ot
h
er an
i
ma
l
s
f
or t
h
e same resource,
f
or examp
l
e,
f
ood, breedin

g
or e
gg
-la
y
in
g
sites, overwinterin
g
sites, or restin
g
sites. Between opposite
sexes of the same species, the interaction ma
y
be for a ver
y
obvious purpose, propa
g
atio
n
of
t
h
es
p
ec
i
es.
4
.1. Intraspec

ifi
c Interact
i
on
s
T
he nature and number of interactions amon
g
members of the same species will depen
d
o
n the density of the population. These interactions may be either beneficial or harmful. I
t
f
o
ll
ows t
h
at t
h
ere w
ill b
eanopt
i
ma
l
range o
fd
ens
i

ty
f
orag
i
ven popu
l
at
i
on, w
i
t
hi
nw
hi
c
h
t
h
e net e
ff
ect o
f
t
h
ese
i
nteract
i
ons w
ill b

e most
b
ene
fi
c
i
a
l
. Outs
id
et
hi
s range o
fd
ens
i
ty
,
that is, when there is underpopulation or overpopulation (crowdin
g
), the net result of these
i
nteractions will be less than o
p
timal for
p
er
p
etuation of the s
p

ecies. Animals have evolve
d
v
arious regulatory mechanisms that serve either to maintain this optimal density or to alter
t
h
eex
i
st
i
ng
d
ens
i
ty so as to
b
r
i
ng
i
tw
i
t
hi
nt
h
e opt
i
ma
l

range. In t
h
e
di
scuss
i
on t
h
at
f
o
ll
ow
s
i
tw
ill b
e seen
h
ow t
h
ese mec
h
an
i
sms operate
i
n some
i
nsects.

4.1.1. Under
p
o
p
ulation
P
ro
b
a
bl
yt
h
e most o
b
v
i
ous
d
etr
i
menta
l
e
ff
ect o
f
un
d
erpopu
l

at
i
on
i
st
h
e
i
ncrease
d diffi
-
c
u
l
ty o
fl
ocat
i
ng a mate
f
or
b
ree
di
ng purposes. For most spec
i
es, mate
l
ocat
i

on requ
i
res an
active search on the part of the members of one sex, which under conditions of underpop-
ulation mi
g
ht present a special problem for weakl
y
fl
y
in
g
insects. To alleviate this, man
y
species have evolved highly refined mechanisms (e.g., production of pheromones, sounds,
o
r
li
g
h
t) t
h
at
f
ac
ili
tate aggregat
i
on or
l

ocat
i
on o
fi
n
di
v
id
ua
l
so
f
t
h
e oppos
i
te sex (C
h
apter 19
,
S
ect
i
on 4.1). T
h
ere
l
at
i
ve

l
ys
li
g
h
tc
h
ance o
ffi
n
di
ng a mate
i
so
ff
set to some extent
b
yt
h
e
f
act that one matin
g
ma
y
suffice for fertilization of all e
gg
s a female ma
y
produce; that

i
s, sperm ma
y
remain viable for a considerable period, and a female ma
y
produce a lar
g
e
n
umber of eggs.
O
n some occas
i
ons t
h
ee
ff
ect o
f
non-spec
ifi
c pre
d
ators
i
s muc
h
greater w
h
en pre

y
d
ens
i
ty
i
s
l
ower t
h
an norma
lb
ecause t
h
ec
h
ance o
f
an
i
n
di
v
id
ua
l
prey organ
i
sm
b

e
i
ng eaten
i
s increased. For example, in the period 193
5
–1940 the population densit
y
of the Australia
n
pla
g
ue
g
rasshopper
,
A
ustroicetes cruciat
a
,
w
as hi
g
h. However, drou
g
ht conditions in th
e
7
03
THE BI

O
TI
C
ENVIR
O
NMEN
T
w
inter of 1940 resulted in a
g
reat shorta
g
eof
g
rasshopper food and a decline in population
numbers. Onl
y
a few small areas of land remained moist enou
g
h to support
g
rowth of
g
rass, and survivin
gg
rasshoppers con
g
re
g
ated in these areas. But so did the birds tha

t
norma
ll
y
f
e
d
on t
h
e
i
nsects an
d
t
h
ey re
d
uce
d
t
h
e popu
l
at
i
on
d
ens
i
ty to an extreme

l
y
l
ow
level (Andrewartha, 19
6
1).
Lower t
h
an norma
ld
ens
i
t
i
es ma
y
a
l
so
h
ave a ser
i
ous e
ff
ect
i
n spec
i
es t

h
at mo
dify
t
h
e
ir
environment, for example, social insects. The temperature and humidit
y
within the nest ar
e
normall
y
quite different from those outside, bein
g
re
g
ulated b
y
the activit
y
of members o
f
th
eco
l
ony. I
f
a proport
i

on o
f
t
h
e popu
l
at
i
on
i
s remove
d
or
d
estroye
d
,t
h
ose
i
n
di
v
id
ua
l
st
h
at
rema

i
n may no
l
onger
b
ea
bl
eto
k
eep t
h
e temperature an
dh
um
idi
ty at t
h
e
d
es
i
re
dl
eve
l
an
d
t
h
eco

l
ony may
di
e. Anot
h
er examp
l
e
i
st
h
e
l
esser gra
i
n
b
orer, R
h
izo
p
ert
h
a
d
ominica
(Coleoptera), which is a serious pest of stored
g
rain in the United States. In dama
g

ed
(cracked)
g
rain beetles can survive and reproduce even at low population densit
y
. However
,
in sound grain only cultures whose density is quite high will survive because the insect
s
th
emse
l
ves, t
h
roug
h
t
h
e
i
rc
h
ew
i
ng act
i
v
i
ty, can cause su
ffi

c
i
ent
d
amage to t
h
e gra
i
nt
h
at
i
t
b
ecomes su
i
ta
bl
e
f
or repro
d
uct
i
on. T
h
e nature o
f
t
hi

ssu
i
ta
bili
ty
i
sun
k
nown.
Below a certain level of population, the so-called “threshold densit
y
,” the chances of
survival for a population are slim because of the unlikelihood of a meetin
g
between insects
of o
pp
osite sex and in re
p
roductive condition. This is im
p
ortant in two areas of a
pp
lied
entomo
l
ogy, name
l
y, quarant
i

ne serv
i
ce an
dbi
o
l
og
i
ca
l
contro
l
. Quarant
i
ne regu
l
at
i
ons are
d
es
i
gne
d
so t
h
at
f
orag
i

ven pest t
h
e num
b
er o
fi
n
di
v
id
ua
l
s enter
i
ng a country over a per
i
o
d
of time is sufficientl
y
low that the chances of the pest establishin
g
itself are ver
y
slim.
I
n biolo
g
ical control pro
g

rammes that use insects as the controllin
g
a
g
ents, experience
shows that it is better to release the insects in a restricted area, especiall
y
if the
y
are
li
m
i
te
di
n num
b
er, rat
h
er t
h
an
di
str
ib
ut
i
ng t
h
em sparse

l
y,
i
nor
d
er to
i
mprove t
h
ec
h
ance
s
o
f
esta
bli
s
hi
ng a
b
ree
di
ng popu
l
at
i
on.
Popu
l

at
i
ons o
f
man
yi
nsect spec
i
es ma
yb
e cons
id
ere
d
se
lf
-re
g
u
l
at
i
n
g
;t
h
at
i
s, s
h

ou
ld
t
he densit
y
of the population fall below normal (thou
g
h not below threshold) it will, over
t
ime, return to its ori
g
inal level. There ma
y
be various reasons for this. As a species’
d
ens
i
ty
f
a
ll
s,
i
ts pre
d
ators may exper
i
ence greater
diffi
cu

l
ty
i
n
fi
n
di
ng
f
oo
d
so t
h
at t
h
ey
m
i
grate e
l
sew
h
ere or pro
d
uce
f
ewer young. As a resu
l
to
f

t
h
e
d
ec
li
ne
i
n pre
d
ator
d
ens
i
ty,
a
l
arger proport
i
on o
f
t
h
e prey spec
i
es may surv
i
ve to repro
d
uce. I

f
t
hi
s cont
i
nues
f
or severa
l
g
enerations, the ori
g
inal population densit
y
ma
y
be reestablished. Another possibilit
y
is
t
hat with a decrease in densit
y
, there will be a
g
reater choice of oviposition and, perhaps,
resting sites. Selection of the best of these sites will again increase the chances of surviva
l
o
f
an

i
nsect or
i
ts progeny an
dl
ea
d
to a popu
l
at
i
on
i
ncrease. Some spec
i
es
h
ave rat
h
er more
spec
ifi
c mec
h
an
i
sms
f
or overcom
i

ng t
h
e
di
sa
d
vantages o
f
un
d
erpopu
l
at
i
on. For examp
l
e,
females of some species use facultative partheno
g
enesis in the absence of males, which
serves not onl
y
to maintain continuit
y
of the population, but, as the pro
g
en
y
are
g

enerall
y
all female, any offspring that do find a mate can make a substantial contribution to the next
generat
i
on. In t
h
e
d
esert
l
ocust a
d
u
l
t
f
ema
l
es
i
nt
h
eso
li
tary p
h
ase (C
h
apter 21, Sect

i
on 7
)
li
ve
l
onger, so t
h
at t
h
ec
h
ance o
f
encounter
i
ngama
l
e
i
s
i
ncrease
d
an
d
,
f
urt
h

er, pro
d
uce up
t
o
f
our t
i
mes as man
y
e
gg
s compare
d
to
g
re
g
ar
i
ous
f
ema
l
es
.
4
.1.2.
O
verpopulat

i
o
n
As population densit
y
rises be
y
ond the normal level, members of a species will in-
creasin
g
l
y
compete with each other for such resources as oviposition sites, overwinterin
g
7
04
CHAPTER
23
sites, restin
g
places, and, occasionall
y
, food. Such competition ma
y
itself have a re
g
ulator
y
e
ffect, as a

