Agriculture

Ecosystems &
Enwronment
ELSEVIER Agriculture, Ecosystem and Environment 57 (1996) 35-47

Arthropod pest and natural enemy abundance under second-level

versus first-level integrated pest management practices in apple
orchards: a 4-year study
Ronald J. Prokopy *, Jennifer L. Mason, Margaret Christie, Starker E. Wright
Departmentof Entomology, Universityof Massachusetts, AmherstMA 01003, USA
Accepted 20 October 1995

Abstract

The authors conceive of second-level integrated pest management (IPM) in apple orchards as involving integration of
multiple management tactics across all classes of pests. From 1991-1994, a second-level IPM pilot project was carried out
in six commercial Massachusetts apple orchard blocks ( 2 - 4 ha) in which pest and natural enemy populations and injuries to
fruit were compared with those in adjacent blocks receiving first-level IPM practices (considered to be integration of tactics
within a single class of pests). The approach to second-level IPM was use of chemically based tactics for arthropod, disease
and weed control during the first part of the growing season (up to mid-June for arthropods) and thereafter use of only
biologically based tactics (cultural, behavioral and biological control methods). This article deals with findings on arthropod
management. As expected, total injury to fruit by insects causing damage before mid-June did not differ between
second-level (4.7%) and first-level (4.8%) IPM blocks. Total injury to fruit by insects active after mid-June averaged about
the same (0.5%) in both types of blocks in 1991 and 1992, but in 1993 and 1994 it averaged more in second-level blocks
(4.8%) than first-level blocks (1.9%). This was particularly true for Grapholitha prunivora Walker and leafrollers and less
so for Cydia pomonella (L.) and Rhagoletis pomonella (Walsh). Among foliar pest arthropods and their natural enemies,
populations of aphids and aphid predators and populations of spider mites and mite predators averaged about the same in
both types of blocks. Populations of leafminers averaged lower and parasitoids of leafminers averaged greater in
second-level blocks. Populations of leafhoppers averaged greater in second-level blocks. Pesticide use against fruit-damaging
insects averaged 37% less in second-level than in first-level blocks, but against foliar-damaging arthropods, it was not less.
Some refinements of second-level IPM tactics for arthropod control are needed before second-level IPM practices can be
recommended broadly to commercial growers in New England as an economical and reliable alternative to first-level IPM.

Keywords: Integrated pest management; Apple

1. Introduction trol in an ecologically and economically sound man-

As described by D o v e r (1985), ideally integrated
pest management (IPM) ought to optimize pest con-
* Corresponding author.
ner, emphasize coordinated use of multiple tactics to
assure stable crop production, and maintain pest
damage below injurious levels while minimizing
hazards to humans, animals, plants and the environ-
ment. During the past 3 decades or so in which
researchers, extension personnel, private consultants

