19 ecology and management of apple arthropod pests · 19.1 introduction apples present a distinct...

19 Ecology and Management of AppleArthropod Pests

Elizabeth H. Beers,1 D. Max Suckling,2 Ronald J. Prokopy3 and Jesús Avilla4

1Washington State University, Tree Fruit Research and Extension Center, Wenatchee,Washington, USA; 2The Horticulture and Food Research Institute of New Zealand Ltd,Canterbury, New Zealand; 3Department of Entomology, University of Massachusetts,Amherst, Massachusetts, USA; 4Centro UdL-IRTA de R+D de Lleida, Universidad de

Lleida, Lleida, Spain

19.1 Introduction 48919.2 Systems of Pest Management 490

19.2.1 Pesticide-based 49019.2.2 Integrated pest management 499

19.3 Fruit Feeders 50119.3.1 Direct pests of buds and fruitlets 50219.3.2 Mature-fruit feeders 503

19.4 Foliage Feeders 50919.4.1 Mesophyll stylet feeders 51019.4.2 Bulk leaf feeders 512

19.5 Structural Feeders 51219.5.1 Superficial woody-tissue and shoot feeders 51219.5.2 Wood-boring insects 51319.5.3 Root-system pests 514

19.6 Conclusion 514

19.1 Introduction

Apples present a distinct challenge to inte-grated pest management (IPM), due in partto their perennial growth habit and physicalcomplexity. The various organs of the tree’sstructure provide multiple habitats suitablefor arthropod colonization. In one study(Oatman et al., 1964), 763 species of arthro-pods were discovered using apple as a hostplant. While many of these were transitory,perhaps 100 or so species have been consid-

ered pests at some point in time. This sur-vey referred to one orchard in a temperateproduction zone in central North America,and we can only presume the total for theworld is far greater. Despite this, only adozen or so arthropods in any given regionare considered serious or chronic pests. Afew, such as the codling moth, the Europeanred mite and, to a lesser extent, the two-spotted spider mite are pests virtuallywherever apples are grown; others arestrictly regional pests.

© CAB International 2003. Apples: Botany, Production and Uses (eds D.C. Ferree and I.J. Warrington) 489

Apples - Chap 19 11/4/03 11:01 am Page 489

When the pest complexes are viewed asa whole, a pattern of ecological homo-logues emerges. These homologues may beclosely related species, or unrelated taxathat have similar feeding habits. Thetetranychid mite complex in the Pacificnorth-west (Tetranychus urticae Koch,Panonychus ulmi (Koch) and Tetranychusmcdanieli McGregor) all feed in the samemanner and cause a similar type of foliardamage (Beers et al., 1993). The leaf-rollercomplex (moths in the family Tortricidae)all feed on leaves and the surface of applefruits. Weevils (e.g. the plum curculioConotrachelus nenuphar (Herbst)) and thrips(the western flower thrips, Frankliniella occi-dentalis (Pergande)) are examples of twounrelated taxa that cause similar types ofdamage (surface feeding and oviposition,leaving a superficial scar) and at about thesame period in fruit development (duringor shortly after bloom).

A number of pest species are strictlymonophagous on apple (e.g. Aphis pomi DeGeer), while others are oligophagous oreven highly polyphagous (e.g. T. urticae).The degree of host specialization does notappear to be related to pest status. One ofthe key pests worldwide (codling moth,Cydia pomonella (L.)) is moderatelyoligophagous, feeding primarily on a fewspecies of Rosaceae and one member (wal-nut) of the Juglandaceae. However, manyspecies exhibit a certain degree of plasticityin their feeding behaviour and are capableof shifting hosts or expanding their hostrange over time. An example is the applemaggot, Rhagoletis pomonella Walsh, in west-ern North America. A host shift was recentlydemonstrated for this species (from apple tocherry) (Jones et al., 1989), even though aclosely related species, Rhagoletis indifferensCurran, already occupied this niche in thisregion (Utah). Apple is an introduced cropin the majority of the areas where it isgrown, so the pest complex of any givenregion is typically a mixture of pests fromthe native region that have been introducedover time (many before strict quarantineregulations were imposed) and native peststhat have adapted to using apple as a host(e.g. apple maggot).

The classification of pests in this chapteris necessarily an arbitrary choice. We referto arthropod taxa, but, for pest-manage-ment purposes, the taxon is not necessarilythe most useful unit. Our approach hasbeen more crop-centred, in that groupingshave been made on the basis of damagetype (Fig. 19.1), which is in turn usuallyhighly related to its potential economicimportance. Within some of the largergroups (fruit feeders), we have groupedpests by time of attack or by type of damagecaused. Overarching the crop and produc-tivity issues, we have superimposed theecological niche and ecological homologueconcepts in an attempt to make theplant–herbivore relationship clearer.

19.2 Systems of Pest Management

19.2.1 Pesticide-based

The discovery and commercialization ofsynthetic organic pesticides in the latter halfof the 20th century represented a majorqualitative change in pest management. Forthe first time since the beginning of agricul-ture, producers had a broad range of highlyeffective and relatively inexpensive prod-ucts to use for insect control (Table 19.1).Their ease of use and often long residualtoxicity to pests made them very popularand, to some extent, the applications werean insurance policy against pest damage.The euphoria was short-lived, as resistanceproblems began developing, sometimeswithin a few seasons’ use. The organochlo-rines, introduced to agriculture after theSecond World War, were largely supplantedby the organophosphates, carbamates andpyrethroids within a few decades. Theproblems associated with the use of theseproducts became apparent after a relativelyshort time, including environmental persis-tence and damage (especially theorganochlorines), mammalian toxicity (e.g.applicator and farm-worker safety, espe-cially the organophosphates), possible con-sumer effects from residues on foods(carcinogenicity, teratogenicity, mutagenic-ity or chronic neural effects), and destruc-

490 E.H. Beers et al.


tion of pests’ natural enemies and selectionfor resistant pest populations. There wereclear economic benefits driving the use ofthese materials: 30–50% damage fromcodling moth in the latter part of the leadarsenate era (1940s) was common (Driggers,1937), whereas the economic threshold forthis pest today is generally set at < 1%.Despite this, the disenchantment with thesematerials has been growing steadily sincethe 1950s.

One of the side-effects of the pesticide-based era was that the bulk of entomologicalresearch was directed at the developmentand optimum use of the new pesticides, andbasic biology and biological-control researchslowed considerably. The search for alterna-

tive tactics was minimal, because of the effi-cacy of the new pesticides. Non-pesticidaltactics with some degree of promise weredismissed because of their relatively higherexpense, lower efficacy or greater complexityof implementation. The concept of matingdisruption, well established by the 1970s(Roelofs, 1979), was not registered for use onapples in North America until the early 1990s,and is still not registered in some Europeancountries. Similarly, the sterile-insect tech-nique, although demonstrated as feasible forcodling-moth control in the 1960s (Proverbset al., 1966), was not implemented in treefruit on a large commercial scale until theearly 1990s, and then only on a limitedacreage in British Columbia, Canada.

Apple Arthropod Pests 491

Fig. 19.1. Examples of arthropod pests attacking various parts of the tree. Clockwise from top: scale (feedon bark); aphids (phloem feeders in shoots and leaves); leafhoppers (pierce mesophyll cells and removecontents); woolly apple aphid galls (on roots); bark beetles (attack trunk and major scaffolds); leaf-rollers(feed on fruit surface and leaves); codling moth (feeds internally in fruit); plum curculio (oviposits and scarsyoung fruitlets). (Illustration by G. Steffan.)



Tab

le 1

9.1.

His

toric

al u

se o

f ins

ectic

ides

and

aca

ricid

es in

app

le.

Type

(I =

inse

ctic

ide,

Use

per

iod

Cla

ss/p

estic

idea

A=

aca

ricid

e)(a

ppro

xim

ate)

Com

men

ts

Inor

gani

cLe

ad A

rsen

ate

I18

90s–

1950

sO

nce

the

sole

con

trol

mea

sure

for

codl

ing

mot

h an

d ot

her

pest

s, th

is c

ompo

und

was

use

d fo

r>

50 y

ears

unt

il re

sist

ance

occ

urre

d an

d re

plac

emen

t ins

ectic

ides

beca

me

avai

labl

e. S

oil r

esid

ues

are

still

pre

sent

Sul

phur

I/ALa

te 1

800s

–pre

sent

O

ften

appl

ied

with

lim

e as

a s

afen

er, t

his

mat

eria

l is

still

wid

ely

used

for

both

da

yar

thro

pod

pest

s an

d di

seas

es. U

sed

in la

te w

inte

r or

ear

ly s

prin

g, it

can

be

phyt

otox

icC

ryol

iteI

Use

d br

iefly

dur

ing

perio

ds o

f cod

ling-

mot

h re

sist

ance

; occ

asio

nal u

se in

org

anic

prod

uctio

n

Din

itro

Com

poun

dsS

ever

al c

ompo

unds

in th

is g

roup

hav

e be

en u

sed,

but

DN

OC

was

the

mos

t com

mon

Din

itro-

o-cr

esol

(D

NO

C)

I/A19

30s–

1970

sH

ighl

y ph

ytot

oxic

; thu

s us

e w

as c

onfin

ed to

dor

man

t spr

ays.

Use

d w

ith o

il to

cont

rol a

phid

egg

s an

d ov

erw

inte

ring

scal

e. N

o lo

nger

per

mitt

ed in

Eur

ope

(200

0)D

N-1

11A

1940

s–ea

rly 1

950s

Asu

mm

er a

caric

ide.

Phy

toto

xic

Bot

anic

als

As

a gr

oup,

thes

e w

ere

once

the

prim

ary

pest

icid

es a

llow

ed in

org

anic

pro

duc-

tion;

som

e ar

e be

ing

with

draw

n (s

ee in

divi

dual

che

mic

als)

. Wid

ely

varia

ble

inte

rms

of m

amm

alia

n to

xici

tyN

eem

I19

80s–

pres

ent

Der

ived

from

the

seed

s of

nee

m (

tree

) (A

zadi

rach

ta in

dica

A. J

uss)

; has

antif

eeda

nt, r

epel

lenc

y an

d/or

gro

wth

-reg

ulat

or in

fluen

ce o

n m

any

orde

rs o

fin

sect

sR

yani

a ex

trac

ts (

mai

n I

1950

s–pr

esen

tG

roun

d ba

rk o

f a tr

opic

al s

hrub

(R

yani

asp

p.);

onc

e w

idel

y us

ed fo

r co

dlin

g-m

oth

activ

e in

gred

ient

rya

nodi

ne)

cont

rol,

it st

ill h

as a

lim

ited

plac

e in

org

anic

app

le p

rodu

ctio

nR

oten

one

I/A19

30s–

pres

ent

Ane

urot

oxin

bes

t kno

wn

for

its to

xici

ty to

fish

; no

long

er a

llow

ed in

mos

t org

anic

cert

ifica

tion

prog

ram

mes

. Com

pone

nt o

f roo

ts o

f tro

pica

l pla

nts

(e.g

. Der

rissp

p.).

Con

trol

s a

wid

e ra

nge

of a

rthr

opod

pes

tsP

yret

hins

I/AA

ncie

nt ti

mes

S

ever

al d

eriv

ativ

es o

f flow

ers

in th

e ge

nus

Chr

ysan

them

um. C

ontro

l of a

wid

e ra

nge

to p

rese

ntof

inse

cts

and

mite

s. R

esid

ues

disa

ppea

r ve

ry q

uick

ly. L

ittle

com

mer

cial

orc

hard

use

exce

pt o

rgan

icN

icot

ine

IA

high

ly p

oiso

nous

sub

stan

ce d

eriv

ed fr

om N

icot

iana

spp.