p
ro
p
ortion of the
p
o
p
ulation will have to be satisfied with less than o
p
tima
l
c
onditions. Thus, if oviposition sites are mar
g
inall
y
suitable, few or no pro
g
en
y
ma
y
result
.
In
l
ess t
h
an a
d

equate overw
i
nter
i
ng s
i
tes,
i
nsects may
di
e
if
t
h
e weat
h
er
i
s severe. I
fi
nsects
c
annot
fi
n
d
proper rest
i
ng p
l

aces, t
h
e
i
rc
h
ances o
fdi
scovery
b
y pre
d
ators or paras
i
to
id
sar
e
i
ncrease
d
, as are t
h
e
i
rc
h
ances o
f dyi
n

gb
ecause o
f
un
f
avora
bl
e weat
h
er con
di
t
i
ons. As note
d
e
arlier (Section 2.1) food is seldom limitin
g
, thou
g
h under unusual circumstances it ma
y
become so
.
In a
ddi
t
i
on to t
h

e genera
l
regu
l
at
i
ng mec
h
an
i
sms
j
ust ment
i
one
d
, some
i
nsects regu
l
ate
population density in more specific ways. Migration (Chapter 22, Section
5
.2) is a mean
s
b
yw
hi
c
h

a spec
i
es may re
d
uce
i
ts popu
l
at
i
on
d
ens
i
ty. In suc
h
spec
i
es,
i
t
i
s crow
di
ng t
h
at
i
nduces the necessar
y

ph
y
siolo
g
ical and behavioral chan
g
es that put an insect into mi
g
rator
y
c
ondition. Crowdin
g
ma
y
also lead to reduction in fecundit
y
. For example, i
n
S
chistocerca
gregar
ia
gregarious females lay fewer eggs than solitary females because (1) their ovarie
s
c
onta
i
n
f

ewer ovar
i
o
l
es, (2) a sma
ll
er proport
i
on o
f
t
h
eovar
i
o
l
es pro
d
uce oocytes
i
n eac
h
o
var
i
an cyc
l
e [as a resu
l
to

f
(1) an
d
(2), eac
h
egg po
d
conta
i
ns
f
ewer eggs], an
d
(3) t
h
ey
h
ave
f
ewer ovarian c
y
cles (Kenned
y
,19
6
1). Likewise, in the mi
g
rator
yg
rasshopper, Melano

p
lus
s
angu
i
n
i
pe
s
,
matin
g
frequenc
y
, which is a function of population densit
y
, is inversel
y
related
to number of eggs produced and longevity (Pickford and Gillott, 1972)
.
Af
ew
ff
s
pec
i
es emp
l
oy a very o

b
v
i
ous means o
f
re
d
uc
i
ng crow
di
ng, name
l
y, cann
ib
a
l-
i
sm o
f
e
i
t
h
er t
h
e same or a
diff
erent
lif

e stage. In
l
arva
l
Zygoptera,
f
or examp
l
e, cann
ib
a
li
sm
o
f earlier instars is common under crowded conditions. For species whose larvae inhabit
small and/or temporar
y
ponds with limited food resources, cannibalism ma
y
be importan
t
i
n ensurin
g
that at least a proportion of the population reaches the adult sta
g
e. Another
c
onsequence
i

st
h
at stragg
l
ers are e
li
m
i
nate
d
,w
hi
c
h
resu
l
ts
i
n greater sync
h
rony o
f
a
d
u
l
t
e
mergence (see a
l

so C
h
apter 22, Sect
i
on 2.3). In t
h
e con
f
use
dfl
our
b
eet
l
e,
T
ri
b
o
l
ium con-
fusu
m
,
an
d
some ot
h
er
b

eet
l
e spec
i
es, a
ll
o
f
w
h
ose
lif
e sta
g
es are spent
i
n
g
ra
i
nor
i
ts
products, e
gg
cannibalism occurs. Adults eat an
y
e
gg
s the

y
find, and, therefore, the hi
g
her
the adult population densit
y
, the
g
reater the number of e
gg
s consumed
.
In some spec
i
es o
fi
nsects t
h
at
i
n
h
a
bi
ta
h
omogeneous env
i
ronment, popu
l

at
i
on
d
ens
i
ty
i
sregu
l
ate
db
yma
ki
ng t
h
eenv
i
ronment
l
ess su
i
ta
bl
e
f
or growt
h
. For examp
l

e,
T
.
con
f
usu
m
l
arvae an
d
a
d
u
l
ts “con
di
t
i
on” t
h
e
fl
our
i
nw
hi
c
h
t
h

ey
li
ve. As a resu
l
t, a sma
ll
er proport
i
o
n
o
f the larvae survive to maturit
y
, and the duration of the larval sta
g
e is increased. The nature
o
f this conditionin
g
is not known.
In some species, regulation of population density is achieved by having individuals that
d
om
i
nate ot
h
ers so t
h
at t
h

e repro
d
uct
i
ve capac
i
ty o
f
t
h
e
l
atter
i
se
i
t
h
er re
d
uce
d
or tota
ll
y sup
-
presse
d
.T
hi

s
i
s seen most c
l
ear
l
y
i
n soc
i
a
l
Hymenoptera w
h
ere one
i
n
di
v
id
ua
l
,t
h
e queen,
dominates the other members of the colon
y
, which are mostl
y
female. In more primitive

species, dominance is achieved initiall
y
b
y
ph
y
sical a
gg
ression, thou
g
h in time the subor
-
dinates recognize the queen by scent and consequently avoid her. In highly social forms,
suc
h
as t
h
e
h
oney
b
ee,
d
om
i
nance
i
s asserte
d
ent

i
re
l
yt
h
roug
h
t
h
ere
l
ease o
f
p
h
eromones
.
In many spec
i
es,
d
om
i
nance
h
as ta
k
en on anot
h
er

f
orm, name
l
y, terr
i
tor
i
a
li
ty, t
h
e
d
e
f
ense o
f
a part
i
cu
l
ar area. T
h
es
i
ze o
f
t
h
e area

d
e
f
en
d
e
d
(terr
i
tor
y
)ma
y
var
y
,
b
ut no
t
below a minimum value, so that a maximum population densit
y
is attained. Territorialit
y
i
s shown b
y
insects in a number of orders, both primitive and advanced, and is t
y
picall
y

assoc
i
ate
d
w
i
t
h
some as
p
ect o
f
re
p
ro
d
uct
i
on. Most o
f
ten ma
l
es esta
bli
s
h
terr
i
tor
i

es an
d
d
e
f
en
d
t
h
em aga
i
nst ot
h
er ma
l
es, usua
ll
y
b
yc
h
as
i
ng an
dfi
g
h
t
i
ng

b
ut occas
i
ona
ll
y
b
y non
-
a
gg
ress
i
ve means suc
h
as c
hi
rp
i
n
gi
n some Ort
h
optera. Fema
l
es enter ma
l
es’ terr
i
tor

i
es
f
o
r
7
05
THE BI
O
TI
C
ENVIR
O
NMEN
T
matin
g
and oviposition. Amon
g
Odonata, where matin
g
immediatel
y
precedes e
gg
la
y
in
g
,

males also protect females as the
y
oviposit.
Territorialit
y
with respect to food availabilit
y
ma
y
be seen in some species, especiall
y
p
aras
i
to
id
san
d
soc
i
a
li
nsects. For exam
pl
e,
f
ema
l
e
i

c
h
neumons,
b
racon
id
s, c
h
a
l
c
idid
s, an
d
sce
li
on
id
s (Hymenoptera) may mar
k
t
h
e
h
ost e
i
t
h
er c
h

em
i
ca
ll
yorp
h
ys
i
ca
ll
yast
h
ey ov
i
pos
it
so t
h
at ot
h
er
f
ema
l
es o
f
t
h
e spec
i

es
d
o not
l
a
yi
nt
h
e same
h
ost. Suc
hb
e
h
av
i
or ensures t
h
a
t
t
he offsprin
g
will have adequate food for complete development. (The marks ma
y
also be
t
he means b
y
which h

y
perparasites locate a host!) Social insects defend both their nest an
d
f
orag
i
ng s
i
tes aga
i
nst mem
b
ers o
f
ot
h
er co
l
on
i
es
.
4.2. Inters
p
ecific Interactions
4
.2.1. Com
p
etition and Coexistence
An

i
mportant
f
orm o
fi
nteract
i
on
i
sw
h
en an
i
nsect competes w
i
t
h
ot
h
er organ
i
sms
f
o
r
th
e same resources. Grass
h
oppers, s
h

eep, an
d
ra
bbi
ts a
ll
eat
g
rass, an
dif
t
hi
s
i
s
i
ns
h
ort
suppl
y
the presence of the mammalian herbivores will have a ver
y
obvious effect on th
e
d
istribution and abundance of
g
rasshoppers livin
g

in the same area. However, as noted
ear
li
er,
f
oo
di
sse
ld
om a
li
m
i
t
i
ng
f
actor as
f
ar as t
h
ea
b
un
d
ance o
f
an
i
ma

l
s
i
s concerne
d
,
an
d
t
h
eot
h
er requ
i
rements o
f
t
h
ese t
h
ree spec
i
es are so
diff
erent t
h
at t
h
e spec
i

es can
coex
i
st per
f
ect
ly
we
ll
.T
h
eco
ll
ect
i
on o
f
requ
i
rements t
h
at must
b
e sat
i
s
fi
e
di
nor

d
er
f
or
a
species to survive and reproduce under natural conditions is described as a niche. Thus,
a
niche includes both ph
y
sical and biotic requirements, and its complexit
y
varies wit
h
t
he environment in which a s
p
ecies finds itself. For exam
p
le, as noted in Cha
p
ter 22,
Sect
i
on 3.2.3, t
h
ecr
i
t
i
ca