0167-8809/96/$15.00 © 1996 Elsevier Science B.V. All rights reserved

SSDI 0167-8809(95)00657-5
36 R.J. Prokopy et al./ Agriculture, Ecosystem and Environment 57 (1996) 35-47
and farmers have gained experience with application
of these ideals in IPM programs across a wide range
of crops, numerous benefits as well as several con-
straints associated with IPM have emerged (Corbet,
1981; Miller, 1983; Wearing, 1988; Rajotte, 1993;
Zalom, 1993). Benefits often include reduction in
amount and cost of chemically based (pesticidal)
control measures and improvement in crop yield or
quality. Constraints usually are expressed as being of
a social, institutional, educational or technical nature.
Technical constraints become particularly challeng-
ing as practitioners move from chemically based
toward biologically based forms of IPM (Frisbie and
Smith, 1991).
As an aid for measuring progress toward achiev-
ing an ideal program of IPM for apple orchards,
Prokopy (1993, Prokopy (1994) proposed that
progress be viewed in the form of taking a series of
steps, analogous to climbing steps of a ladder. The
first step up the ladder (equivalent to first-level IPM)
involves integrating use of chemically based and
biologically based management tactics within a sin-
gle class of pests, such as arthropods, diseases, weeds
or vertebrates. The second step (equivalent to sec-
ond-level IPM) integrates multiple management tac-
tics across all classes of pests. Third-level IPM
emphasizes integration of pest management ap-
proaches with the entire system of crop production
on a farm. Fourth-level IPM involves social, cultural
and political realms. Progress under first-level IPM
for apple orchards has been reported for Australia
(Be wer et al., 1993), Europe (references in Blom-
me~ ;, 1994) and North America (references in
Prckopy and Croft, 1994). Guidelines for integrated
production of apples in Europe corresponding to
second-level (and even third-level) IPM practices are
given in Dickler and Schafermeyer (1990). Progress
by some European apple growers in production and
marketing of high quality fruit under second- or
third-level IPM is described by Oberhofer (199t)
and Cross (1996). Implementation of second- or
third-level IPM practices in North American apple
orchards is in a state of early development.
From 1991-1994, a second-level IPM pilot pro-
ject was conducted in blocks of trees at several
commercial apple orchards in Massachusetts. The
evolution of concepts and practices leading up to
initiation of this pilot project, together with a subset
of findings for 1993, are given in Prokopy et al.
(1994). The predominant approach to second-level
IPM involved use of chemically based tactics for
arthropod, disease and weed control during the first
part of the growing season (up to mid-June) and
thereafter use of biologically based tactics. It was
believed that relying to the greatest extent possible
on biologically based tactics during the second part
of the growing season would maximize the potential
for build-up of beneficial natural enemies of arthro-
pod pests, reduce selection pressure on pests to
develop resistance to pesticides and minimize the
amount of pesticide residue on the fruit at harvest.
The objective was to compare pest and natural en-
emy populations and injuries to fruit in second-level
IPM blocks with those in adjacent first-level IPM
blocks that were under chemically based manage-
ment throughout the growing season. Here, all 4
years of findings for arthropods are presented. Find-
ings on disease, weed and vertebrate pest manage-
ment are planned for future articles.
2. Materials and methods
In each of six commercial orchards, one second-
level IPM pilot project block and one first-level IPM
block were established, each ~ 2-4 ha. Nearly all
blocks were bordered on two sides by woods, on one
side by an open field and on one side by apple trees
under first-level IPM management. Both types of
blocks consisted primarily of 'Mclntosh', 'Cortland',
'Red Delicious' and 'Empire' cultivars on M.26 or
M.7 rootstock. Crop load in each block varied from
medium to heavy during the 4 years of study.
In Massachusetts, principal fruit-damaging arthro-
pod pests on apple trees active from bud break until
mid-June include tarnished plant bug, Lygus lineo-
Iaris (Palisot de Beauvois), European apple sawfly
Hoplocampa testudinea (Klug), plum curculio,
Conotrachelus nenuphar (Herbst), green fruitworms,
Orthosia spp. , and first generations of San Jos~
scale, Quadraspidiotus perniciosis (Comstock), red-
banded leafroller, Argyrotaenia velutinana (Walker),
obliquebanded leafroller, Choristoneura rosaceana
(Harris), lesser appleworm, Grapholitha prunivora
Walker, and codling moth, Cydia pomonella (L.).
Principal foliar-damaging arthropods active in or-
 R.1. Prokopy et a l . / Agriculture, Ecosystem and Enoironment 57 (1996) 35-47