, use

d co

mm

only

in th

eea

rly p

art o

f the

cen

tury

for

aphi

d an

d ot

her

soft-

bodi

ed in

sect

con

trol

. Usu

ally

as

nico

tine

sulp

hate

Apples - Chap 19 11/4/03 11:01 am 92


Chl

orin

ated

hyd

roca

rbon

sG

ener

ally

a v

ery

pers

iste

nt g

roup

of n

euro

toxi

c co

mpo

unds

in s

oil,

wat

er a

nd a

nim

altis

sues

; ver

y fe

w s

till i

n us

e to

day

for t

his

reas

on. M

amm

alia

n to

xici

ty re

lativ

ely

low

DD

T(d

ichl

orod

iphe

nyltr

ichl

oroe

than

e)I

Mid

-194

0s–1

970s

The

mos

t rec

ogni

zabl

e na

me

in th

is c

lass

, sub

ject

of t

he b

ook

Sile

nt S

prin

g.H

ighl

y pe

rsis

tent

, orig

inal

ly w

ith a

ver

y br

oad

spec

trum

of a

ctiv

ity. P

rimar

y ta

rget

was

cod

ling

mot

h, b

ut it

cre

ated

sev

ere

mite

flar

e-up

s. T

oxic

to m

any

bene

ficia

lin

sect

sT

DE

(D

DD

) I

Phy

sica

l and

che

mic

al p

rope

rtie

s si

mila

r to

DD

T; m

ore

effe

ctiv

e th

an D

DT

agai

nst

(dic

hlor

odip

heny

ldic

hlor

oeth

ane)

red-

band

ed le

af-r

olle

rB

enze

ne h

exac

hlor

ide

(BH

C)

IU

sed

prim

arily

pre

-blo

om fo

r ap

hid

cont

rol;

in s

easo

n us

e co

uld

give

frui

t an

off

flavo

urLi

ndan

eI

1940

s–pr

esen

tP

urer

gam

ma

isom

er o

f BH

C, m

ore

wid

ely

used

Met

hoxy

chlo

rI

1940

s–pr

esen

tU

se in

tree

frui

t cur

rent

ly li

mite

d to

leaf

-min

er c

ontr

ol (

as a

pre

mix

with

mal

athi

on)

End

rinI

1960

sLi

mite

d us

e ag

ains

t Lep

idop

tera

End

osul

fan

I/A19

50s–

pres

ent

One

of t

he fe

w r

emai

ning

chl

orin

ated

hyd

roca

rbon

com

poun

ds s

till w

idel

y us

ed(p

rimar

ily in

US

A).

Con

trol

of s

ucki

ng, c

hew

ing,

bor

ing

inse

cts;

som

e ac

aric

idal

activ

ity, e

spec

ially

rus

t mite

sD

icof

olA

1950

s–pr

esen

tR

elat

ed to

DD

T. H

ighl

y to

xic

to p

hyto

seiid

mite

s, le

ss u

sed

curr

ently

DM

C (

dich

loro

met

hylb

enzh

ydro

l)A

1950

sR

elat

ed to

DD

T. L

imite

d av

aila

bilit

y an

d hi

gh c

ost

Eth

yldi

chlo

robe

nzila

teA

1950

sLi

mite

d us

e du

e to

phy

toto

xici

ty

Org

anop

hosp

hate

sB

road

-spe

ctru

m n

euro

toxi

ns in

trod

uced

afte

r S

econ

d W

orld

War

, man

y m

embe

rsac

utel

y to

xic

to m

amm

als.

Man

y w

ere

acar

icid

al w

hen

first

use

d, b

ut r

esis

tanc

ede

velo

ped

afte

r a

few

sea

sons

’use

. Onc

e th

e m

ost p

reva

lent

gro

up u

sed

on tr

eefr

uits

, the

y ar

e gr

adua

lly b

eing

rep

lace

d by

new

com

poun

dsT

EP

P(t

etra

ethy

lpyr

opho

spha

te)

I/AV

ery

high

ly to

xic

to m

amm

als,

but

sho

rt-li

ved

resi

dues

. Use

d ag

ains

t aph

ids,

mite

s, s

cale

s an

d Le

pido

pter

aA

zinp

hosm

ethy

lI

1950

s–pr

esen

tB

road

-spe

ctru

m a

nd w

idel

y us

ed fo

r 30

–40

year

s; fa

irly

high

mam

mal

ian

toxi

city

;us

es c

urre

ntly

bei

ng r

estr

icte

dD

iazi

non

I19

50s–

pres

ent

Bro

ad-s

pect

rum

, mod

erat

e m

amm

alia

n to

xici

ty; a

lso

avai

labl

e to

hom

e-ow

ners

Mal

athi

onI

1950

s–pr

esen

tO

ne o

f the

low

est m

amm

alia

n-to

xici

ty c

ompo

unds

in th

is g

roup

; litt

le u

sed

inco

mm

erci

al p

rodu

ctio

n an

y m

ore.

Sho

rt r

esid

ual,

thus

pre

harv

est u

se is

pop

ular

Chl

orpy

rifos

-eth

ylI

1960

–pre

sent

Wid

ely

used

for

pre-

bloo

m a

phid

con

trol

and

pos

t-bl

oom

Lep

idop

tera

con

trol

Chl

orpy

rifos

-met

hyl

I19

60s–

pres

ent

Con

trol

of v

ario

us fo

liar

pest

s (le

pido

pter

ous,

aph

ids,

sca

les)

Eth

ion

I19

50s–

1980

sS

ome

use

pre-

bloo

m fo

r sc

ale

and

aphi

dsC

arbo

phen

othi

onI/(

A)

1950

sS

omew

hat p

hyto

toxi

c, m

ore

limite

d sp

ectr

um o

f act

ivity

than

azi

npho

smet

hyl a

ndpa

rath

ion

Con

tinue

d



Tab

le 1

9.1.

Con

tinue

d.

Type

(I =

inse

ctic

ide,

Use

per

iod

Cla

ss/p

estic

idea

A=

aca

ricid

e)(a

ppro

xim

ate)

Com

men

ts

Met

hida

thio

nI

1950

s–pr

esen

tM

inor

use

pre

-blo

om a

gain

st S

an J

ose

scal

e (U

SA

)E

thyl

par

athi

onI/(

A)

Late

194

0s–1

990s

Hig

hly

toxi

c, b

road

-spe

ctru

m a

nd o

nce

wid

ely

used

, thi

s m

ater

ial w

as w

ithdr

awn

from

the

mar

ket i

n so

me

coun

trie

s in

the

1990

s. O

rigin

ally

als

o ac

aric

idal

Met

hyl p

arat

hion

I19

40s–

1990

sS

imila

r in

toxi

city

and

spe

ctru

m to

eth

yl p

arat

hion

; ofte

n so

ld a

s an

enc

apsu

late

dfo

rmul

atio

n to

pro

long

the

resi

due;

with

draw

n fr

om th

e m

arke

t in

the

1990

sP

hosm

etI

Ear

ly 1

970s

–pre

sent

Mod

erat

ely

broa

d ac

tivity

, sim

ilar

to a

zinp

hosm

ethy

l, bu

t low

er w

orke

r ha

zard

Dem

eton

I/(A

)M

id-1

950s

–lat

e 19

80s

Asy

stem

ic m

ater

ial u

sed

prim

arily

for

aphi

d co

ntro

l. O

rigin

ally

aca

ricid

alP

hora

teI/(

A)

1950

sS

yste

mic

in b

oth

folia

r an

d so

il ap

plic

atio

ns. O

rigin

ally

aca

ricid

al. P

oten

tially

phyt

otox

icP

hosp

ham

idon

I/(A

)19

50s–

1980

sS

yste

mic

. Wid

ely

used

as

an a

phic

ide,

orig

inal

ly a

caric

idal

. Mar

gina

lly p

hyto

toxi

cM

evin

phos

IM

id-1

950s

–mid

-S

yste

mic

. Ext

rem

e ac

ute

oral

and

der

mal

toxi

city

to m

amm

als,

but

sho

rt r

esid

ual.

1990

sU

sed

prim

arily

as

an a

phic

ide,

som

e Le

pido

pter

a ac

tivity

Dim

etho

ate

I/ALa

te 1

960s

–pre

sent

Sys

tem

ic. U

sed

for

aphi

d an

d Ly

gus

cont

rol

Pho

salo

neI/A

1960

s–pr

esen

tB

road

-spe

ctru

m p

estic

ide.

Con

trol

of L

epid

opte

ra a

nd D

ipte

ra

Car

bam

ates

Neu

roto

xins

with

a s

light

ly d

iffer

ent m

ode

of a

ctiv

ity fr

om th

at o

f the

org

anop

hos-

phat

esC

arba

ryl

I/A19

50s–

pre

sent

Bro

ad-s

pect

rum

inse

ctic

ide,

low

mam

mal

ian

toxi

city

; wid

ely

used

as

a fr

uit t

hinn

eras

wel

l as

an in

sect

icid

e. S

ome

erio

phyi

d ac

tivity

, tox

ic to

phy

tose

iids,

cau

sing

spid

er-m

ite o

utbr

eaks

Met

hom

ylI

1970

s–pr

esen

tM

uch

high

er m

amm

alia

n to

xici

ty, u

sed

prim

arily

for

cont

rol o

f Lep

idop

tera

Oxa

myl

I/AM

id-1

980s

–pre

sent

Am

ore

toxi

c ca

rbam

ate,

som

etim

es u

sed

for

Lepi

dopt

era;

als

o to

xic

to b

oth

phyt

opha

gous

and

pre

dato

ry m

ites

For

met

anat

e hy

droc

hlor

ide

I/A19

70s–

pres

ent

Effe

ctiv

e ag

ains

t mite

s, th

rips,

som

e H

emip

tera

/Hom

opte

ra a

nd L

epid

opte

ra;

toxi

c to

pre

dato

ry m

ites

Piri

mic

arb

I19

70s–

pres

ent

Sel

ectiv

e sy

stem

ic in

sect

icid

e us

ed p

rimar

ily a

s an

aph

icid

e (e

xcep

t US

A).

Low

toxi

city

to n

atur

al e

nem

ies

Org

anot

ins

Aca

ricid

es w

idel

y us

ed in

the

1970

s an

d 19

80s;

res

ista

nce

prob

lem

s cu

rtai

led

use

Azo

cycl

otin

A19

70s–

pres

ent

Long

-act

ing

acar

icid

e w

ith c

onta

ct a

ctio

nC

yhex

atin

(he

xaki

s)A

1970

s–m

id-1

980s

Wid

ely

used

unt

il re

sist

ance

bec

ame

wid

espr

ead;

with

draw

n fr

om th

e U

S m

arke

tin

198

7F

enbu

tatin

oxi

deA

1970

s–pr

esen

tS

imila

r in

act

ivity

to c

yhex

atin

, app

aren

t cro

ss-r

esis

tanc

e to

that

com

poun

d



Pyr

ethr

oids

Agr

oup

base

d on

the

activ

ity o

f nat

ural

pyr

ethi

ns, b

ut m

ore

activ

e an

d w

ith lo

nger

resi

dual

. Gen

eral

ly-b

road

spe

ctru

m in

sect

icid

es/a

caric

idie

s w

ith lo

w m

amm

alia

nto

xici

ty, b

ut fa

mou

s fo

r ac

ute

toxi

city

to p

hyto

seiid

mite

s. U

sefu

l nea

r to

har

vest

due

to th

eir

smal

l saf

e-to

-har

vest

inte

rval

(fe

w d

ays)

Fen

vale

rate

/esf

enva

lera

teI/A

1970

s–pr

esen

tTa

rget

ed L

epid

opte

ra, b

ut o

ther

pes

ts a

lso

cont

rolle

d (H

emip

tera

/Hom

opte

ra).