ld
ay
l
engt
hf
or
i
n
d
uct
i
on o
fdi
apause
i
n a spec
i
es may vary w
i
t
h
l
at
i
tu
d
e. Equa
ll
y, w
i

t
h
re
f
erence to
bi
ot
i
c requ
i
rements, t
h
e comp
l
ex
i
ty o
f
an
i
c
h
ew
ill diff
er
accordin
g
to the number and nature of other species utilizin
g
the same resources. The more

closel
y
two species are related, the more nearl
y
identical will be their requirements (i.e.
,
t
heir niche), and the greater will be the degree of competition between them where the two
spec
i
es coex
i
st. Norma
ll
y,
i
nt
hi
ss
i
tuat
i
on t
h
e
l
ess we
ll
-a
d

apte
d
spec
i
es
b
ecomes ext
i
nct or
restr
i
cte
d
to areas w
h
ere
i
t can aga
i
n compete
f
avora
bl
yw
i
t
h
t
h
eot

h
er spec
i
es as a resu
lt
of different environmental conditions, a phenomenon known as competitive exclusion or
d
is
p
lacement. In the absence of com
p
etition, a s
p
ecies’ niche will be broader (less com
p
lex)
;
t
hat is, a species’ requirements will be less strin
g
ent and form the so-called “fundamental
”
n
i
c
h
e. Converse
l
y, t
h

en
i
c
h
e occup
i
e
db
y a spec
i
es t
h
at coex
i
sts w
i
t
h
ot
h
ers
i
s
k
nown as t
he
“rea
li
ze
d

”n
i
c
h
e
.
Awe
ll
-
d
ocumente
d
examp
l
eo
f
compet
i
t
i
ve exc
l
us
i
on
i
n
i
nsects
i

nvo
l
ves t
h
ree spec
i
e
s
of chalcidid, belon
g
in
g
to the
g
enu
s
A
phytis, which are
p
arasitoids of the California red scale,
A
onidiella aurantii, found on citrus fruits. In the earl
y
1900s, the
g
olden chalcidid,
A
phytis
ch
r

y
somp
h
a
l
i
,
w
a
s acc
id
enta
ll
y
i
ntro
d
uce
di
nto sout
h
ern Ca
lif
orn
i
a, pro
b
a
bl
ya

l
ong w
i
t
h
re
d
sca
l
e on nursery stoc
ki
mporte
df
rom t
h
eMe
di
terranean reg
i
on, t
h
oug
hi
t
i
s a nat
i
ve o
f
China. Durin

g
the next
5
0
y
ears
,
A
.c
h
r
y
somp
h
a
li
sprea
d
a
l
on
g
w
i
t
hi
ts
h
ost t
h

rou
gh
out t
h
e
citrus-
g
rowin
g
area and exerted a reasonable de
g
ree of control over red scale, particularl
y
i
n
t
he milder coastal areas. However, in 1948, a second s
p
ecies, also Chinese, A. lingnaneni
s
,
w
a
s
introduced in the hope of obtaining even better control of the pest. During the 1950s,
A
.
l
in
g

nanensi
s
gra
d
ua
ll
y
di
sp
l
ace
d
A. c
h
r
y
somp
h
a
l
i so that, by 1961, the latter was virtually
ext
i
nct,
b
e
i
ng restr
i
cte

d
to a
f
ew sma
ll
areas a
l
ong t
h
e coast. However,
A
.
l
in
g
nanensi
s
w
as
ineffective as a control a
g
ent of red scale in the inland citrus-
g
rowin
g
areas around San
70
6
CHAPTER
23

F
I
GU
RE 23.5. C
h
an
g
es
i
nt
h
e
di
str
ib
ut
i
on o
f
A
p
h
ytis c
h
rysomp
h
a
l
i
,

A
.
l
ingnanensi
s
,
an
d
A
.me
l
inu
s
i
n sout
h
ern
C
alifornia between 1948 and 1965. [After P. DeBach and R. A. Sundby, 1963, Competitive displacement betwee
n
e
co
l
og
i
ca
lh
omo
l
ogues,

H
i
l
gar
d
i
a
34
:
105–166. By permission of Agricultural Sciences Publications, Universit
y
of
Ca
lif
orn
i
a; an
d
P. DeBac
h
, D. Rosen, an
d
C. E. Kennet, 1971, B
i
o
l
o
gi
ca
l

contro
l
o
f
cocc
id
s
by i
ntro
d
uce
d
n
atural enemies, in: Biolo
g
ical Control (C. B. Huffaker, ed.). By permission of Plenum Publishing Corporatio
n
an
d
t
h
e aut
h
ors.
]
Fernando, San Bernadino, and Riverside, where annual climatic chan
g
es are
g
reater. It was

f
ound, for exam
p
le, that
p
eriods of cool weather (1
8
◦
C
or
l
ess for 1 or 2 weeks
)
or several
n
ights of hard frost caused high mortality of all stages. Even light overnight frosts
(
−
1
◦
C
f
or 8
h
ours)
kill
e
d
sperm
i

nt
h
e spermat
h
ecae o
ff
ema
l
es, w
hi
c
h did
not mate aga
i
n, an
d
r
endered males sterile. Also, exposure of females to a temperature of 1
5
◦
Cf
or 24
h
ours
l
e
d
to an increase in proportion of male pro
g
en

y
. These factors caused a reduction in “effectiv
e
p
ro
g
en
y
production” (number of female offsprin
g
produced per female) from 21.4 to 4.5
a
nd a resultant inability of the species to control red scale populations. Consequently, a
t
hi
r
d
spec
i
es, A. me
l
inu
s
,
w
as introduced from India and Pakistan in 1
95
6 and 1
95
7. This

s
pec
i
es rap
idl
y
di
sp
l
ace
d
A
.
l
in
g
nanensi
s
f
rom these inland areas, and by 19
6
1 virtually
the entire population of chalcidids in these areas was made up of
A
. melinu
s
(
DeBach and
Rosen, 1991). Chan
g

es in the distribution of the three
A
phytis s
p
ecies between 1948 an
d
1
965 are summarized in Fi
g
ure 23.5.
Compet
i
t
i
ve
di
sp
l
acement
d
oes not a
l
ways occur,
h
owever,
b
ecause c
l
ose
l

yre
l
ate
d
o
rgan
i
sms
h
ave evo
l
ve
d
mec
h
an
i
sms t
h
at ena
bl
et
h
em to occupy a
l
most
b
ut not qu
i
te t

he
s
ame n
i
c
h
e. T
h
ese mec
h
an
i
sms
i
nc
l
u
d
e
h
a
bi
tat se
l
ect
i
on (spat
i
a
l

se
l
ect
i
on), m
i
cro
h
a
bi
tat
s
election, temporal (diurnal and seasonal) se
g
re
g
ation, and dietar
y
differences. Two or mor
e
o
f these mechanisms ma
y
operate simultaneousl
y
to prevent competition between species.
Spat
i
a
l

segregat
i
on
i
ss
h
own
b
yt
h
e
di
str
ib
ut
i
on o
f
A
.
l
in
g
nanensis
a
n
d
A
.me
l

inu
s
in
s
out
h
ern Ca
lif
orn
i
a, w
hi
c
h
DeBac
h
an
d
Rosen (1991) cons
id
ere
d
to
h
ave sta
bili
ze
d
,w
i

t
h
A.
l
in
g
nanensis occup
yi
n
g
t
h
em
ild
er (
l
ess c
li
mat
i
ca
lly
extreme) coasta
ldi
str
i
cts an
d
A
.

melinus
t
he interior. Spatial separation is also seen in larval damselflies (Z
yg
optera), which
7
07
THE BI
O
TI
C
ENVIR
O
NMEN
T
F
I
G
URE 23.5.
(
Continue
d
)
i
n
h
a
bi
t pra
i

r
i
e pon
d
s. For examp
l
e, two spec
i
es o
f
Coenagr
i
on
id
ae,
C
oena
g
rion reso
l
u-
tu
m and Enalla
g
ma boreale
,
hatch, develop, and emer
g
e as adults almost s
y

nchronousl
y
.
However, the s
p
ecies can coexist because larval
E. bo
r
eale
a
re restricted to dee
p
,o
p
en
w
ater, while C
.
r
esolutum
o
ccurs in shallow water with emer
g
ent ve
g
etation (Sawch
y
nan
d
G

illott, 197
5
).
Pr
i
ce (1997) prov
id
e
d
severa
l
examp
l
es o
f
m
i
cro
h
a
bi
tat se
l
ect
i
on t
h
at ena
bl
ec

l
ose
ly
re
l
ate
d
spec
i
es to coex
i
st. In En
gl
an
d
, two spec
i
es o
f
Psocoptera,
M
eso
p
socus immuni
s
an
d
M. uni
p
unctatus, coexist on larch twi

g
s with no readil
y
obvious differences in their biolo
gy
.
7
08
CHAPTER
23
S
tudies revealed, however, that the species oviposit in different microhabitats.
M
. immuni
s
p
refers to ovi
p
osit in the axils of dwarf side shoots, whereas M. un
ip
unctatus selects
g
irdl
e
scars and leaf scars. The con
g
eneric flea beetles,
P
hyllotreta cruci
f

erae
a
n
d
P.
striolat
a
,
are concentrate
d
on
diff
erent
p
arts o
f
t
h
e
i
r
f
oo
dpl
ant, Bra
ss
ica o
l
erace
a