Esf

enva

lera

te w

as a

mor

e ac

tive

isom

er o

f fen

vale

rate

, rep

laci

ng it

in th

e 19

80s

Per

met

hrin

I19

70s–

pres

ent

Con

trol

of f

ruit-

and

leaf

-eat

ing

Lepi

dopt

era

and

Col

eopt

era

Acr

inat

hrin

A/I

1990

s–pr

esen

tM

ainl

y us

ed a

s an

aca

ricid

e ag

ains

t Eur

opea

n re

d m

ite. G

ood

inse

ctic

idal

act

ivity

agai

nst t

hrip

sB

ifent

hrin

I/A19

80s–

pres

ent

Mai

nly

used

as

an in

sect

icid

e ag

ains

t Lep

idop

tera

Del

tam

ethr

inI

1970

s–pr

esen

tB

road

-spe

ctru

m in

sect

icid

e, a

lso

used

aga

inst

frui

t flie

sF

lucy

thrin

ate

I19

80s–

pres

ent

Mai

nly

agai

nst L

epid

opte

ra a

nd H

omop

tera

Lam

bda-

cyha

loth

rinI

1980

s–pr

esen

tB

road

-spe

ctru

mTa

u-flu

valin

ate

I/A19

80s–

pres

ent

It re

plac

ed fl

uval

inat

e. M

ainl

y us

ed a

gain

st le

pido

pter

ous

and

aphi

d pe

sts

Mic

robi

al in

sect

icid

esM

ater

ials

that

pro

duce

dis

ease

in th

e in

sect

hos

t; ve

ry s

peci

fic, t

hus

mam

mal

ian

toxi

city

is lo

wB

acill

us th

urin

gien

sis

(Bt)

I

1980

s–pr

esen

tB

acte

ria th

at p

rodu

ce a

n ex

otox

in, w

hich

, whe

n in

gest

ed, c

ause

s gu

t par

alys

is.

subs

p. k

urst

aki

Spe

cific

to le

pido

pter

ous

larv

ae. P

rimar

ily fo

r le

af-r

olle

rsC

odlin

g m

oth

gran

ulov

irus

I19

80s–

pres

ent

Vira

l dis

ease

spe

cific

to c

odlin

g m

oth;

use

d pr

imar

ily in

Eur

ope

as a

‘sof

t’(C

pGV

)in

sect

icid

e su

pple

men

t to

codl

ing-

mot

h co

ntro

l. Lo

w p

ersi

sten

ceA

doxo

phye

s or

ana

I19

90s–

pres

ent

Vira

l dis

ease

spe

cific

to s

umm

er fr

uit t

ortr

ix la

rvae

. Mor

e ef

fect

ive

agai

nst fi

rst-

gran

ulov

irus

(AoG

V)

inst

ar la

rvae

Bea

uvar

ia b

assi

ana

I19

80s–

pres

ent

Fun

gal d

isea

se; d

epen

dent

on

wea

ther

con

ditio

ns; l

ittle

com

mer

cial

use

as

yet

Mac

rocy

clic

lact

ones

Are

lativ

ely

new

gro

up o

f com

poun

ds w

hose

act

ive

ingr

edie

nt is

from

toxi

ns p

ro-

duce

d by

soi

l mic

roor

gani

sms;

larg

e co

mpl

ex m

olec

ules

, som

e ar

e se

mi-s

ynth

etic

Aba

mec

tinI/A

1980

s–pr

esen

tD

eriv

ed fr

om S

trep

tom

yces

ave

rmiti

lis; c

ontr

ols

mite

s, le

af-m

iner

s, s

ome

area

sre

port

con

trol

of l

eafh

oppe

rS

pino

sad

I19

90s–

pres

ent

Der

ived

from

Sac

char

opol

yspo

ra s

pino

sa; l

eaf-

rolle

r an

d le

af-m

iner

con

trol

, als

oth

rips

and

poss

ibly

som

e te

phrit

id fr

uit fl

ies

Milb

emec

tinI/A

Der

ived

from

Str

epto

myc

es h

ygro

scop

icus

. Act

ivity

spe

ctru

m s

imila

r to

that

of

abam

ectin

; not

yet

reg

iste

red

in U

SA

/Eur

ope

Pol

ynac

tins

AD

eriv

ed fr

om S

trep

tom

yces

aur

eus.

Con

trol

of s

pide

r m

ites

Con

tinue

d



Tab

le 1

9.1.

Con

tinue

d.

Type

(I =

inse

ctic

ide,

Use

per

iod

Cla

ss/p

estic

idea

A=

aca

ricid

e)(a

ppro

xim

ate)

Com

men

ts

Inse

ct g

row

th r

egul

ator

sA

new

er g

roup

of

inse

ctic

ides

atta

ckin

g va

rious

poi

nts

in t

he i

nsec

t’s h

orm

onal

syst

em,

thus

mak

ing

them

spe

cific

to

inve

rteb

rate

s an

d la

rgel

y no

n-to

xic

to m

am-

mal

s. T

arge

ts a

re m

ostly

Lep

idop

tera

, som

e H

omop

tera

Ben

zoyl

urea

s (d

iflub

enzu

ron,

I/A

1970

s–pr

esen

tT

hese

com

poun

ds a

ct a

s ch

itin-

synt

hesi

s in

hibi

tors

. Use

d m

ainl

y ag

ains

t lea

f-

hexa

flum

uron

, fluf

enox

uron

, an

d fr

uit-

eatin

g le

pido

pter

ous

larv

ae (

codl

ing

mot

h, le

af-r

olle

rs a

nd le

af-m

iner

s);

trifl

umur

on, l

ufen

uron

, so

me

have

som

e ef

fect

aga

inst

rus

t mite

s (lu

fenu

ron)

or

spid

er m

ites

teflu

benz

uron

)(fl

ufen

oxur

on);

res

ista

nce

to d

iflub

enzu

ron

has

been

rep

orte

d in

Eur

ope;

nev

erre

gist

ered

in th

e U

SA

Fen

oxyc

arb

I19

80s–

pres

ent

Alth

ough

che

mic

ally

a c

arba

mat

e, it

act

s as

a ju

veni

le h

orm

one

anal

ogue

, with

ast

rong

juve

nile

hor

mon

e-lik

e ac

tivity

, inh

ibiti

ng m

etam

orph

osis

to th

e ad

ult s

tage

and

inte

rfer

ing

with

the

mou

lting

of e

arly

-inst

ar la

rvae

; wid

ely

used

in E

urop

e fr

omth

e 19

80s

agai

nst c

odlin

g m

oth

and

leaf

-rol

lers

; nev

er r

egis

tere

d in

the

US

ATe

bufe

nozi

deI

1990

s–pr

esen

tE

cdys

one

agon

ist,b

whi

ch a

cts

by b

indi

ng to

the

ecdy

sone

rec

epto

r pr

otei

n. A

s a

cons

eque

nce,

the

mou

lting

pro

cess

is le

thal

ly a

ccel

erat

ed. U

sed

in E

urop

e fo

r th

eco

ntro

l of c

odlin

g m

oth

and

leaf

-rol

lers

Met

hoxy

feno

zide

I19

90s–

pres

ent

Ecd

yson

e ag

onis

t; m

ore

activ

e th

an te

bufe

nozi

de; c

odlin

g m

oth,

leaf

-rol

lers

, lea

f-m

iner

sP

yrip

roxy

fen

I20

00–p

rese

ntJu

veni

le h

orm

one

anal

ogue

, goo

d sc

ale

and

othe

r H

omop

tera

act

ivity

, som

esu

ppre

ssio

n of

Lep

idop

tera

Nic

otin

oids

Neu

roto

xins

that

act

at t

he n

icot

inyl

site

; a n

ewer

gro

up o

f ins

ectic

ides

, fai

rlybr

oad

activ

ity s

pect

rum

Imid

aclo

prid

I19

80s–

pres

ent

The

ear

liest

reg

istr

atio

n of

the

grou

p; w

idel

y us

ed fo

r ap

hid

cont

rol;

also

effe

ctiv

eag

ains

t oth

er H

omop

tera

, inc

ludi

ng le

afho

pper

s an

d m

ealy

bugs

. Als

o to

xic

toap

ple

mag

got

Thi

amet

hoxa

mI

2001

–pre

sent

Rec

ently

reg

iste

red;

act

ivity

spe

ctru

m in

clud

es L

epid

opte

ra a

ndH

emip

tera

/Hom

opte

ra

Chl

orin

ated

sul

phur

aca

ricid

esA

ram

ite

A19

50s

Ach

lorin

ated

sul

phite

Chl

orfe

nson

(O

vex)

A19

50s

Ach

lorin

ated

sul

phon

ate,

som

ewha

t phy

toto

toxi

cG

enite

923

, Mito

x, F

enso

nA

1950

s–19

60s

Clo

sely

rel

ated

chl

orin

ated

sul

phur

com

poun

dsS

ulph

enon

eA

1950

sA

chlo

rinat

ed s

ulph

one.

Phy

toto

xic

Tetr

adifo

nA

1960

s–pr

esen

tLo

ng r

esid

ual e

ffect

, tra

nsla

min

ar a

ctiv

ity. A

lso

ovic

idal



Mis

cella

neou

s sy

nthe

tic o

rgan

ic p

estic

ides

Oxy

thio

quin

oxI/A

1960

s–pr

esen

tA

hete

rocy

clic

car

bona

te, u

sed

prim

arily

as

an a

caric

ide,

but

with

som

e ac

tivity

agai

nst p

sylla

and

mild

ewIn

doxa

carb

I20

01–p

rese

ntA

carb

amat

e-lik

e co

mpo

und,

prim

arily

use

d ag

ains

t Lep

idop

tera

Pyr

idab

enA

/I19

90s–

pres

ent

Use

d m

ainl

y in

app

le o

rcha

rds

as a

n ac

aric

ide

agai

nst E

urop

ean

red

mite

. It i

s an

inhi

bito

r of

the

elec

tron

tran

spor

t at m

itoch

ondr

ial l

evel

(M

ET

Ic ). H

igh

knoc

k-do

wn

effe

ct a

nd lo

ng r

esid

ual a

ctiv

ity to

all

mob

ile s

tage

s. T

oxic

to p

hyto

seiid

s. R

isk

ofde

velo

ping

res

ista

nce

Tebu

fenp

yrad

A19

90s–

pres

ent

Ano

ther

ME

TI a

caric

ide,

but

with

som

e ac

tivity

aga

inst

sum

mer

egg

s an

d al

so a

tran

slam

inar

act

ion.

Tox

ic to

phy

tose

iids.

Ris

k of

dev

elop

ing

resi

stan

ceF

enaz

aqui

nA

1990

s–pr

esen

tA

noth

er M

ET

I aca

ricid

e w

ith s

ome

activ

ity a

gain

st s

umm

er e

ggs.

Tox

ic to

phyt

osei

ids.