(ca
bb
age an
d
re
l
at
i
ves). T
h
e
f
ormer spec
i
es s
h
ows a pre
f
erence
f
or sunny
l
ocat
i
ons an
d
occurs
l
arge
l

yon
t
h
e upper sur
f
ace o
f
top an
d
m
iddl
e
l
eaves. P
.
s
trio
l
ata
i
s concentrate
d
on t
h
eun
d
ers
id
eo
f

leaves, especiall
y
those near the base of the plant.
D
iurnal se
g
re
g
ation is shown b
y
two species o
f
Andrena
,
A
. rozen
i
a
n
d
A
. chylismiae
,
so
li
tary
b
ees t
h
at

f
orage on even
i
ng pr
i
mrose (Oenot
h
era c
l
avae
f
ormi
s
)
w
h
ose
fl
ower
s
rema
i
n
i
n
bl
oom
f
or
l

ess t
h
an a
d
ay. F
l
owers open
i
n
l
ate a
f
ternoon an
d
are v
i
s
i
te
dby
A. ro
z
en
i
b
etween about 1
6
00 and 1
9
00 hours. A. c

hyl
ismiae
i
sanear
l
y morn
i
ng
f
orage
r
and visits flowers between 0500 and 0800 hours, that is,
j
ust before the
y
wilt
.
Clear-cut seasonal se
g
re
g
ation is shown b
y
the damselflies studied b
y
Sawch
y
nan
d
Gillott (1974a,b, 1975), who were able to arrange the damselflies into three types according

to t
h
e
i
r seasona
lbi
o
l
ogy. Type A spec
i
es, w
hi
c
hi
nc
l
u
d
es
C
oena
g
rion reso
l
utum
,
E
na
ll
a

g
ma
b
orea
le
,an
d
ot
h
er Coenagr
i
on
id
ae, overw
i
nter
i
n
di
apause as we
ll
-
d
eve
l
ope
dl
arvae an
d
e

mer
g
ehi
g
hl
y
s
y
nchronousl
y
between the last week of Ma
y
and mid-June. Sexual matu
-
ration takes about 1 week and the oviposition period extends to the end of Jul
y
. Females
lay eggs in the submerged parts of floating plants. Embryogenesis is direct and requires
l
ess t
h
an 3 wee
k
s;
h
a
lf
-grown
l
arvae may

b
eco
ll
ecte
db
e
f
ore t
h
een
d
o
f
Ju
l
yan
d
mature
l
arvae
b
ym
id
-Septem
b
er. Inc
l
u
d
e

di
n Type B are t
h
ree spec
i
es o
f
L
e
s
te
s
:
L. un
g
uicu
l
atus
,
L
. disjunctus
,
and L. dr
y
a
s
, which overwinter in diapause as well developed embr
y
os. E
ggs

hatch s
y
nchronousl
y
durin
g
earl
y
Ma
y
, but the ver
yy
oun
g
larvae are not pre
y
ed on b
y
the lar
g
er larvae of T
y
pe A species either because the
y
are too small, that is, outside the
range o
f
prey s
i
ze, or

b
ecause t
h
e Type A
l
arvae
h
ave cease
d
to
f
ee
di
n preparat
i
on
f
or
t
h
e
fi
na
l
mo
l
t. Type B
l
arvae
d

eve
l
op rap
idl
y, an
d
sync
h
ron
i
ze
d
a
d
u
l
t emergence
b
eg
i
ns
i
n earl
y
Jul
y
and is completed within 2 weeks. Adult maturation requires 1
6
–18 da
y

s, an
d
f
emales oviposit in
g
reen emer
g
ent stems o
f
S
cir
p
u
s
(bulrush), which ma
y
relate to the
requirement of water for embr
y
o
g
enesis. Adults are not normall
y
seen after the end of
A
ugust, t
h
oug
hi
nm

ild
years t
h
ey may surv
i
ve
i
nto Octo
b
er. In Type C
i
s
i
nc
l
u
d
e
d
on
e
spec
i
es
,
Lestes con
g
ener,w
hi
c

hi
sc
h
aracter
i
ze
db
yt
h
e
l
ateness o
fi
ts seasona
l
c
h
rono
l
ogy.
L
. con
g
ene
r
ov
e
rw
i
nters

i
n
di
apause at an ear
l
y (pre
bl
asto
ki
net
i
c) stage o
f
em
b
ryogenes
i
s.
E
mbr
y
onic development continues in the sprin
g
after the e
gg
s are wetted and hatchin
g
o
ccurs at the end of Ma
y

. However, the
y
oun
g
larvae are too small to serve as pre
y
for the
Type B species. Larval development is rapid in
L
. congener so that synchronized emer
-
gence
b
eg
i
ns
i
n
l
ate Ju
l
yan
d
cont
i
nues
f
or a
b
out 3 wee

k
s. T
h
e muc
hl
arger
l
arvae o
f
L
. con
g
ene
r
g
enera
ll
y
d
o not eat
l
arvae o
f
Type A spec
i
e
s
.
Sexua
l

maturat
i
on
i
n L. con-
gener
takes about 3 weeks. Oviposition be
g
ins in mid-Au
g
ust and copulatin
g
adults ma
y
b
e seen until earl
y
October. Femal
e
L
. congene
r
oviposit onl
y
in dr
y
stems o
f
S
cir

p
us,
a
f
eature associated with the lack of prediapause embryonic development observed in thi
s
s
p
ec
i
es
.
Th
us, t
h
e occurrence o
f
seasona
l
segregat
i
on
b
etween types an
d
o
f
m
i
cro

h
a
bi
tat seg
-
re
g
at
i
on (e.
g
.,
d
eep versus s
h
a
ll
ow water
f
or
l
arvae, an
d
ov
i
pos
i
t
i
on

i
n
fl
oat
i
n
g
ve
g
etat
i
on
,
o
r emer
g
ent
g
reen or dr
y
stems in adults) both between and within t
y
pes, enables a numbe
r
o
f species of Z
yg
optera to coexist and make use of the rich food suppl
y
(in the form o

f
D
ap
h
nia, D
i
aptomu
s
,an
d dip
teran
l
arvae) w
hi
c
hi
s
f
oun
di
n
p
ra
i
r
i
e
p
on
d

s
.
Di
etary
diff
erences a
l
so ena
bl
ec
l
ose
l
yre
l
ate
d
spec
i
es to coex
i
st. For examp
l
e,
l
arvae
of
t
h
eca

ddi
s
fli
es P
y
cnops
y
c
h
e
g
enti
l
i
s
an
d
P.
lucule
n
ta
coex
i
st
i
nwoo
dl
an
d
streams

in
7
09
THE BI
O
TI
C
ENVIRONMEN
T
Quebec because the former prefers fallen leaves, whereas
P.
lucule
n
ta
feeds on submer
g
e
d
t
wi
g
s or, if these are not available, on detritus or well-rotted leaves (MacKa
y
an
d
Kalff, 1973).
4
.2.2. Predator-Prey Relat
i
onsh

i
p
s
I
t will be abundantl
y
clear that the distribution and abundance of a species will be
g
reatl
y
affected b
y
those or
g
anisms that use it as food and that the reverse is also true
,
name
l
y, t
h
at t
h
e
di
str
ib
ut
i
on an
d

a
b
un
d
ance o
f
prey w
ill d
eterm
i
ne t
h
e
di
str
ib
ut
i
on an
d
a
b
un
d
ance o
f
pre
d
ators.
Most Insecta

f
ee
d
on p
l
ant mater
i
a
li
n one
f
orm or anot
h
er, t
h
at
i
s, are pr
i
mar
y
con
-
sumers, and therefore pla
y
ama
j
or role in the flow of ener
gy
stored in plants to hi

g
he
r
t
rophic levels. However, another lar
g
e
g
roup, probabl
y
about 10% of known species, feed
on ot
h
er an
i
ma
l
s, espec
i
a
ll
y
i
nsects. Some o
f
t
h
ese are typ
i
ca

l
pre
d
ators or paras
i
tes,
b
ut t
he
ma
j
or
i
ty are paras
i
to
id
st
h
at
b
e
l
ong espec
i
a
ll
ytot
h
eTac

hi
n
id
ae (D
i
ptera), Streps
i
ptera, an
d
so-ca
ll
e
d
“paras
i
t
i
c” H
y
menoptera (C
h
apter 10, Sect
i
on 7). A paras
i
to
id
ma
yb
e

d
e
fi
ne
d
as “an insect that requires and eats onl
y
one animal in its life span, but ma
y
be ultimatel
y
responsible for killin
g
man
y
” (Price, 1997, p. 141). T
y
picall
y
, a female parasitoid deposits
as
i
ng
l
e egg or
l
arva on eac
hh
ost, w
hi

c
hi
st
h
en gra
d
ua
ll
y eaten as t
h
eo
ff
spr
i
ng
d
eve
l
ops
.
A
d
u
l
t paras
i
to
id
s are
f

ree-
li
v
i
ng an
d
e
i
t
h
er
d
o not
f
ee
d
or su
b
s
i
st on nectar an
d
/or po
ll
en.
Th
us, a paras
i
to
id diff

ers
f
romat
y
p
i
ca
l
pre
d
ator, w
hi
c
hf
ee
d
sonman
y
or
g
an
i
sms
d
ur
i
n
g
its life, and a parasite, which ma
y

feed on one to several host individuals but does not kil
l
t
hem. However, as Price (1997)
p
ointed out, the distinction between
p
redator and
p
arasitoi
d
i
s not a
l
ways c
l
ear. For examp
l
e, a
bi
r
d
t
h
at captures
i
nsects as
f
oo
df

or
i
ts o
ff
spr
i
ng
is
compara
bl
ew
i
t
h
a paras
i
to
id
t
h
at
l
ays
i
tseggona
f
res
hl
y
kill

e
d
or para
l
yze
dh
ost. Furt
h
er,
a pre
d
ator an
d
paras
i
to
id f
ace t
h
e same pro
bl
em, name
ly
,
l
ocat
i
on o
f
pre