Ris

k of

dev

elop

ing

resi

stan

ceF

enpy

roxi

mat

eA

1990

s–pr

esen

tA

caric

ide

activ

e ag

ains

t Tet

rany

chid

ae a

nd s

ome

effe

ct a

gain

st E

rioph

yida

e. It

acts

as

a gr

owth

reg

ulat

or. M

oder

atel

y to

xic

to p

hyto

seiid

sC

hlor

dim

efor

mA

1970

sA

chlo

rinat

ed p

hena

mid

ine

Pro

parg

iteA

1970

s–pr

esen

tA

rela

tivel

y se

lect

ive

acar

icid

e, w

ithdr

awn

from

the

US

mar

ket i

n th

e 19

90s

due

tow

orke

r de

rmat

itis

prob

lem

s. S

till i

n us

e in

Eur

ope

Hex

ythi

azox

A19

90s–

pres

ent

It ha

s ov

icid

al, l

arvi

cida

l and

nym

phic

idal

act

ivity

, and

als

o st

erili

zes

fem

ales

;hi

ghly

sel

ectiv

e, b

ut p

oten

tial f

or r

esis

tanc

e fo

und

soon

afte

r in

trod

uctio

n. It

inhi

bits

the

synt

hesi

s of

chi

tinC

lofe

ntez

ine

A19

80s–

pres

ent

Prim

arily

ovi

cida

l (it

inhi

bits

the

deve

lopm

ent o

f the

em

bryo

) an

d so

me

actio

nag

ains

t new

ly h

atch

ed la

rvae

, lon

g pe

rsis

tent

and

hig

hly

sele

ctiv

e, b

ut p

oten

tial

for

resi

stan

ce fo

und

soon

afte

r in

trod

uctio

nA

mitr

azA

/I19

70s–

pres

ent

Mai

nly

used

as

an a

caric

ide,

to c

ontr

ol a

ll st

ages

of t

etra

nych

id a

nd e

rioph

yid

mite

s

Oth

erM

ater

ials

of t

his

type

, som

e of

whi

ch h

ave

been

use

d fo

r ove

r a c

entu

ry, a

re e

njoy

ing

a re

surg

ence

of i

nter

est,

due

to th

eir l

ow e

nviro

nmen

tal a

nd h

uman

hea

lth im

pact

Oil

(pet

role

um)

I/A18

80s–

pres

ent

Hig

hly

refin

ed n

arro

w-c

ut p

etro

leum

pro

duct

s w

ith e

mul

sifie

rs a

dded

; bro

adac

tivity

aga

inst

sof

t-bo

died

inse

cts

and

som

e re

pelle

nt a

ctiv

ity (

espe

cial

lyov

ipos

ition

). O

ften

used

as

an a

djuv

ant

Oil

(pla

nt-d

eriv

ed)

Ear

ly 1

900s

Mai

nly

used

as

stic

kers

for

othe

r pe

stic

ides

Oil

(ani

mal

-der

ived

)E

arly

190

0s–p

rese

ntP

rimar

ily fi

sh-o

il. W

idel

y us

ed a

gain

st c

odlin

g m

oth

in th

e ea

rly p

art o

f the

cent

ury,

use

d in

org

anic

pro

duct

ion

toda

y to

som

e ex

tent

Kao

lin c

lay

I/ALa

te 1

990s

–pre

sent

Als

o kn

own

as p

artic

le fi

lm te

chno

logy

(P

FT

), th

is r

ecen

tly in

trod

uced

com

poun

dha

s a

broa

d sp

ectr

um o

f act

ivity

. Pro

babl

y re

pelle

nt, o

r m

asks

pla

nt h

ost

Dia

tom

aceo

us e

arth

I19

50s–

pres

ent

An

abra

sive

sili

ca-c

onta

inin

g m

ater

ial m

ined

from

dep

osits

of s

kele

tons

of m

arin

em

icro

orga

nism

s; m

any

indu

stria

l use

s; li

ttle

used

in a

pple

pro

duct

ion

Con

tinue

d



Tab

le 1

9.1.

Con

tinue

d.

Type

(I =

inse

ctic

ide,

Use

per

iod

Cla

ss/p

estic

idea

A=

aca

ricid

e)(a

ppro

xim

ate)

Com

men

ts

Soa

pI/A

1950

s–pr

esen

tF

atty

aci

d de

rivat

ives

that

are

bro

adly

toxi

c to

sof

t-bo

died

inse

cts;

not

wid

ely

used

beca

use

of s

hort

res

idua

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19.2.2 Integrated pest management

The problems with the so-called ‘pesticidetreadmill’ were part of the impetus to re-examine and reorganize pest-managementefforts. The use of pesticides engendered apest-by-pest approach, with little regard forthe effect of the sprays on the rest of theagroecosystem (let alone the environment orconsumer). With the realization that these dis-junctive efforts were in some cases workingagainst each other, a framework of thoughtwas developed to try simultaneously toaccount for multiple effects and to solve mul-tiple problems. This theoretical frameworkbecame known as ‘integrated pest manage-ment’, or IPM (Stern et al., 1959). Althoughthere are a number of variants (Steiner et al.,1977), this is still the predominant philosophygoverning apple pest research.

The guiding philosophy behind IPM wasthe optimization and harmonization of tacticsto achieve ‘the best economic, environmental,and social’ outcome (Rabb, 1972). While thisseems straightforward enough, turning thisphilosophy into practice has been an ongoingand occasionally hotly disputed process. Oneoverriding difficulty has been evaluating therelative value of a practice where there areclear economic consequences (usually for theproducer) and more nebulous, but potentiallyfar-reaching, consequences for society atlarge. Where the quality and quantity of foodproduction overall are an overriding issue,the value of less expensive or more abundantfood has often outweighed the more long-term environmental and social issues.However, in affluent countries with amplefood supply and relative economic wealth,the conflict becomes more acute. This is gen-erally reflected in the increasing interest inIPM, integrated fruit production (IFP) andorganic production in Europe, the Americasand parts of Asia.

A number of key concepts of IPM form thefoundation of most apple pest-managementprogrammes (Metcalf and Luckmann, 1975).The first fundamental concept is to developsome quantitative relationship between thepest population and the loss in yield or pro-ductivity. This loss must then be assigned aneconomic value, based on the projected yield

from the orchard and the value of the crop. Thesecond is that of sampling pest populations inorder to arrive at some numerical or risk-basedassessment of the population. With these ele-ments in place, a comparison is made betweenthe cost of some control measure and the pro-jected value of crop loss from insect damage.The point at which the two are equal is calledthe economic injury level (EIL) (Stern et al.,1959). As a general principle, the producerwants to ensure that the insect populationdoes not exceed the EIL (because preventableeconomic loss occurs), nor is there any particu-lar benefit in merely breaking even. Ideally,the producer needs to forecast the futureinsect population from the current one (basedon previous experience or population growthmodels) and, when it is clear that the EIL willbe exceeded at some future date, the controlmeasure is the preferred course of action.

Not surprisingly, all elements of this sys-tem are fraught with uncertainty. Unless theproducer is growing his/her fruit under con-tract, the future value of the fruit is unknown.Indeed, for decisions made early in the sea-son, even the size of the crop is uncertain.Insect population growth is influenced bymany factors, including the action of naturalenemies, the influence of weather conditions,sprays aimed at other pests or diseases andthe tree vigour. All of these modify theinsect’s innate ability to reproduce (the intrin-sic rate of increase (Birch, 1948)), which is theinteraction of the number of progeny perfemale, the time to first reproduction and thesex ratio. Examples of accurate models thatare actually in use in apple production arefew, if any; however, there is usually a goodsense of the potential growth factor of aninsect population from one generation to thenext in the absence of control measures. Inseveral cases (e.g. tetranychid mites andgracillariid leaf-miners), the modifying effectof natural enemies is partially quantified,such that, at a given predator : pest ratio(Croft, 1975; Avilla et al., 1993) or percentageparasitism (Beers et al., 1993), a reasonableestimate of whether the population willrequire treatment can be made.

Another aspect to sampling insect popu-lations is monitoring their phenologicaldevelopment in order to determine the opti-



mum timing for control measures. Insectsare poikilotherms and speed or slow theirdevelopment in response to ambient tem-perature. This principle underlies the con-cept of physiological time, using some typeof time–temperature summation (e.g.degree-days). Computer simulations ofdevelopment (degree-day models) weredeveloped for many pest species (e.g.codling moth (Fig. 19.2)). This degree-daymodel has been applied most often to thedetermination of optimum timing of pesti-cide applications, but is equally applicableto (for example) distributing mating-disrup-tion dispensers in the orchard or releasing abiocontrol agent. Since monitoring somespecies may be difficult (due to extremelylow population levels) or time-consuming,phenological models have been developedto facilitate the process. These models, oftendriven by fairly simple temperature inputs(daily maxima and minima) and some ini-tialization point (often the first capture of anadult in a pheromone or visual/odour trap),provide producers with greatly improvedaccuracy of determining insect-stage devel-opment. They do not, however, tell the pro-ducer anything about the need for controlmeasures, which must be accomplished byother means.

19.2.2.1 IPM tactics

In one sense, almost any pest-control tacticmay potentially have a place in an IPMframework. Some tactics tend to be moreoften associated with IPM or viewed morefavourably. It should be noted at the outsetthat the use of insecticides and acaricides, inthe appropriate circumstances, is considereda legitimate IPM tactic. Increasingly, IPM isdefining the characteristics of appropriatepesticides more and more narrowly. In anycase, pesticide use must always be context-sensitive: the insect must have reached somecritical population level to warrant treat-ment; the optimum timing and placement ofthe material must have been considered; themost appropriate compound must be chosenin light of its effects on natural enemies andother pests in the orchard. In addition, fac-tors such as worker and environmentalsafety are being given more weight in thedecision-making process.

Biological control is considered in manyways to be the ideal pest-management tac-tic, because it tends to be environmentallyinnocuous, self-sustaining and low cost.Each of these characteristics may depend agreat deal on the system in question. Thelow environmental impact of biological


Accumulated degree-days

% Male flight

% Egg hatch

100

90

80

70

60

50

40

30

20

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0

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codl

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mot

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Fig.19.2. Codling-moth degree-day model. Degrees are calculated using a horizontal cut-off sine-wavemethod, with lower and upper temperatures of 10 and 31°C, respectively (Brunner et al., 1982).


control was formerly considered dogma;recent studies (Follett and Duan, 2000),however, point out that ecosystem disrup-tion from imported organisms can be exten-sive and unexpected.

Conservation biological control isarguably the easiest and thus most fre-quently pursued. This approach uses a nat-ural enemy species that already occurs in theregion and makes the environment morefavourable for its growth and development.This can include cultivating plants in thevicinity of the orchard that provide an alter-native insect host or habitat or avoiding pes-ticides that are toxic to one or more lifestages. The latter is often referred to as ‘inte-grated control’ or the integration of biologi-cal and chemical control tactics. Classicalbiological control is the importation of a nat-ural enemy, often from the region where thecrop originates, which has the capacity toprovide complete economic control of thepest in question. The purest form of this typeis in minimally managed systems, wherepesticide use for other pests does not disruptthe imported natural enemy. Examples ofthis type are rare in tree fruits, because theuse of at least some pesticides is ubiquitous.However, there is still an interest in theimportation of natural enemies, which, ifestablished, become candidates for conserva-tion biological control. The last methodsinvolve ongoing releases of artificially rearednatural enemies; these can occur either occa-sionally (augmentative) or in the form of a‘biological pesticide’ (inundative). Becausethe expense of rearing natural enemies canbe considerable, the latter two methods havebeen little implemented.

Cultural control involves manipulatingthe orchard or the immediate environment toreduce pest numbers or mitigate pest dam-age. Irrigation may reduce water stress andallow arthropod-stressed trees to producebetter than they could otherwise. Orchard-floor management (e.g. the mix of plants inthe row middles) may allow more naturalenemies to build up in the cover crop and beavailable to reduce arboreal pest popula-tions. Reducing fertilization so that vegeta-tive growth is minimized may slow thepopulation growth of flush-feeding insects,

such as aphids. Cultivars or strains that havereduced terminal growth, such as the spur-type cultivars, may play the same role. Ingeneral, however, producers prioritize plantgrowth and productivity in their orchard-management practices, which may conflictwith the optimal pest-control practice.

Host-plant resistance, while frequentlyused in field crops, has played a very smallrole in arthropod-pest management oforchard crops. The horticultural characteris-tics, especially precocity, productivity,flavour and storability, are the primary dri-vers of cultivar choice. One notable excep-tion is the use of resistant rootstocks forwoolly apple aphid.

Ultimately, IPM can be viewed as justanother evolutionary step in our overallproblem-solving process in agriculture. Morerecently, theories have emerged (primarily inEurope and New Zealand) that take the nextlogical step of integration to the entire pro-duction system – integrated fruit production,or IFP (Boller et al., 1998; see Chapter 21). Toan extent, this may be viewed as a reincarna-tion of the organic-production philosophy(see Chapter 22), which also encompasses allaspects of the production system but withthe additional caveat of restricting the mate-rials used to only naturally occurring, mini-mally processed products (in terms ofpesticides, plant-growth regulators and fer-tilizers).

19.3 Fruit Feeders

This group of insects attacks the fruitdirectly, leaving either feeding scars or deepentries, potentially serving as an infectionsite for pathogens. The EILs for these pestsare relatively straightforward for fresh-mar-ket fruit, because virtually all defects areremoved during packing. The issue is some-what clouded for processing fruit, wheresome level of damage, especially healed sur-face damage, does not detract from the util-ity or quality of the fruit. Overall,pest-management programmes havefocused most intensely on this group ofpests because of their clear and apparenteffect on usable yield.



The fruit may be attacked at almost anypoint during the growing season, from earlyin the bud stage to harvest. Fruit attackedearly in the season is more likely to abscisenaturally, or it can be selectively thinnedduring hand-thinning. Fruit attacked duringthe mid-season is more likely to stay on thetree and thus has a higher likelihood of beingharvested. Fruit attacked very late may gen-erate sufficient ethylene to abscise prema-turely and has a slightly reduced chance ofentering the packing or processing plant.Clearly, excessive amounts of fruit drop justbefore harvest will have a detrimental effecton yield.

19.3.1 Direct pests of buds and fruitlets

19.3.1.1 Noctuids (Lepidoptera: Noctuidae)

There is a complex of species in this family inwhich the young larvae feed on developingbuds and fruitlets. The feeding damage canprevent development, cause prematureabscission or leave deep scars that distort thefruit. This group, called the green fruit-worms in North America, include Orthosiahibisci (Guenée), Amphipyra pyrimadoides(Guenée) and Lithophane antennata (Walker).Several species, such as Orthosia incerta(Hufnagel), may be found in Europe,depending on the region (Carter, 1984).These pests may be regionally important, butare generally considered minor. Pheromonesmay be used to monitor their flight to helppredict phenology and relative abundance,e.g. Graphania mutans in New Zealand(Burnip et al., 1995).

19.3.1.2 Weevils (Coleoptera: Curculionidae,Attelabidae)

Although several different species of weevilsare known to feed on buds, fruit, foliage andwoody tissue of apple trees, only two areconsidered to be major pests against whichapple growers take specific action. These arethe apple blossom weevil, Anthonomus pomo-rum (L.), a native and widespread pest ofapples (and occasionally pears) in Europe(Toepfer et al., 1999), and the plum curculio,

C. nenuphar (Herbst), which has become akey pest of apple and other pome and stonefruit in its native range of eastern and mid-western North America. In addition, severalspecies of Rynchites are local or sporadicpests in Europe.

Apple-blossom weevil adults feed ondeveloping apple buds in spring. Feeding isfollowed by oviposition and larval feedingon the bases of flower petals, resulting insterility and a brown-capped appearance ofthe flowers. Low to moderate populationsmay act as natural blossom thinners. Largepopulations, more common in recent years,can overthin the crop. Plum-curculio adultslikewise feed on developing apple buds inspring but also feed upon and then ovipositinto young fruitlets, where larvae tunnel andcause most injured fruitlets to drop. Injuredfruit remaining on trees are scarred by thefeeding and ovipositional wounds, whichusually render injured fruit unmarketable.Whereas apple-blossom weevils and north-ern populations of plum curculios have onegeneration per year, more southern popula-tions of plum curculio have an additionalgeneration and threaten not only fruitlets butalso apples approaching maturity.

An understanding of the ecology of theseweevil species is the key to successful man-agement (Vincent et al., 1999). Both speciescan build into large populations on unman-aged host trees. In some locales, plum cur-culio annually infests 90% of the fruit onunmanaged trees. Although resident verte-brate and invertebrate predators, parasitoidsand pathogens do have some impact, thedegree of population suppression by thesebiocontrol agents has generally been insuffi-cient to maintain infestations below levelsthat threaten the quality of buds or fruitlets.Fortunately, adults of both species haverather limited flight capability, usually nomore than a few hundred metres. Even so,many blocks of apple trees in Europe andeastern and midwestern North Americahave at least one border exposed to suffi-cient numbers of nearby unmanaged hoststo constitute high susceptibility to invasion.Another important ecological considerationis overwintering, which occurs in the adultstage, when individuals move in autumn



from infested trees to protected sites beneathfallen leaves, bark or debris at margins ofnearby woods or hedgerows. Finally, whenoverwintered adults migrate into orchardsin spring, there is a strong propensity forestablishment on perimeter trees and succes-sively less propensity for movement on tointerior trees with increasing distance fromthe perimeter.

Application of organophosphate or otherinsecticides timed to coincide with pulses ofadult immigration continues to be the mainapproach to managing both of these pests.Because there still exists no truly effectivetrap for monitoring immigrant adults(Prokopy et al., 1999), timing of application isbased on degree-day models that predictperiods of immigration (Reissig et al., 1998).Improved understanding of the ecology ofthese species has facilitated excellentorchard-wide control using a much-reducedamount of material through restricting appli-cation to only those orchard trees most likelyto become infested, i.e. trees within 20 m orless of the perimeter (Vincent et al., 1997).

19.3.1.3 Mirids (Hemiptera: Miridae)

Like the weevils, the serious mirid pests ofapple are orchard invaders, completing themajority of their life cycle outside theorchard and immigrating only during briefperiods to feed on fruit. This presents anadditional challenge to pest management inthat the grower is forced to respond reac-tively, rather than being able to take proac-tive steps in management. The tarnishedplant bug or Lygus bug (Lygus lineolarisPalisot de Beauvois) (Plate 19.1) is a spo-radic pest of apple. It pierces the develop-ing fruitlet with its piercing–suckingmouth-parts, leaving a deep, inverted dim-ple on the mature fruit. Although themullein plant bug (Campylomma verbasci(Meyer)) feeds in a similar way, it leaves araised corky wart on the fruit. Several otherpests in the same group occur in differentareas of Europe and North America, includ-ing the genera Lygocoris, Lygidea,Heterocordylus (Boivin and Stewart, 1982),Campyloneura, Plesiocoris, Blepharidopterus(Alford, 1984) and Atractotomus (MacPhee,

1976). With the exception of L. lineolaris,most of the apple-feeding mirids are facul-tatively predacious and thus are considerednatural enemies as well as pests.

19.3.1.4 Thrips (Thysanoptera: Thripidae)

Thrips are serious and widespread croppests worldwide, but have few representa-tives in the apple pest complex. The mostcommon species is F. occidentalis (Pergande).The adults are attracted to blooming plantsand are often present in the orchard onblooming weeds. When apple blossomsopen, they move to developing fruits. Theirfeeding activities (sucking mouth-parts)cause a condition called ‘pansy spot’ on sen-sitive cultivars, and they leave a small ovipo-sition scar in the centre of the pansy. Thedamage is most apparent on light-colouredcultivars, often colouring over on deeplycoloured sports (Plate 19.2). The pear thrips,Taeniothrips inconsequens (Uzel) is primarily apest of pear and sugar-maple, but is an occa-sional pest of apple.

19.3.1.5 Sawflies (Hymenoptera:Tenthredinidae)

Hymenopterous pests of apple are few innumber (see also late-season direct fruitfeeders). Hoplocampa testudinea (Klug), theapple sawfly, is a widespread and sometimesserious pest of apple in Europe (Giraud et al.,1996), although elevated natural mortalitiesmay be caused by various fungi and the ich-neumonid Lathrolestes marginatus (Jaworska,1992). The adults appear during bloom andlay eggs in the flower, giving rise to larvaethat burrow and feed in the fruit. The adultsmay be monitored with white sticky panels.

19.3.2 Mature-fruit feeders

19.3.2.1 Codling moth

BIOLOGY Codling moth, C. pomonella (L.), isthe main direct pest of apples worldwideand has been extensively studied (e.g.http://ippc.orst.edu/codlingmoth) (Plate19.3). It is not reported as present in Japan,



Taiwan, Korea or eastern China, but is other-wise cosmopolitan. It is present in the urbanareas of the Brazilian apple-growing area,but it has not yet invaded the orchards.There are typically between one and fourgenerations per year, depending on the cli-mate. The level of infestation on untreatedapple trees can reach 100% of fruit infested,with evidence of multiple ‘stings’ or larvalattacks. The economic threshold for codlingmoth is low (c. 1% damaged fruit), even forcrops that are not exported. These factorshave combined to make this pest one of thegreatest scourges for apple growers. It is alsoone of the most researched and consequentlybest understood insect pests. The absence ofthe insect from Asian growing regions hasled to stringent procedures, including fumi-gation of apples and other potential hostfruit with methyl bromide (e.g. Maindonaldet al., 1992).

Female moths oviposit single eggs on ornear developing fruit. Larvae hatch out andlocate apples on the basis of an apple fruitvolatile, (E,E)-α-farnesene (Sutherland andHutchins, 1972). Larvae then begin to enterthe fruit and make their way to the core tofeed on the seeds, like other members of thegenus Cydia (Witzgall et al., 1996b). Theentrance hole is frequently plugged withfrass. Mature larvae emerge from the fruitwith a characteristic exit hole. Diapausingfifth-instar larvae overwinter in cocoons insuitably protected locations under the bark ofthe host tree or on the ground. Factors con-tributing to population regulation of codlingmoth have been the subject of considerableresearch. There appears to be general accep-tance of the findings of Geier (1963) that lim-ited supply of fruit and overwintering sitesare the key factors limiting codling-mothpopulations on unmanaged trees.

The main recorded hosts are apple,European pear, nashi (Asian pear), Chinesepear and quince. Walnut and plum are con-sistently attacked, while peach, nectarineand apricot are also recorded hosts, anddamage can be significant in some situations.Differences in the host preference, develop-ment, diapause, phenology and populationdynamics have been found for strains orraces of the moth taken from apple, plum or

walnut host plants (Barnes, 1991). Theremoval of alternative or abandoned hosttrees can therefore make an important contri-bution to control by reducing migration ofthe pest into smaller orchards.

DETECTION AND INSPECTION METHODS Pheromonetraps have been used for detecting adult malecodling moths since the initial pheromoneidentification (Roelofs et al., 1971). This is oneof the best understood and most widely usedpheromone monitoring systems. A number ofdifferent management approaches have beenbased on pheromone-trap detection of males,including forecasting female moth flight andoviposition from sustained male flight activity,used with day-degree accumulation (Riedl,1976), spray thresholds based on the numberof moths in standard traps (Wearing andCharles, 1978) and the use of traps to deter-mine the efficacy of mating disruption, some-times with lures with higher pheromone loadsto overcome the pheromone background(Charmillot, 1990).

Cardboard bands applied at the right timearound tree trunks to collect diapausing lar-vae are useful for estimating the number oflarvae per tree (Eyer, 1937) and have beenwidely used in research and by organicgrowers for cultural control. They may beespecially useful for comparing the larvalpopulations from year to year in a givenorchard. Direct observation of damagedapples during the growing season is anotherobvious method of monitoring the pest pop-ulation, although detection of a direct pest atharvest is usually too late for economic pro-duction where there is a single generation.

CHEMICAL CONTROL For much of the 20th cen-tury, chemical control was the most wide-spread method of pest control. However,after usage and selection for populationswith genetic resistance to arsenic (Hough,1928), followed by the same pattern withdichlorodiphenyltrichloroethene (DDT)(Glass and Fiori, 1955), orchardists haveswitched to other broad-spectrum insecti-cides. Development of resistance to otherinsecticides has occurred, although it has notalways occurred in all countries or been doc-umented adequately.