y
(
h
ost), an
d
ma
y
solve the problem in an identical manner. Of course, from the pre
y
’s point of view, it mat-
t
ers not whether the a
gg
ressor is predator or parasitoid; for either, it must take appropriate
steps to avoid being eaten! In the final analysis, the population dynamics of predator-pre
y
an
d
paras
i
to
id
-
h
ost re
l
at
i
ons
hi

ps w
ill b
e
id
ent
i
ca
l
,an
di
t
i
st
h
ere
f
ore appropr
i
ate to
di
scus
s
th
ese re
l
at
i
ons
hi
ps un

d
er t
h
e same
h
ea
di
ng. In t
h
e rema
i
n
d
er o
f
t
hi
s sect
i
on, t
h
ere
f
ore, t
h
e
t
erms “predator” and “pre
y
” should be taken to include “parasitoid” and “host,” respectivel

y
,
except where specificall
y
stated otherwise.
First, what strategies are employed by prey species in order to reduce the chances of their
mem
b
ers
b
e
i
ng eaten? Pro
b
a
bl
y, t
h
e most o
b
v
i
ous strategy
i
s
f
or
i
nsects to avo
id d

etect
i
on
.
Thi
st
h
ey may
d
o
i
nvar
i
ous ways—
b
y
b
urrow
i
ng
i
ntoasu
b
strate, w
hi
c
hf
requent
l
ya

l
s
o
serves as food, b
y
hidin
g
, for example, on the underside of leaves, b
y
becomin
g
active for
a restricted period of the da
y
, or throu
g
h camoufla
g
e where their color pattern mer
g
es with
t
he back
g
round on which the
y
normall
y
rest, or the
y

precisel
y
resemble a twi
g
or leaf of
th
e
i
r
f
oo
d
p
l
ant. Ot
h
er prey spec
i
es
h
ave evo
l
ve
d
ot
h
er protect
i
ve mec
h

an
i
sms t
h
at
d
epen
d
on
i
n
i
t
i
a
l
recogn
i
t
i
on o
f
t
h
e prey
b
yt
h
e pre
d

ator
f
or t
h
e
i
re
ff
ect
i
veness. Suc
h
mec
h
an
i
sms
i
nc
l
u
d
e
b
e
i
n
gdi
staste
f

u
l
,a
f
eature usua
lly
accompan
i
e
dby
aposemat
i
c (warn
i
n
g
)co
l
orat
i
on
so that a predator soon learns to reco
g
nize that species are distasteful. Related to this i
s
M
ullerian mimicry in which distantly related, distasteful species resemble each other, so
¨
th
at

if
a pre
d
ator recogn
i
zes t
h
e
i
r pattern o
f
co
l
orat
i
on a
ll
spec
i
es are protecte
d
. Anot
h
e
r
f
orm o
f
m
i

m
i
cry
i
s Bates
i
an,
i
nw
hi
c
h
an e
dibl
e spec
i
es (t
h
em
i
m
i
c) comes to resem
ble
a
di
staste
f
u
l

spec
i
es (t
h
emo
d
e
l
)(F
ig
ure 9.33). T
h
e success o
f
t
hi
s met
h
o
d
o
f
avo
idi
n
g
predation relies on the probabilit
y
of the predator selectin
g

the distasteful model rather tha
n
7
10
CHAPTER
23
the edible mimic; that is, the population densit
y
of the model must
g
reatl
y
outwei
g
h tha
t
o
f the mimic. Another chemical method of defense is to secrete obnoxious li
q
uid or va
p
or
w
hose odor re
p
els
p
redators. Other s
p
ecies release

p
oisons that, on contact with skin or
wh
en
i
n
j
ecte
db
y means o
f
sp
i
nes,
h
a
i
rs, or st
i
ng,
i
n
j
ure or
kill
t
h
e attac
k
er (B

l
um, 1981)
.
Some
i
nsects, espec
i
a
ll
y spec
i
es o
fb
utter
fli
es, pract
i
ce
i
nt
i
m
id
at
i
on
di
sp
l
ays a

i
me
d
at
f
r
igh
ten
i
n
g
wou
ld
-
b
e (verte
b
rate) pre
d
ators. T
h
e
b
utter
fli
es norma
lly
rest w
i
t

h
t
h
e
i
rw
i
n
gs
c
losed verticall
y
above the bod
y
. On bein
g
disturbed, the butterflies rapidl
y
open their win
g
s
to reveal a strikin
g
color pattern, often includin
g
lar
g
e“e
y
espots,” intended to evoke promp

t
retreat o
f
t
h
e aggressor
.
P
re
d
ators use a var
i
ety o
f
st
i
mu
li i
nor
d
er to
l
ocate prey. Some may attempt to capture
an
d
eat anyt
hi
ng t
h
at moves w

i
t
hi
n a certa
i
ns
i
ze range an
d
emp
l
oy on
l
ys
i
mp
l
ev
i
sua
l
o
r
m
echanical cues for detection of pre
y
. Most species are, however, relativel
y
pre
y

-specifi
c
(
feed on onl
y
afeworasin
g
le species of pre
y
), and pre
y
location is therefore a muc
h
m
ore elaborate process. For many of these more specialized predators, the first step is
l
ocat
i
on o
f
t
h
e prey’s
h
a
bi
tat, an
d
t
hi

s
i
so
f
ten ac
hi
eve
d
as a resu
l
to
f
attract
i
on to o
d
or
s
re
l
ease
df
rom t
h
e
f
oo
d
o
f

t
h
e prey. For examp
l
e,
f
ema
l
es o
f
t
h
e
i
c
h
neumon
fl
y
,
Ito
pl
ectis
c
on
q
uisito
r
,a
p

arasitoid, are attracted b
y
the odor of pine oil, especiall
y
that of Scots pin
e
(
P
inus sylvestri
s
)
, on which one of its
p
referred hosts, cater
p
illars of the Euro
p
ean
p
in
e
shoot moth, Rhyacionia buolian
a
, are found. For some predators, attraction is greater afte
r
t
h
e
f
oo

d
o
f
t
h
e prey
h
as
b
een
d
amage
db
yt
h
e prey. T
h
e pteroma
lid
Nason
i
av
i
tr
i
penn
i
s,
f
o

r
e
xamp
l
e,
i
s attracte
d
to meat, espec
i
a
ll
yw
h
en t
hi
s
h
as
b
een contam
i
nate
db
yt
h
e paras
i
to
id

’s
hosts, various muscid flies. Similarl
y
, the ichneumo
n
N
emeritis
(
=
V
enturia
)
cane
s
cen
s
i
s
m
ore attracted to oatmeal contaminated b
y
its host, larvae of the Mediterranean flour moth,
Ephestia k
uhniella
¨
,
than to clean oatmeal (Vinson, 1975).
Hav
i
ng

b
een attracte
d
to t
h
e
h
a
bi
tat o
fi
ts prey, a pre
d
ator must now spec
ifi
ca
ll
y
l
ocat
e
t
h
e prey. For many spec
i
es t
hi
s
i
nvo

l
ves a systemat
i
c searc
h
,t
h
oug
h
t
hi
s
b
e
h
av
i
or
i
s
i
n
i
-
t
i
ate
d
on
ly

a
f
ter rece
i
pt o
f
an appropr
i
ate s
ig
na
l
t
h
at
i
n
di
cates t
h
e
lik
e
lih
oo
d
o
f
pre
yi

n
the immediate area. A
g
ain, such si
g
nals are usuall
y
chemical in nature and include odor
s
f
rom the pre
y
’s feces or from the dama
g
ed tissues of the pre
y
’s food plant. Pheromones
re
l
ease
db
yt
h
e
h
ost are o
f
ten use
db
y paras

i
to
id
sto
l
ocate t
h
e
h
ost (Powe
ll
, 1999; Powe
ll
an
d
Poppy, 2001; an
d
see C
h
apter 13, Sect
i
on 4.2). F
i
na
ll
ocat
i
on o
f
prey

i
s common
l
y
ac
hi
eve
db
y means o
fi
ts taste, rare
l
y
b
y
i
ts o
d
or (e
ff
ect
i
ve on
l
yoveraverys
h
ort
di
stance)
.

S
ome parasitoids locate hosts b
y
the vibrations or sounds the latter make as the
y
burro
w
throu
g
h the substrate
.
In some species, location of prey is followed immediately by feeding or, in parasitoids,
o
v
i
pos
i
t
i
on or
l
arv
i
pos
i
t
i
on. In ot
h
ers, a

ddi
t
i
ona
l
st
i
mu
li
must
b
e rece
i
ve
db
e
f
ore prey
i
s
d
eeme
d
accepta
bl
e. T
h
ese appear to
b
e espec

i
a
ll
ycr
i
t
i
ca
li
n paras
i
to
id
s
f
or w
hi
c
h
se
l
ect
i
on
o
f hosts of the correct a
g
e(
j
ud

g
ed b
y
size, color, shape, texture, or taste) ma
y
b
y
important
.
Fo
re
xample, some parasitoids accept onl
y
hosts above a certain size; c
y
lindrical host
sha
p
eim
p
roved acce
p
tance in the ichneumon
P
impla instigator
;
hairiness of the host (by
pre
f
erence, caterp

ill
ars o
f
t
h
e gypsy mot
h
, L
y
mantria
d
ispar)
i
sa
n
i
m
p
ortant
d
eterm
i
nan
t
of
accepta
bili
ty
i
nt

h
e
b
racon
id
Ap
ante
l
es me
l
anosce
l
us
;
an
df
ema
le
I
top
l
ectis conquisito
r
pro
b
e
h
ost
l
arvae w

i
t
h
t
h
e
i
rov
i
pos
i
tor
b
ut w
ill l
a
y
e
gg
son
ly if
t
h
e
h
ost’s
h
emo
ly
mp

hh
as a
suitable taste. Movement ma
y
be an important stimulant or deterrent of acceptabilit
y
. Some
parasitoids oviposit onl
y
if a larval host moves, whereas movement of an embr
y
o within
an egg (
i
n
di
cat
i
ve o
f
t
h
e egg’s age) may
i
n
hibi
tov
i
pos
i

t
i
on
b
y egg paras
i
to
id
s(V
i
nson,
1
97
5
, 1976). A special feature of many parasitoids is their ability to discriminate between
n
on-paras
i
t
i
ze
d
an
d
paras
i
t
i
ze
dh

osts on t
h
e
b
as
i
so
f
p
hy
s
i
ca
l
mar
ki
n
g
s, o
d
ors, or taste
s
7
11
THE BI
O
TI
C
ENVIR
O