Organophosphates were the next chemi-cal group used in many countries (azinphos-methyl, phosmet, diazinon and phosalone),but resistance is now widely recorded(Barnes and Moffitt, 1963; Bush et al., 1993;Varela et al., 1993; Blomefield, 1994; Knight etal., 1994). Pyrethroids (bifenthrin, cyfluthrin,cypermethrin, deltamethrin, esfenvalerate,fenpropathrin, fenvalerate, flucythrinate, flu-valinate and permethrin) have seen someacceptance in the eastern USA (primarily forleaf-roller control), although the trend inmuch of Europe has been to avoid suchbroad-spectrum insecticides due to their neg-ative impacts on natural enemies.

In Europe, more selective insecticideshave been increasingly used, includingjuvenoids (such as fenoxycarb (Charmillot,1989)), chitin synthesis inhibitors (difluben-zuron, triflumuron, chlorfluazuron andteflubenzuron) and ecdysone agonists (e.g.tebufenozide and methoxyfenozide) (Helleret al., 1992). However, there are also exam-ples of resistance to these compounds(Moffitt et al., 1988; Sauphanor and Bouvier,1995). In addition, avermectin (a macrocycliclactone fermentation product) has some effi-cacy (Cox et al., 1995), as does spinosad,another fermentation product. The advan-tage of more selective insecticides is thereduced impacts on natural enemies, per-mitting the maximum contribution of bio-logical control against other pests.Petroleum oils have been used as ovicides(Webster and Carlson, 1942), although ear-lier products often caused phytotoxicity.More recently, highly refined and purifiedproducts have been shown to have goodefficacy (Riedl et al., 1995) and have reducedphytotoxicity problems. Particle films(Unruh et al., 2000) also have some efficacyagainst codling moth.

Mechanical control, using bands on treetrunks to collect diapausing larvae, has alsobeen used, but these do not collect the pro-portion of the population that falls to theground directly. They can be effective ifused in conjunction with other tactics (e.g.Judd et al., 1997).

BIOLOGICAL CONTROL There are a range ofbiological control agents of codling moth,

attacking by predation (Knight et al., 1997) orparasitism (Hassan, 1989) of eggs andneonate larvae (MacLellan, 1972). The cryp-tic habit of the larval stages (including dia-pause) offers some protection against naturalenemies. In some situations, bird predationof diapausing larvae can be significant(Wearing and McCarthy, 1992). However, thehigh levels of damage typically observed inthe absence of controls indicate that biologi-cal control, if present, is insufficient to main-tain the pest below the economic threshold,which is relatively low.

MATING DISRUPTION The release of sufficientsynthetic sex pheromone to delay or preventmating and provide control of codling mothhas been researched extensively worldwide,based on promising results with a range offormulations (Charmillot, 1978; Moffitt andWestigard, 1984; Gut et al., 1992; Minks andvan Deventer, 1992; Judd et al., 1997). Themechanisms by which disruption acts are notentirely clear (Minks and Cardé, 1988) and itmay be possible to use pheromone-relatedcompounds to improve results (Witzgall etal., 1996a).

Mating disruption is inversely density-dependent and therefore works best at lowpest densities in sites without significantimmigration. It is not as effective in situa-tions where the pheromone cloud is difficultto maintain (steep slopes, windy sites, miss-ing trees or uneven orchard canopy) or inclose proximity to unmanaged populations.The first commercially available pheromonedispenser for control of codling moth(Isomate-C®) became available in the USA in1991. Mating disruption of codling moth isnow commercially accepted in several coun-tries, and c. 40,000 ha of orchards weretreated with pheromone formulations inWashington, California and Oregon in 2000(G. Thayer, Oregon, 2000, personal commu-nication). This has occurred in part becauseof the failure of conventional insecticides,due to resistance, as well as the intrinsicenvironmental and worker safety ofpheromone products.

Although codling-moth mating disrup-tion is not yet registered in all Europeancountries, it has been widely used in some



areas (e.g. northern Italy). The relativelyhigher cost of this technique slows its adop-tion, especially in warmer regions where twoapplications per season of the dispenser arenecessary.

MASS TRAPPING AND ATTRACTICIDAL CONTROL

Mass trapping has not proved to be veryeffective against codling moth (e.g. Proverbset al., 1975), in part because of the cost andpractical difficulties of deploying sufficientstations. As with mating disruption, the tac-tic aims to prevent mating and thereforepest progeny. However, whereas in matingdisruption males can survive to find a matethe next night, this is not possible wheremales have been removed from the system,which represents a potential strength of theapproach. If droplets containing sexpheromone and a fast-acting insecticide areused instead of traps (Charmillot et al.,1996), then the costs can be somewhatreduced. It may also be possible to developmultiple-species attracticides (Suckling andBrockerhoff, 1999).

STERILE-INSECT TECHNIQUE Although it is tech-nically feasible (e.g. Proverbs et al., 1982),sterile-insect release is expensive and hasseveral important limitations. Most impor-tantly, it requires mass rearing with special-ized capital-intensive facilities, excellentquality control to maintain mating competi-tiveness with feral insects, geographical iso-lation, political support and ongoinginvestment in the event of movement of con-taminated fruit. There are apparently fewregional orchard industries that meet thesecriteria. A sterile-insect release programmewas commenced in the 1990s to eradicate thecodling moth from the 8000 ha of apple andpear trees in the Okanagan valley in BritishColumbia. While successful in some respects,the goal of eradication has not been realizedand the programme has been redirected to aminimal-insecticide control programme (H.Thistlewood, personal communication).

MICROBIAL CONTROL The most promisingmicrobial control against codling-mothneonate larvae is a granulosis virus (Tanada,1964), which has been tested extensively in

Europe (Audemard et al., 1992), including theUK (Glen and Payne, 1984), New Zealand(Wearing, 1990) and the USA (Westigard andHoyt, 1990). In hot climates with high levelsof solar radiation, the persistence of the virusin the field is poor (about 1 week), makingfrequent applications necessary. However, itseffectiveness against high pest populations,in combination with mating disruption,offers organic apple growers an effective wayof reducing pest populations to levels atwhich mating disruption can operate effec-tively. Commercial use of the virus has unfor-tunately been limited by the costs ofproduction using live insects. Industrial-scaleproduction offers reduced costs to growers(M. Guillon, personal communication), whichshould assist adoption in future.

19.3.2.2 Oriental fruit moth and otherGrapholita (= Cydia) species

Grapholita molesta (Busck) (Plate 19.4) andother members of the Grapholita genus, suchas G. lobarzewskii (= Cydia lobarzewskii) and G.janthinana (Cydia janthinana (Dup.)) are some-times recorded as pests of apple (Kalman etal., 1994). In several countries, G. molesta (ororiental fruit moth) is reported to be increas-ingly important as a pest of apples (e.g. Reiset al., 1988; Pollini and Bariselli, 1993). Thesespecies typically feed on shoots early in theseason, as well as fruits later in the season.The biology and options for control are simi-lar to those for codling moth, but the peststatus may not always warrant intervention.Within the past few years, oriental fruit mothhas emerged as a major pest in several mid-western and eastern US growing districts,surpassing codling moth in importance.

19.3.2.3 Tephritid fruit flies (Diptera:Tephritidae)

True fruit flies of the family Tephritidae (Alujaand Norrbom, 2000) deposit eggs directly intothe flesh of developing fruit, particularly fruitapproaching readiness for harvest. The tinypuncture made through the skin of fruit dur-ing egg-laying is difficult to detect withoutmagnification and may remain so even whenunderlying flesh has decayed substantially



during larval feeding. Commonly, infestedfruit are detected only after a few days ofexposure to room temperature following pur-chase by an unwary consumer.

Three species of tephritid flies are keypests of apples in geographical areas wheretheir presence coincides with commercialapple production. The apple maggot fly, R.pomonella (Walsh) (Plate 19.5), is native toNorth America and is not known to occurelsewhere. It is especially important as a pestof apples in eastern and midwestern regions.It has a more limited, but growing, distribu-tion in the western fruit-growing regions.The Mediterranean fruit fly, Ceratitis capitata(Wiedemann), is native to Africa and hasspread to most fruit-growing regions of theworld. It has become an important pest ofapples in Middle Eastern countries, includ-ing Israel, Syria and Turkey. The SouthAmerican fruit fly, Anastrepha fraterculus(Wiedemann), is native to South America buthas spread to Central America and Mexico.Recently, it has begun to damage commer-cially produced apples in southern Brazil(Sugayama et al., 1998). For all three species,there is an extremely low tolerance, border-ing on zero, for larval-infested fruit, espe-cially fruit intended for export.

Sometime during the past two centuries,all three species expanded their host range toinclude apples. In the process, they haveescaped most of their natural enemies (partic-ularly parasitoids), which provide some bio-logical control of fruit-fly eggs or larvae innative host fruit. Apparently the chemicaland physical properties of apples are suffi-ciently similar to those of the native hosts ofthese flies to have facilitated fly colonizationof apples but are different enough from thenative hosts to exclude colonization by para-sitoids, most of which respond only to highlyspecialized cues when searching for hosts. Inconsequence, fly populations on feral or oth-erwise unmanaged apples or other newlyacquired host trees can build to large num-bers and severely threaten apple orchardswithin a kilometre (in the case of apple mag-got fly) or more (in the case of Mediterraneanand South American fruit flies). Despitegrower vigilance in preventing fly oviposi-tion and larval development in commercial

orchards, annual invasion by adults frombeyond orchard perimeters represents amajor challenge to managing these pests. Inmany situations, not owning the land beyondorchard perimeters severely compromisesgrowers’ ability to reduce invading fliesthrough eliminating nearby unmanaged hosttrees. This may be especially problematicwhere orchard blocks are comparativelysmall and perimeters are exposed to consid-erable non-orchard vegetation.

Currently, all three pest species are man-aged primarily by applications oforganophosphate insecticides, although insome areas the preharvest interval dictates theuse of pyrethroids. Applications are timed inaccordance with the occurrence and abun-dance of captures of invading adults by moni-toring traps placed on perimeter trees.Predictive phenology models (Jones et al.,1989) have been useful in determining thetiming of emergence. In some cases, confininginsecticide application only to perimeter treesor baiting perimeter trees with odour–visualtraps has provided effective control (Cohenand Yuval, 2000; Prokopy et al., 2000). Eventhough there are no known cases of insecti-cide resistance in any tephritid fly, the needfor continuous protection of apples by insecti-cide residue over the course of the 2–3-monthperiod of susceptibility to fly oviposition isprompting some growers to seek alternativeapproaches to fly management.

19.3.2.4 Leaf-rollers (Lepidoptera: Tortricidae)

BIOLOGY Leaf-rollers have only an indirectphysiological impact on the tree, since theyfeed on the fruit surface rather than theseeds. While the impact on the tree may benegligible, the impact of fruit feeding ongrower returns is a direct one. Leaf-rollersemerge as a major concern in many orchardsthat apply selective controls for codlingmoth, as well as for exporters forced to meetquarantine tolerances with a nil threshold.Larvae typically web foliage together andmany also feed directly on the fruit surface.This cryptic habit has often made insecticidalcontrol difficult. Fruit damage is visible asscarring or corking or as rots associated withopen wounds in storage, and larvae occa-



sionally enter the apple calyx. Injury to fruitsdestined for fresh and especially export mar-kets has the most significant economicimpact, compared with that of processing-grade apples.

Leaf-roller biology differs in severalimportant ways from the internal feedingtortricid species (van der Geest andEvenhuis, 1991). Many have much widerhost ranges and feed on leaves as well asfruit (Chapman and Lienk, 1971). Theirexternal life habit is accompanied by larvaldispersal through ballooning, typically fol-lowed by the establishment of a larval neston shoots or the undersides of leaves. Largerlarvae are able to relocate to fresh nests anduse their silken thread for both nest con-struction and escape. Many species are mul-tivoltine, with up to four generations peryear. Unlike codling moth, few leaf-rollerspecies are geographically widespread.Instead, apple-growing regions typicallyhave a unique complex of leaf-roller species(Table 19.2; Chambon, 1986).