NMEN
T
F
I
GU
RE 23.6
.
Ant feeding on honeydew exuded from the anus of a treehopper (Membracidae). [Photograp
h
courtesy o
f
Dan L. Per
l
man.
]
left b
y
the ori
g
inal parasitoid as it oviposited or larviposited. Such marks render a host
u
nacceptable to the parasitoids that locate it subsequentl
y
and ensure that the parasitoid
larva, on hatching, has sufficient food for its complete development. Other parasitoids leav
e
t
ra
il
-mar

ki
ng p
h
eromones as t
h
ey searc
hf
or
h
osts, w
hi
c
hi
n
hibi
t researc
hi
ng o
f
an area an
d
th
ere
b
y
f
ac
ili
tate
di

spersa
l
o
f
t
h
e spec
i
es
.
W
hen
g
iven a choice a predator ma
y
consistentl
y
select a particular species for pre
y.
However, in its natural habitat its survival does not normall
y
depend on availabilit
y
of that
species, and in its absence other species are acceptable as prey. Special mention is made of
thi
spo
i
nt, as
i

t
h
as somet
i
mes
b
een over
l
oo
k
e
di
n attempts at
bi
o
l
og
i
ca
l
contro
l
o
f
pests.
Some attempts
h
ave
f
a

il
e
db
ecause t
h
e
i
ntro
d
uce
d
pre
d
ator re
d
uce
d
t
h
e pest to
l
ow
d
ens
i
ty
and then died out because alternate pre
y
was not available in the new habitat. As a result,
t

he pest was able to rebound to an economicall
y
important level. In other words, secondar
y
pre
y
species form an important reservoir for the predator at times when the densit
y
of the
pr
i
mary prey
i
s
l
ow
.
4
.2.3. Insect-Insect Mutualisms
Mutua
li
st
i
cre
l
at
i
ons
hi
ps

b
etween
i
nsects are re
l
at
i
ve
l
y uncommon, an
i
mportant ex-
cept
i
on
b
e
i
ng t
h
at
i
nw
hi
c
h
some spec
i
es o
f

ants ten
d
, protect, an
d
somet
i
mes transport
t
onew
l
ocat
i
ons ot
h
er
i
nsects, nota
bly
var
i
ous
h
omopterans (ap
hid
s, ps
yllid
s, an
d
mem
-

b
racids) and the larvae of man
y
l
y
caenid butterflies, in return for which the ants feed on
fl
uids produced by their associate. In homopterans the fluid is the honeydew defecated
in large amounts through the anus (Figure 23.6); in myrmecophilous lycaenids, however,
spec
i
a
l
“Newcomer’s g
l
an
d
s” on t
h
e
d
orsum o
f
t
h
e sevent
h
a
bd
om

i
na
l
segment pro
d
uce an
enriched sugar solution (H¨
olldobler and Wilson, 1990).
¨
5
.In
sec
tD
iseases
I
n insects, as well as in almost all other or
g
anisms, the
g
reat ma
j
orit
y
of individuals (80
%
t
o 99.99% of those born) never survive to reproduce. Fift
y
percent or more of this mortalit
y

may
b
ere
l
ate
d
to pre
d
at
i
on, w
hil
et
h
e rema
i
n
d
er resu
l
ts
f
rom unsu
i
ta
bl
e weat
h
er con
di

t
i
ons,
per
h
aps starvat
i
on, an
d
espec
i
a
ll
y
di
sease. D
i
seases may
b
esu
bdi
v
id
e
di
nto non-
i
n
f
ect

i
ou
s
and infectious cate
g
ories. The former includes those that result from ph
y
sical or chemica
l
in
j
ur
y
, nutritional diseases (caused b
y
deficiencies of specific nutrients),
g
enetic diseases
7
12
CHAPTER
23
(
inherited abnormalities), and ph
y
siolo
g
ical, metabolic, or developmental disturbances
.
Infectious diseases, which can be spread rapidl

y
within a population of or
g
anisms, are cause
d
b
y
microor
g
anisms, includin
g
viruses, rickettsias, spirochetes, bacteria, fun
g
i, protozoa
,
an
d
nemato
d
es. T
h
oug
hi
n
f
ect
i
ons o
f
many o

f
t
h
ese pat
h
ogens may
b
e
di
rect
l
y
f
ata
l
,ot
h
e
r
pat
h
ogens s
i
mp
l
y wea
k
en an
i
nsect, ren

d
er
i
ng
i
t more suscept
ibl
etopre
d
at
i
on, paras
i
t
i
sm,
o
rot
h
er pat
h
o
g
ens, to c
h
em
i
ca
l
an

d
ot
h
er means o
f
contro
l
,ora
l
ter
i
n
gi
ts
g
rowt
h
rate an
d
reproductive capacit
y
. Most of the time in natural populations, the effects of patho
g
ens
are not readil
y
obvious. This is described as the enzootic sta
g
e. On occasion, however,
c

on
di
t
i
ons are suc
h
t
h
at t
h
e pat
h
ogens can repro
d
uce an
d
sprea
d
rap
idl
yto
d
ec
i
mate t
h
e
h
ost popu
l

at
i
on. T
hi
s
i
s
k
nown as t
h
eep
i
zoot
i
cp
h
ase, an
d
t
h
e out
b
rea
ki
s
d
escr
ib
e
d

a
s
an ep
i
zoot
i
c, compara
bl
etoanep
id
em
i
cw
i
t
hi
n a popu
l
at
i
on o
fh
umans. Stu
d
yo
f
t
h
e
f

actors that lead to epizootics, epizootiolo
gy
, is of interest not onl
y
from a purel
y
ecolo
g
ical
perspective but also in li
g
ht of the potential use of microor
g
anisms in the biolo
g
ical contro
l
o
f insect
p
ests.
Thi
s sect
i
on w
ill
out
li
ne t
h

e
i
mportant
f
actors
i
n out
b
rea
k
so
fi
n
f
ect
i
ous
di
seases an
d
survey t
h
ema
j
or groups o
fi
nsect pat
h
ogens.
5.1. E

p
izootics
E
ssent
i
a
ll
y, t
h
ere are
f
our pr
i
mary components
i
nt
h
e
d
eve
l
opment o
f
an ep
i
zoot
i
c: t
h
e

pat
h
ogen popu
l
at
i
on, t
h
e
h
ost popu
l
at
i
on, an e
ffi
c
i
ent means o
f
pat
h
ogen transm
i
ss
i
on, an
d
t
h

eenv
i
ronment, a
ll
o
f
w
hi
c
h
are c
l
ose
ly i
nterre
l
ate
d.
K
e
y
features of a patho
g
en are its virulence (disease-producin
g
power), infectivit
y
(
capacit
y

to spread amon
g
hosts), and abilit
y
to survive. Clearl
y
, patho
g
ens (or specific
stra
i
ns o
f
a pat
h
ogen) t
h
at
h
ave
b
ot
hhi
g
h
v
i
ru
l
ence an

dhi
g
hi
n
f
ect
i
v
i
ty are t
h
e ones t
h
a
t
m
ost o
f
ten cause ep
i
zoot
i
cs, t
h
oug
h
t
h
e suscept
ibili

ty o
f
t
h
e
h
ost
i
sa
l
so
i
mportant. Some
pat
h
o
g
ens ma
yb
e
highly
v
i
ru
l
ent
b
ut o
fl
ow

i
n
f
ect
i
v
i
t
y
an
d
, as a resu
l
t,
h
ave a
l
ow po-
tential for causin
g
epizootics. Bacillus thuringiensis, for example, thou
g
h patho
g
enic for
m
an
y
Lepidoptera, seldom causes an epizootic under natural conditions because of its poo
r

powers of dispersal. Indeed, inability to disperse and limited capacity to survive outside a
h
ost are pro
b
a
bl
yt
h
ema
i
n reasons w
h
yep
i
zoot
i
cs occur re
l
at
i
ve
l
y rare
l
y. D
i
spersa
l
ma
y

b
ee
ff
ecte
d
e
i
t
h
er
b
ya
bi
ot
i
cor
bi
ot
i
c agents
i
nt
h
eenv
i
ronment,
i
nc
l
u

di
ng w
i
n
d
,ra
i
n, run
-
n
in
g
water, snow, host or
g
anisms (both health
y
and infected), and their predators (bot
h
v
ertebrate and invertebrate) or parasites. Host or
g
anisms ma
y
disperse the patho
g
en a
s
a result of defecation, regurgitation, oviposition (i.e., the pathogen occurs either on or
wi
t

hi
nt
h
e eggs),
di
s
i
ntegrat
i
on o
f
t
h
e
b
o
d
ya
f
ter
d
eat
h
, or cann
ib
a
li
sm. Pre
d
ators com

-
m
on
l
y
di
str
ib
ute pat
h
ogens v
i
at
h
e
i
r
f
eces, t
h
oug
h
some
i
nsect paras
i
to
id
s trans
f

er t
he
m
icroor
g
anisms via their ovipositor when the
y
either stin
g
the host or la
y
an e
gg
on or i
n
i
t. Patho
g
ens ma
y
survive in either the host or the environment, sometimes for consider
-
able periods. Those that survive in the environment t
y
picall
y
haveahi
g
hl
y

resistant restin
g
stage, suc
h
as spores (
b
acter
i
a,
f
ung
i
,an
d
protozoa),
i
nc
l
us
i
on
b
o
di
es (v
i
ruses), or cysts
(
nemato
d

es).
M
em
b
ers o
f
t
h
e
h
ost popu
l
at
i
on p
i
c
k
up pat
h
o
g
ens as a resu
l
to
f
p
hy
s
i

ca
l
contact w
i
t
h
c
ontaminated surfaces, or eatin
g
contaminated food (includin
g
cannibalism), or receive
patho
g
ens directl
y
from the mother via transovarian transmission. Contact with a patho
g
en,
h
owever,
d
oes not necessar
il
y resu
l
t
i
n
ill

e
ff
ects
f
or t
h
e
h
ost, as t
h
e
l
atter
h
as var
i
ous
m
eans of defending itself (Chapter 17, Section
5
). Further, even when some members of a
popu
l
at
i
on are suscept
ibl
etoapat
h
o

g
en, an ep
i
zoot
i
c
d
oes not a
l
wa
y
s
f
o
ll
ow
b
ecause o
f
7
13
THE BI
O
TI
C
ENVIR
O
NMEN
T
t

he difficult
y
of dispersal of the patho
g
en referred to above and because other members of
t
he population ma
y
have var
y
in
g
de
g
rees of resistance.
Densit
y
, distribution, and mobilit
y
of hosts are important factors in the development
o
f
an ep
i
zoot
i
c. Genera
ll
y, ep
i

zoot
i
cs are more
lik
e
l
y to occur at
hi
g
hd
ens
i
t
i
es, even
di
str
i-
b
ut
i
on, an
dhi
g
h
mo
bili
ty o
fh
osts, as t

h
ec
h
ances o
fdi
spersa
l
o
f
t
h
e pat
h
ogen are greater
u
n
d
er t
h
ese con
di
t
i
ons. On occas
i
on, an ep
i
zoot
i
cma

yd
eve
l
op at
l
ow
h
ost
d
ens
i
t
y
,asare-
sult of widel
y
dispersed but lon
g
-lived patho
g
ens that remain from a previous hi
g
h-densit
y
outbreak. Even at hi
g
h host-population densit
y
, an epizootic ma
y

not develop if the hos
t
popu
l
at
i
on
h
as a
di
scont
i
nuous
di
str
ib
ut
i
on an
d
/or poor mo
bili
ty.
T
h
e
i
mportance o
f
t

h
eenv
i
ronment, p
h
ys
i
ca
l
an
dbi
ot
i
c,
i
nt
h
e
di
spersa
l
an
d
surv
i
va
l
o
f
pat

h
ogens
h
as a
l
rea
d
y
b
een note
d
.Env
i
ronmenta
lf
actors are
i
mportant
i
not
h
er way
s
in relation to epizootics. For example, factors that induce stress in an insect, especiall
y
extremes of temperature, hi
g
h humidit
y
, and inadequate food, ma

y
lower its resistance to
a
pathogen
.
I
n conc
l
us
i
on,
i
t
i
sc
l
ear t
h
at w
h
et
h
er or not an ep
i
zoot
i
c occurs
d
epen
d

sonavar
i
ety
o
f
con
di
t
i
ons re
l
at
i
ng to pat
h
ogen,
h
ost, an
d
env
i
ronment. On
l
yw
h
en
k
now
l
e

d
ge o
f
a
ll
o
f
t
hese factors is available for a
g
iven host-patho
g
en interaction can an accurate forecast of a
potential disease outbreak be made. Such knowled
g
e is of critical importance in determinin
g
t
he success or otherwise of biological control using pathogenic microorganisms
.
5
.2. Types o
f
Pathogens
I
t is natural that the best-known patho
g
ens are those that cause epizootics in econom-
icall
y

important insects and show potential for use in microbial control of pest species. In
thi
ss
h
ort account, t
h
ema
j
or
f
eatures o
f
some o
f
t
h
ese pat
h
ogens w
ill b
e out
li
ne
d
,asa
b
as
i
s
f

or t
h
e
di
scuss
i
on on m
i
cro
bi
a
l
contro
l
presente
di
nC
h
apter 24, Sect
i
on 4.3.1.
5.2.1. Bacteria
Many spec
i
es o
fb
acter
i
a
h

ave
b
een s
h
own exper
i
menta
ll
yto
b
e
hi
g
hl
y pat
h
ogen
i
c
s
h
ou
ld
t
h
ey ga
i
n access to t
h
e

b
o
d
ycav
i
ty. However, un
d
er natura
l
con
di
t
i
ons, t
h
ema
j
or
i
ty
of these never cause epizootics (even thou
g
h their infectivit
y
is hi
g
h) because of the barrier
presented b
y
the inte

g
ument and linin
g
of the
g
ut. Further, the
g
ut ma
y
be unsuitable fo
r
survival and multi
p
lication of the bacteria because of its
p
H or redox
p
otential, or because o
f
th
e presence w
i
t
hi
n
i
to
f
ant
ib

acter
i
a
l
su
b
stances or antagon
i
st
i
cm
i
croorgan
i
sms. In
f
ect
i
o
n
o
f
an
i
n
di
v
id
ua
li

nsect occurs w
h
en t
h
e
i
ntegument or gut
i
sp
h
ys
i
ca
ll
y
d
amage
d
.T
he
commonest route of invasion appears to be via the mid
g
ut. Bacteria are sometimes able to
slip between the peritrophic matrix and the mid
g
ut epithelium at either the anterior or the
posterior end of the midgut, or through ruptures in the matrix caused by the passage of food
a
l
ong t

h
e gut.
T
h
esu
b
sequent mo
d
eo
f
act
i
on o
f
t
h
e
b
acter
i
a, t
h
at
i
s,
h
ow t
h
ey cause a pat
h

o
l
og
i
ca
l
condition, is varied. Invasion and destruction of the mid
g
ut epithelium is t
y
picall
y
the first
step, and for some bacteria this ma
y
be their onl
y
activit
y
, their host then d
y
in
g
of starvation.
M
ore often, bacteria not onl
y
destro
y
the mid

g
ut epithelium but then
g
row rapidl
y
in the
h
emo
l
ymp
h
an
d
ot
h
er t
i
ssues, caus
i
ng mass
i
ve sept
i
cem
i
a. Ot
h
ers act
b
y toxem

i
a; t
h
at
i
s,
th
ey
lib
erate tox
i
ns t
h
at
kill
t
h
e
h
ost’s ce
ll
s. Ot
h
er
b
acter
i
a
b
ecome pat

h
ogen
i
con
l
yw
h
e
n
th
e
y
are a
bl
e to enter t
h
e
h
emocoe
l
v
i
a
l
es
i
ons
i
nt
h

em
idg
ut ep
i
t
h
e
li
um cause
dby
ot
h
er
microor
g
anisms such as protozoa, viruses, and nematodes
.
7
14
CHAPTER
23
B
acteria known to be naturall
y
patho
g
enic in insects can be arran
g
ed in two
g

roups, th
e
n
on-s
p
ore-formers and the s
p
ore-formers.
∗
Included amon
g
the non-spore-formin
g
bacteri
a
is
S
erratia marcescens, varieties of which attack aran
g
e of insect species and whose presence
i
s recogn
i
ze
db
yt
h
ere
ddi
s

h
co
l
or o
f
t
h
e
d
ea
dh
ost. Out
b
rea
k
so
f
S
.
marce
s
cen
s
a
r
eco
mm
o
n
i

n high-density laboratory cultures of insects. According to Bailey (19
6
8), at least five
s
pec
i
es o
fb
acter
i
a are
i
nvo
l
ve
di
n European
f
ou
lb
roo
ddi
sease o
fl
arva
lh
one
yb
ees, t
h

ou
gh
a
non-s
p
ore-former,
S
tre
p
tococcus
p
luto
n
,
i
s
the causative a
g
ent. The remainin
g
species ar
e
s
econdar
y
patho
g
ens or saproph
y
tes

.
Th
e spore-
f
ormers are t
h
e most
i
mportant group
f
rom t
h
epo
i
nt o
f
v
i
ew o
f
ep
i
zoot
i
cs
a
n
df
or t
h

e
i
r potent
i
a
li
mportance
i
n
bi
o
l
og
i
ca
l
contro
l
,
l
arge
l
y
b
ecause t
h
ey rema
i
nv
i

a
bl
e
f
or a cons
id
era
bl
et
i
me outs
id
et
h
e
i
r
h
ost. Furt
h
er, some spec
i
es (t
h
e so-ca
ll
e
d
cr
y

sta
llif
erous
bacteria) are hi
g
hl
y
patho
g
enic in some insects should their sporan
g
ia be in
g
ested because
the sporan
g
ia include, in addition to a spore, a cr
y
stalline structure, the parasporal bod
y
that contains various toxic
p
roteins (the
δ
-
endotoxins)
.
T
w
oo

f
t
h
e
b
etter
k
nown, spore-
f
orm
i
ng, non-crysta
llif
erous
b
acter
i
aar
e
B
aci
ll
u
s
cereu
s
,
w
hi
c

hh
as
b
een
i
so
l
ate
df
rom a range o
fh
ost spec
i
es, an
d
B
.
l
ar
v
ae
,
w
hi
c
hi
s
the cause of American foulbrood in bee larvae. Onl
yy
oun

g
larvae (up to
55
hours old) are
s
usceptible, su
gg
estin
g
that onl
y
in earl
y
larval life are
g
ut conditions suitable for spor
e
g
ermination. Despite the availability of antibiotics for treatment of American foulbrood, it
c
ont
i
nues to
b
e a common
di
sease. T
h
oug
h

t
hi
s
i
s part
i
a
ll
yre
l
ate
d
to t
h
e
l
ong-
li
ve
d
natur
e
of
B
.
l
ar
v
ae spores (espec
i