HOST RANGE Many leaf-rollers attacking applehave very wide host ranges. The followingrepresents a partial list of hosts of the lightbrown apple moth, Epiphyas posvittana, to indi-cate the range of economically important alter-native hosts: Actinidia chinensis (kiwifruit),Chrysanthemum � morifolium (chrysanthemum

(florists’)), Crataegus (hawthorns), cotoneaster,Eucalyptus, Humulus lupulus (hop), Jasminum(jasmine), Ligustrum vulgare (privet), Litchi chi-nensis (lychee), Macadamia integrifolia(macadamia nut), Medicago sativa (lucerne =alfalfa), Pinus (pines), Prunus persica (peach),Prunus armeniaca (apricot), Pyrus (pears),Quercus (oaks), Rubus (blackberry, raspberry),Solanum tuberosum (potato), Trifolium (clovers),Vicia faba (broad bean), Vitis vinifera(grapevine), Ribes (currants), Rosa (roses), cit-rus, Diospyros (malabar ebony), Populus(poplars), Vaccinium (blueberries).

DETECTION AND INSPECTION METHODS Phero-mones are known for many tortricids affecting apples (http://www.nysaes.cornell.edu/pheronet), and traps have beenwidely used for detection and monitoring ofleaf-roller populations. A range of applica-tions were reported by Suckling and Karg(2000), including species-distribution sur-veys, insecticide-resistance monitoring,insecticide spray-reduction programmes andsample collection for population studies.More labour-intensive systems involving lar-val assessments on shoot tips have also beenused for predicting the size of subsequentgenerations within a season.

Modern diagnostic methods are also underdevelopment for a range of tortricids. SeveralDNA methods have been used for species


Table 19.2. Abbreviated list of leaf-roller pests affecting apple in various regions.

Species Common name Distribution

Adoxophyes orana (Fischer von Summer-fruit tortrix Europe, AsiaRöslerstamm)

Archips argyrospila (Walker) Fruit-tree leaf-roller North AmericaArchips breviplicanus (Walsingham) Asiatic leaf-roller AsiaArchips podana (Scopoli) Great brown-twist moth Europe, AsiaArchips rosana (L.) European leaf-roller Europe, USAArchips xylosteanus (L.) Apple leaf-roller Eastern EuropeArgyrotaenia velutinana (Walker) Red-banded leaf-roller Eastern USAChoristoneura rosaceana (Harris) Oblique-banded leaf-roller North AmericaEpiphyas postvittana (Walker) Light brown apple moth Australia, New ZealandPandemis heparana (Denis and Schiffermüller) Pandemis leaf-roller EuropePandemis limitata (Robinson) Pandemis leaf-roller North AmericaPandemis pyrusana Kearfott Pandemis leaf-roller Western USAPlatynota flavedana Clemens Variegated leaf-roller Eastern USAPlatynota idaeusalis (Walker) Tufted apple-bud moth Eastern USA


identification (Sin et al., 1995; Gleeson et al.,2000), and this approach should provide readytaxonomic support for ecological studies.

BIOLOGICAL CONTROL Reduction in broad-spectrum insecticide use on apple is typicallyaccompanied by an increase in biological-control activity of leaf-rollers and other pests.An example is the spread of the parasitoidwasp Colpoclypeus florus Walker (Plate 19.6)for control of the oblique-banded leaf-roller,Choristoneura rosaceana (Harris) (Plate 19.7)after the reduction of organophosphate use inWashington. In many cases, leaf-roller para-sitoids and predators are present on alterna-tive host plants outside orchards and followthe pest populations across a range of hostplants (Suckling et al., 1998). A fuller treat-ment of leaf-roller biological control is pre-sent in Mills and Carl (1991).

19.3.2.5 Cutworms and fruit worms(Lepidoptera: Noctuidae)

Although minor in importance in compari-son with the tortricids, several species arecapable of fruit feeding later in the season.The larvae excavate shallow round holes inthe fruit, rendering them unmarketable. Thespotted cutworm (Xestia c-nigrum (L.)),Bertha army worm (Mamestra configurataWalker), variegated cutworm (Periodromasaucia (Hübner)), black cutworm (Agrotisipsilon Hufnagel) and the western yellow-striped army worm (Spodoptera praefica) are afew of the species that can damage applefruits and leaves. More recently, a newspecies, Lacanobia subjuncta (Grote &Robinson), was recorded from WashingtonState (Landolt, 1998) and has become animportant pest in some areas.

19.3.2.6 Fruit-stinging insects (Hemiptera)

Pests in this group are also orchard invadersand damage levels are often highest aroundthe orchard borders. The surrounding habi-tat is a primary determinant of the intensityof attack. The most common example are thestinkbugs (Pentatomidae; Euschistus consper-sus Uhler and Acrosternum hilare (Say)), butthe western box-elder bug (Leptocoris rubro-

lineatus Barber; Hempitera: Rhopalidae) hassimilar pest status. Damage usually occurs inthe latter part of the season and is character-ized by a spongy, depressed area c. 1 cm insize surrounding the feeding puncture.Externally, damage can resemble physiologi-cal disorders such as bitter pit, but the tissuebeneath the skin does not turn brown.

19.3.2.7 Miscellaneous opportunists

A number of insects are attracted to ripeningor overripe fruit and will either create apoint of entry or enlarge damage due toother causes (splits, stem punctures, etc.).Vespid wasps are often found in orchardsnear harvest and, although they are primar-ily predacious, they chew holes in ripe fruitand pose a hazard to harvesters. Nitidulidbeetles are also attracted to ripening fruitand can be found feeding under the surface.Earwigs are orchard residents that are usu-ally predacious, but will also chew orenlarge holes in fruit. They can curl up in thestem cavity and make their way into thepacking-house. The dock sawfly, Ametastegiaglabrata (Fallén), tunnels into the fruit, espe-cially those close to the ground, in order tofind an overwintering shelter.

19.4 Foliage Feeders

There are multiple groups of arthropods thatattack and feed mainly on foliage, with theprimary damage being loss of photosyntheticcapacity due to loss of chlorophyll and dis-rupted osmotic balance. From the perspectiveof plant productivity, specifically yield para-meters, the effect of chlorophyll loss is con-troversial. No clear and uncontestedrelationships have been established, althoughit seems clear from the body of literature thatthere is not a directly proportional relation-ship between loss of chlorophyll and loss ofphotosynthetic capacity.

Trees are capable of sustaining a certaindegree of foliar damage without any mea-surable loss in yield; thus, the critical ques-tion becomes: ‘How much damage?’ Thestudies performed attempting to establishsuch relationships quantitatively have been



restricted in interpretation to the particularcombination of cultivar, climate and growingregime in which they were conducted and,as a consequence, the results and interpreta-tion have been quite variable.

The implication of some level of tolerabledamage has a critical implication for IPM:the latitude for biological control. In manycases, some level of the pest population mustsurvive in order for the natural enemy tosurvive (unless there is an alternative host).Unlike pests of quarantine importance ordirect fruit feeders, there is a greater windowof opportunity for non-pesticidal controlmeasures, since the need for control is not soimmediate or triggered at a low threshold.Given the societal emphasis on reduction inpesticide use, this characteristic should bemore fully exploited in the future.

Many of the foliage feeders are classed assecondary (in importance) or induced pests.The latter classification implies that theywould not have achieved pest status with-out pesticide inputs directed at a primary(often direct) pest. Again, this points to theopportunity to regulate this group usingnon-pesticidal methods, or only on an occa-sional basis.

19.4.1 Mesophyll stylet feeders

This group feeds on cellular contents(including chlorophyll) by penetrating theleaf surface (often from the underside),killing only one or a group of cells at eachfeeding site. The damage appears as speck-ling (leafhoppers) or bronzing (tetranychidand eriophyid mites), depending on the sizeof the mouth-parts and the depth of penetra-tion. Reduction in photosynthesis may fol-low extensive feeding, due possibly to acombination of chlorophyll loss and/orstomatal closure caused by water loss.

19.4.1.1 Tetranychid (spider) mites

Several species are worldwide pests ofapple, including the European red mite (P.ulmi (Koch) (Plate 19.8) and two-spottedspider mite (T. urticae Koch) (Plate 19.9).Other species (T. mcdanieli, Tetranychus vien-

nensis, Eotetranychus carpini, Bryobia spp.)cause a similar type of damage, but areregional in distribution. A few species oftenuipalpids (false spider mites) and tarson-emids (e.g. Cenopalpus pulcher Canestrini &Fanzago) are apple pests in some regions(Jeppson et al., 1975b).

The biological control of spider mites iswell studied and implemented, with vary-ing degrees of success. The predatory mitesin the family Phytoseiidae (Kostianinen andHoy, 1996) are the most frequent and suc-cessful biological-control agents (e.g.Typhlodromus (= Galandromus = Metaseiulus)occidentalis (Plate 19.10), Typhlodromus pyriScheuten, Amblyseius fallacis (Garman),Ambylseius andersoni (Chant), Neoseiulus cali-fornicus (McGregor)) (Jeppson et al., 1975a).Different species are better adapted to differ-ent growing regions; for example, T. occiden-talis is ideally suited to the arid climate ofthe western USA, whereas T. pyri requires amore humid, temperate climate (Beers et al.,1993). T. pyri is the most important mitepredator in the temperate regions ofEurope (excluding Scandinavia and theMediterranean region). It is widely used forEuropean red-mite control, often throughthe release of organophosphate (OP)-resistant strains (Blommers, 1994). Thenumber of years needed to achieve success-ful spider-mite control may vary between 1(temperate conditions) and 3 (cooler con-ditions). T. pyri does not occur in theMediterranean area, where summers are toohot and dry. A. andersoni is the most impor-tant predator in these areas, where its nat-ural populations can very successfullycontrol the pest populations (García-Marí etal., 1989).

Several predatory mite species haveadapted well to orchard spray regimes, andthis is, in large part, the reason why inte-grated control programmes have been possi-ble (Hoyt, 1969). In addition, several speciesare reared commercially and sold for releasein orchards either as an inoculative measureor as a sort of ‘living pesticide’; some strainshave been selected for tolerance to pesticides(Hoy and Knop, 1981; Roush and Hoy, 1981).Other families also contain predatory speciesuseful in apple orchards (e.g. Trombidiidae,



Anystidae, Stigmaeidae and Tydeidae); how-ever, these predators usually play a support-ing role to the phytoseiids. In themid-Atlantic area of the USA, a predatorycoccinellid (Stethorus punctum (LeConte))provides the greatest degree of biologicalcontrol, whereas a related species in thewestern USA (Stethorus picipes Casey) playsonly a minor role. Several groups of preda-tory bugs (especially mirids in the generaCampylomma, Campyloneura, Blepharidopterus,Atractotomus) will prey on mites and mayplay an important role in biological control.The relative dominance or contribution of apredator is governed by many factors,including climate, pest complex, surround-ing habitat and spray regimes prevalent inthe area.

19.4.1.2 Eriophyid mites

There are two basic groups of eriophyids,free-living and those causing plant deformi-ties (galls or blisters). In the former category,the apple-rust mite, Aculus schlechtendali(Nalepa), is widely distributed and com-mon, but rarely considered a serious pest.While high populations can cause leafbronzing and premature terminal bud set(Hull et al., 1986), it is considered a quasi-beneficial species in some areas in that itprovides an alternative prey for predatorymites (Hoyt, 1969). Sensitive cultivars (e.g.‘Golden Delicious’) may be russeted byfeeding in the calyx area, which occursshortly after bloom. Examples of the gall-formers attacking apple are few. Burts (1970)reported on two closely related speciesEriophyes (Phytoptus) pyri (Pagenstecher) andEriophyes mali (Burts), both of which mayattack apple. They cause blisters on theleaves and fruit, leaving the latter scarredand deformed. The current spray pro-gramme has made these mites rare.