a
ll
y
i
n
h
oney),
i
ts appearance
i
s
f
requent
l
yt
h
e resu
l
to
f
poo
r
mana
g
ement on the part of beekeepers who expose contaminated
y
et unoccupied supers
.
†
Bees from ad

j
acent hives visit the supers to steal hone
y
and in doin
g
so spread the disease.
O
f the crystalliferous species,
B
. thuringiensis
,
B. popillia
e
,
an
d
B. lentimorbu
s
h
a
v
e
been the subject of considerable research, pure and applied, during the past
5
0 years. Les
s
w
e
ll k
nown

b
ut w
i
t
h
some econom
i
c potent
i
a
li
s B. s
ph
aericus
.
B. thuringiensis
i
ncludes a lar
g
e number of hi
g
hl
y
patho
g
enic subspecies [Bee
g
le and
Yamamoto (1992), list 36] which attack Le
p

ido
p
tera and re
p
resentatives of other orders (no
-
tably Diptera and Coleoptera), including a wide array of economically important species
(
G
l
are an
d
O’Ca
ll
ag
h
an, 2000). Fortunate
l
y,
h
oney
b
ees an
d
many
h
ymenopterous para
-
s
i

to
id
s are not
di
rect
l
y suscept
ibl
et
h
oug
h
,t
h
roug
h
t
h
e
i
re
ff
ect on t
h
e
h
ost, t
h
e paras
i

to
id
s
m
a
y
die within the dead host or have reduced reproductive potential (Vinson, 1990). The
ke
yf
actor that determines host susceptibility is the pH of the midgut. The parasporal body
f
f
o
f most subs
p
ecies of
B
. thuringiensis (but not B. t. israelensi
s
which attacks Di
p
tera) i
s
so
l
u
bili
ze
db
ya

lk
a
li
ne gut
j
u
i
ces an
db
ro
k
en
d
own
b
y gut proteases
i
nto sma
ll
er, tox
i
c
f
rag
-
m
ents. T
he
δ
-

en
d
otox
i
ns
bi
n
d
w
i
t
h
spec
ifi
cg
l
ycoprote
i
n receptors
i
nt
h
ep
l
asma
l
emma o
f
t
h

e
g
ut ep
i
t
h
e
li
a
l
ce
ll
s, caus
i
n
gdi
srupt
i
on o
fi
on an
d
am
i
no ac
id
transport an
d
c
y

to
ly
s
i
s(G
ill
et al.
, 1992). Two other classes of toxins are produced b
y
B. thuringiensi
s
, thurin
g
iensin (
β
-
e
xotoxin), which is a nucleotide and inhibits RNA s
y
nthesis, and a
g
roup of miscellaneous
tox
i
ns t
h
at
i
nc
l

u
d
e
ph
os
ph
o
lip
aseCan
d
t
h
e“
l
ouse
f
actor,” so-ca
ll
e
db
ecause
i
t (rat
h
er t
h
an
t
he
δ

-
en
d
otox
i
ns or t
h
ur
i
ng
i
ens
i
n)
i
s respons
ibl
e
f
or t
h
e tox
i
c
i
ty o
f
B
.t
h

urin
g
iensis
a
ga
i
ns
t
t
h
es
h
eep
b
o
dy l
ouse (Bovico
l
aovi
s
)
(Gou
gh
et al.
, 2002
)
.
E
xtensive field testin
g

showed tha
t
B
. thuringiensi
s
has desirable attributes for suc
-
c
essful control of selected insect
p
ests, and commercial
p
re
p
arations are now available fo
r
∗
T
his is not a taxonomic arrangement but one of convenience used by insect pathologists.
†
S
upers are t
h
e
b
oxes, w
i
t
h
out top or

b
ottom, t
h
at conta
i
nt
h
e
f
rames o
fh
oneycom
b
.P
l
ace
d
one on top o
f
t
he
ot
h
er, t
h
e
y
const
i
tute t

h
e
hi
ve.
7
15
THE BI
O
TI
C
ENVIR
O
NMEN
T
a wide ran
g
e of applications, makin
g
it easil
y
the most successful microbial pest control
a
g
ent. This aspect is taken up a
g
ain in Chapter 24 (Section 4.3.1)
.
B. popillia
e
a

n
d
B
. lentimorbus
c
ause “milk
y
disease” in larvae of some scarabaeid
b
eet
l
es,
i
nc
l
u
di
ng t
h
e Japanese
b
eet
l
e, Popi
ll
ia
j
aponica
,
an

i
m
p
ortant
p
est
i
nt
h
e easter
n
Un
i
te
d
States, t
h
at
f
ee
d
s on roots o
f
grasses, vegeta
bl
es, an
d
nursery stoc
k
. Mass-pro

d
uce
d
spore preparat
i
ons o
f
B.
p
o
p
i
ll
iae are mar
k
ete
df
or contro
l
o
f
t
hi
s pest
.
The first patho
g
enicall
y
active strain of B. s

p
haericu
s
was
isolated in 1965 fro
m
mos
q
uito larvae (Charles
et al.
, 1996). Thou
g
h man
y
strains of this bacterium are known,
not a
ll
are pat
h
ogen
i
c. Stra
i
ns
i
so
l
ate
df
rom

l
arvae o
f
C
u
l
e
x
a
n
d
A
nop
h
e
l
es
s
pp. are gen
-
era
ll
y
hi
g
hl
y act
i
ve, w
h

ereas t
h
ose
f
ro
m
A
e
d
e
s
a
re on
l
y wea
kl
y pat
h
ogen
i
c or non-tox
i
c
.
Th
ere
h
as
b
een some

i
nterest
i
n
d
eve
l
op
i
ng
B
.s
ph
aericus asam
i
cro
bi
a
l
pest
i
c
id
e, an
d
t
hree commercial formulations are available, thou
g
h its narrow host ran
g

eisasi
g
nificant
d
rawback
(
Khetan, 2001
).
5.2.2. R
ic
k
e
tt
sias
Onl
y
a few species of rickettsias are patho
g
enic in insects, thou
g
h some infect pests and
ma
y
have potential as biolo
g
ical control a
g
ents, for example, Rickettsiella popillia
e
, which

attac
k
s Japanese
b
eet
l
es. However, a
l
most no wor
kh
as
b
een
d
one to test t
hi
s poss
ibili
ty
per
h
aps, as St. Ju
li
an et a
l
. (
i
nBu
ll
a, 1973) suggeste

d
,
b
ecause some r
i
c
k
etts
i
as o
fi
nsect
s
are a
l
so pat
h
ogen
i
c
i
n mamma
l
s
.
5.2.3.
V
iruse
s
According to David (197

5
), more than 700 species of insects are known to be susceptible
t
o viral diseases. Of these, about 80% are Lepidoptera, 10% Diptera, and
5
% Hymenoptera
.
M
an
y
of these species are economicall
y
important, and much research has been and is bein
g
conducted to determine the value of viruses in biolo
g
ical control.
Viruses may be arranged in two categories, according to whether the nucleic aci
d
th
ey conta
i
n
i
s
i
nt
h
e
f

orm o
f
DNAorRNA.V
i
ruses
i
n
b
ot
h
groups use raw mater
i
a
l
s
i
n
h
ost ce
ll
s
f
or rep
li
cat
i
ng t
h
e
i

r nuc
l
e
i
cac
id
s, an
d
,
b
y pro
d
uc
i
ng v
i
ra
l
mRNA, t
h
ey use t
he
h
ost’s ribosomes for s
y
nthesis of viral proteins, thereb
y
causin
g
disruption of the host cell’

s
metabolism. The DNA viruses (baculoviruses) include nucleopol
y
hedroviruses (NPVs)
,
g
ranuloviruses (GVs), and iridescent viruses (IVs), while amon
g
the RNA-containin
g
v
i
ruses t
h
e
b
est
k
nown are t
h
e cypov
i
ruses (CPVs). T
h
ec
h
aracter
i
st
i

cs o
f
t
h
ese var
i
ous
forms are given in Steinhaus (1963, Vol. 1), by David (197
5
), and in standard texts o
n
v
i
ro
l
o
gy
or m
i
cro
bi
o
l
o
gy
.
Like bacteria, viruses mainl
y
infect insects when in
g

ested on contaminated food o
r
d
urin
g
cannibalism, thou
g
h some ma
y
be transmitted on the surface of or within e
gg
s
(Rot
h
man an
d
Myers, 2000). Bacu
l
ov
i
ruses
h
ave ro
d
-s
h
ape
d
v
i

ra
l
part
i
c
l
es enc
l
ose
d
w
i
t
hi
n
a protect
i
ve prote
i
naceous s
h
eat
h
,
f
orm
i
ng an occ
l
us

i
on
b
o
d
y. On reac
hi
ng t
h
em
id
gut, t
he
occ
l
us
i
on
b
o
dy di
sso
l
ves
i
nt
h
ea
lk
a

li
ne
g
ut
j
u
i
ce, re
l
eas
i
n
g
t
h
ev
i
rus part
i
c
l
es. In
i
t
i
a
lly
,
t
hese infect the mid

g
ut epithelial cells, replicate, and then enter the hemocoel where the
infection spreads to the fat bod
y
, hemoc
y
tes, and, to a lesser extent, other tissues. In the fina
l
stages of infection, more occlusion bodies are produced, sometimes in massive numbers
(10
9
p
er corpse) to
b
ere
l
ease
d
as t
h
e corpse
d
ecays or
i
s eaten
.
S
ome v
i
ruses are re

l
at
i
ve
ly
s
h
ort-
li
ve
d
outs
id
et
h
e
i
nsect
h
ost an
d
t
h
e
i
r surv
i
va
lf
ro

m
y
ear to
y
ear requires that at least some members of the host population survive. Others,