19.4.1.3 Leaf-miners

Several families of microlepidoptera (moths)mine apple leaves in the larval stage. Theegg is laid on the surface of the leaf (usuallythe underside) and the newly hatched larvapenetrates the leaf directly from the egg,

with no exposure on the leaf surface. Theentire preimaginal period is spent in themine, which is formed between the upperand lower epidermis by the larva’s feedingactivities. The shape of the mine is usuallycharacteristic of the species or group: thegracillariid leaf-miners (Phyllonorycter (=Lithocoletis) blancardella, Phyllonorycterelmaella, Phyllonorycter crategella), or so-called ‘tentiform’ leaf-miners, produce a dis-tinctive dome-shaped mine with whitefeeding specks visible from the upper leafsurface. Two species of lyonetid moths(Leucoptera malifoliella (= scitella) and Lyonetiaclerkella) produce a blotch and sinuous mine,respectively (Alford, 1984). Several speciesof coleophorid moth (case-bearers) also formmines, but these are usually minor pests.

The cryptic habit of the larvae presentssome challenges for chemical control. Eitherthe adult must be targeted with applicationssufficient to cover the entire flight period orthe pesticide must penetrate the leaf surfacein order to deliver the toxicant to where thelarvae are feeding. True systemic insecti-cides are now rare and, because of residueproblems, few are being developed.Insecticides with translaminar activity aresufficient and typically present few prob-lems in the registration process. While sev-eral effective insecticides are registered foruse against leaf-miners, biological controlhas been reasonably well studied and par-tially implemented. Parasitic wasps (e.g.Pnigalio flavipes, Pnigalio marylandensis,Apanteles ornigis) are regionally abundantand can provide substantial levels of con-trol. However, hymenopterous parasitoids,as a group, tend to be less tolerant of broad-spectrum insecticides, and biological con-trol is easily disrupted.

19.4.1.4 Skeletonizers

There are several species of arthropods fromvarious groups that skeletonize leaves, butnone are specialists on apple and their signif-icance is sporadic and local. Examplesinclude the apple and thorn skeletonizer(Eurtomula pariana; Lepidoptera: Choreutidae)and the pear slug (Caliroa cerasi; Hymenoptera:Tenthridinidae).



19.4.2 Bulk leaf feeders

This is a varied group, comprised mostly ofpolyphagous Lepidoptera. Many are pests ofdeciduous forest trees, which can use appleas a host in the absence of pesticide residues.Examples include the notodontid mothsDatana ministra and Schizura concinna andseveral species in the lasiocampid/lymantriid group (Orygia antiqua; Euproctischrysoheoea, brown-tail moth; Euproctissimilis). The winter moth (Operophthera bru-mata) is occasionally an important pest ofapple in Europe. The autumn webworm(Hyphantria cunea; Arctiidae) is an example ofa gregarious nest maker, which forms a largeweb (up to 50 cm long) and devours all leafmaterial inside it. Other gregarious lepi-dopterans include the tent caterpillars(Malacosoma americana, Malacosoma fragilisand Malacosoma disstria; Lasiocampidae) andthe ermine moths (Yponomeutidae, e.g.Yponomeuta malinellus (apple ermine moth));and others in the genera Swammerdamia andParaswammerdamia are capable of using appleas a host. Currently, these are primarily pestson unsprayed back-garden trees, but theyrepresent a rich pool of potential insectspecies that may respond to our changingpest-control regimes.

19.5 Structural Feeders

The group is defined as those attacking plantparts other than fruits and foliage, that is,branches, trunk and root systems. The groupis a varied one taxonomically, and several ofthe pests included cross the damage-classifi-cation boundaries as defined here. Whilesome of these pests can cause sufficient dam-age to cause tree death, as a group they aregenerally considered less important than thefruit and foliage feeders.

19.5.1 Superficial woody-tissue and shootfeeders

Two groups of Homoptera (scales andmealybugs) are widespread and sometimesimportant pests of apple. San Jose scale

(Quadraspidiotus perniciosus (Comstock)) iswidely distributed and, left unchecked, cancause reduced tree vigour or even mortality(Plate 19.11). Scales feed primarily throughtree bark, forming large encrustations thatdevitalize the tree. Mealybugs (especiallyPseudococcidae) also suck plant juices, butusually choose more tender tissues (shootsand leaf axils) as feeding sites. In the lattercase, the primary damage is not fromremoval of plant product, but rather the pro-duction of honeydew (liquid drops of excre-ment rich in simple sugars). Honeydewdripping on fruit can cause fruit russeting onsensitive cultivars or can support the growthof sooty mould, a superficial but unsightlyfungal growth.

Both scales and mealybugs are consideredto be induced secondary pests, which wouldoccur only at low levels if their natural-enemy complex were not decimated bybroad-spectrum pesticides. Currently, thepre-bloom use of horticultural spray oilsappears to keep scales in check, although thisactivity is probably supplemented by in-sea-son use of organophosphates. Mealybugs, onthe other hand, can be extremely persistentonce established (usually in large, older trees)and even an intense spray programme canonly keep them in check, not eradicate them.Both species will infest the fruit towards thelatter part of the season, especially whenpopulations are high. A red ring appearsaround the scale that settles on fruit; mealy-bugs usually move to the calyx, where detec-tion is difficult during packing operations.Feeding in the calyx end causes a softeningand deterioration, which may be exacerbatedby long-term storage. Quarantine measuresand food contamination are issues with thesetwo groups of pests.

The psyllids (Homoptera: Psyllidae) arekey pests of pear, but one species, Psylla mali(apple sucker), is a corresponding pest ofapple in some regions. Like pear psylla, thispest feeds on shoots and produces honey-dew, with the attendant problems for fruitand vegetative growth. However, its impor-tance on apples is minor in magnitude com-pared with the related species attacking pear.

Another large and important group ofhomopterans (aphids) may also be classed as



shoot feeders. This group has specialized inphloem feeding and is a large and successfulgroup of pests on many crops. The aphidsthat feed on apple may use it as their onlyhost or as the primary or overwintering host,with a different plant species as a summerhost. The two life-history patterns have adefinite influence on management.

Apple aphid (Aphis pomi) (Plate 19.12) isa widespread pest of apple, occurring inmost apple-growing regions of the world. Itspends its entire life cycle on apple, repro-ducing by parthenogenesis for the greaterpart of the season. Winged (alate) forms areproduced under high population levels tocolonize new host plants, and in theautumn sexual forms are produced, whichmate and lay overwintering eggs. Bothleaves and shoots are attacked, and somelevel of growth reduction is assumed underheavy attack; however, most of the concernfor this pest involves the production of hon-eydew and sooty mould and the resultingfruit contamination.

Several other common aphid species areheteroecious, although their damage maybe quite distinct from that of apple aphid.The rosy apple aphid (Dysaphis plantagineaor Dysaphis devecta) also feeds on shoots andleaves, but injects a salivary toxin, whichseverely deforms both organs. In addition,the toxin causes fruit deformity on sensitivecultivars. This pest colonizes a herbaceousweed host during the summer; thus controlmeasures must occur fairly early in order tobe effective. Woolly apple aphid uses elm asthe alternative host in some areas, but isfunctionally monophagous in the north-western USA and Europe. This species pro-duces both aerial and edaphic colonies; theformer are easily controlled, the latter withgreat difficulty. The root colonies arethought to devitalize the tree and, eventhough rootstocks were developed specifi-cally to be resistant to woolly apple aphid(the Malling–Merton series), there is evi-dence that this resistance is breaking down.Feeding by both the root and shoot coloniesproduces galls; typically, the above-groundgalls (which occur in leaf axils) are prunedoff and are of little significance. Severalspecies of Rhopalosipum (R. fitchii and R.

insertum) are occasional pests of apple,using one of the Gramineae as their summerhost. Only very heavy infestations, whichcan infest developing fruitlets, are consid-ered damaging.

Aphids have a rich and varied natural-enemy complex that prey on them, includinglacewings (Chrysopa and Hemerobius), coc-cinellids (ladybirds), various parasitic waspsand a variety of predatory mirids (e.g.Campylomma, Deraeocoris, Orius). Despitethis, aphids often escape from biological con-trol. Many of their predators are generalistsand will only be attracted to large aphidpopulations (i.e. after the point where con-trol is needed or desired). A number ofbroad-spectrum pesticides used in orchardsare toxic to one or more of these natural ene-mies and disruption of biological controlearly in the season may preclude stable regu-lation for the rest of the season.

Woolly apple aphid (Plate 19.13) was oneof the earliest targets (1920s and 1930s) of awidespread introduction of a biological-con-trol agent, the parasitic wasp Aphelinus mali.This wasp was introduced in many of theareas around the world where woolly appleaphid had also been introduced and wassuccessfully established in most areas(Yothers, 1953). It is still thought to providethe primary means of biological controltoday, although the generalist predatorsdescribed above also play a role.

19.5.2 Wood-boring insects

Several families of Lepidoptera attack thecambium of the trunk and major scaffoldlimbs, and prolonged attack can girdle andkill these organs. The clearwing moths(Sesiidae) have several species that attackvarious fruit and ornamental trees and atleast one species that infests apple(Synathedon myopaeformis; UK and continen-tal Europe). One species of tortricid moth(cherry-bark tortrix, Enarmonia formosana)causes a similar type of damage.

While rarely a problem in sprayedorchards, these insects can be difficult to con-trol once established. It is difficult, if notimpossible, to kill larvae in their galleries



with pesticides; thus pesticidal control mea-sures must be directed at the adults. Typicallythey are univoltine, with a prolonged flight,making continuous coverage a necessity.

The scolytid beetles comprise some of themore serious forest pests, and several speciesin the genera Scolytus and Xyloborus are pestsof apple. The larvae form distinctive galleriesin the wood, and adults often bore intoshoots just below buds, causing weakeningand breakage. In general, these insects areusually attracted to trees that are alreadyweakened by some other pest or disease,although young trees can suffer damagewhen they are close to a source of emergingadults. Coleopteran wood-borers in the fami-lies Buprestidae and Cerambycidae may alsoattack apple, but are rare in sprayed com-mercial orchards.

19.5.3 Root-system pests

This is a fairly restricted group of pests,which are given little attention eitherbecause they cause only occasional damageor because of their cryptic life history. Thelarvae of scarab beetles (several species inthe genera Polyphylla and Pleocoma) feed onroots and can be locally severe. Trees onsandy soils where the grubs thrive may suf-fer long-term damage; orchardists will oftenreplant repeatedly, trying various combina-tions of fertilizer or watering to promote treegrowth, when in fact the root system is beingsystematically destroyed.

Soil fumigation is currently the best rem-edy to allow trees sufficient time to establishbefore the beetles reinfest the orchard. Soil-applied pesticides are widely discouraged

because of groundwater contaminationissues. While biological-control agents areknown, their management is little studied or applied. Entomophagous nematodes(injected into the soil) may alleviate the prob-lem, but their effect is not well studied intree fruits.

One very large species of cerambycid bee-tle (Prionis sp.) can attack apple; control mea-sures are similarly difficult. Weevil(curculionid) larvae are known to attack theroot system on occasion, but the extent ofdamage is not well defined. The adults ofsome species may also be problematic whenthey feed on fruits, fruit stems or foliage.

Woolly apple aphid is the only truly ubi-quitous root pest of apple (see above),although typically only the aerial coloniesare treated.

19.6 Conclusion

Apple pest management is continuallyevolving in response to changing horticul-tural practices, the genetic structure of insectpopulations, the importation or re-emer-gence of new pests and societal pressures.These pressures encompass fewer and saferresidues on food products, reduced environ-mental impact and the concept of sustainableagricultural production. The result has beenincreased regulation of pesticide use world-wide and incentive programmes (specialtylabels) that promote reduced-impact pest-management programmes. With the global-ization of fruit marketing, it is likely that allcountries wanting to export apples will haveto conform to production and pest-manage-ment practices that embrace these concepts.


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19 ecology and management of apple arthropod pests · 19.1 introduction apples present a distinct...

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