chards during this time include first generations of
European red mite, Panonychus ulmi (Koch), Phyl-
lonorycter lea/miners, and white apple lea/hopper,
Typhlocyba pomaria McAtee.
Because no effective biologically based control
methods have been developed for several of these
pests, particularly tarnished plant bug, European ap-
ple sawfly, plum curculio and green fruitworms, the
authors felt obliged to rely upon chemically based
methods of control up to mid-June (none of these
four pests causes injury after mid-June). Determina-
tion of need and timing of pesticide application
against arthropod pests active up to mid-June was
based on monitoring pest abundance. The monitoring
methods used, described in Prokopy et al. (1994),
were employed in both second- and first-level IPM
blocks. Pesticides used to treat either type of block in
which an arthropod pest exceeded an action thresh-
old (Prokopy et al., 1991) included diflubenzuron
(experimental use permit) against lea/miners in sec-
ond-level blocks, oxamyl or methomyl against
lea/miners in first-level blocks, endosulfan against
lea/hoppers and phosmet or azinphosmethyl against
all other insects. Horticultural oil was applied pre-
bloom to all blocks against overwintering European
red mite eggs and overwintering San Jos~ scale as a
preventative treatment.
In Massachusetts, principal fruit-damaging arthro-
pod pests on apple trees active from mid-June to
harvest include apple maggot, Rhagoletis pomonella
(Walsh), and summer generations of codling moth,
lesser appleworm, lea/rollers and San Jos~ scale.
Principal foliar-damaging arthropods include apple
aphids, Aphis pomi DeGeer, spirea aphids, Aphis
spiraecola Patch, woolly apple aphids, Erisoma
lanigerum (Hausmann), rose lea/hoppers, Edward-
siana rosae (L.), potato lea/hoppers, Empoasca fabae
(Harris), two-spotted spider mites, Tetranychus ur-
ticae (Koch), and summer generations of European
red mites, lea/miners and white apple lea/hoppers.
In second-level IPM blocks, 8-cm red spherical
sticky-coated traps were used (Tangletrap TM) to con-
trol apple maggot. Each trap was baited with a
polyethylene vial containing the synthetic fruit at-
tractant butyl hexanoate (release rate = 500/zg h- l )
and one semi-permeable membrane containing the
synthetic food attractant ammonium acetate (Consep
Membranes Inc., Bend, OR). In late June, traps were
37
placed 5 m apart on perimeter apple trees to intercept
adults entering orchard blocks from neighboring
abandoned trees up to 2 km away. The authors chose
this perimeter-tree approach to trap deployment be-
cause their prior experience suggested that the vast
majority of apple maggot flies infesting Mas-
sachusetts orchards originated from neighboring un-
sprayed apple trees and not within the orchard itself.
To minimize within-orchard origin and emergence of
apple maggot flies, it was requested at the outset that
fallen apples in each second-level block be removed
by growers at weekly intervals. None of the cooper-
ating growers was able to carry out this recommen-
dation, however. Traps were cleaned and the sticky-
coating renewed (if needed) every 2 weeks until
harvest. For controlling summer generations of
codling moth and lesser appleworm, all unsprayed
apple and pear trees (primary hosts of these pests)
within 100 m of the orchard block perimeter were
cut down to discourage females of these pests from
entering the block (Prokopy et al., 1990). None of
the first-level IPM blocks was close enough to be
affected by this practice. No direct action was planned
against lea/rollers, San Jos~ scale, or foliar pests
because it was anticipated that these pests would be
held below injurious levels by natural enemies build-
ing up in the absence of insecticide or acaricide use
after mid-June.
In first-level IPM blocks, arthropod pests active
after mid-June were monitored and treated by grow-
ers with pesticide based on recommended thresholds
(Prokopy et al., 1991) or the grower's own criteria
for need to treat. Pesticides used for treating first-
level IPM blocks after mid-June included: phosmet,
azinphosmethyl or chlorpyrifos against apple mag-
got, codling moth, lesser appleworm or lea/rollers;
horticultural oil, hexakis or propargite against mites;
methomyl against lea/miners and endosulfan against
leafhoppers.
To estimate the amount of insect-injured fruit in
each block at harvest, 10 fruit on each of 20 interior
trees of each principal cultivar and 10 fruit on each
of 10 perimeter-row trees were examined (average
number of fruit sampled per block = 700). To esti-
mate the abundance of fotiar-feeding pests and
predators of pests in each block, every other week
from petal fall to harvest, 10 fruit cluster leaves and
10 shoot terminals on each of 20 interior trees were
38 R.J. Prokopy et al./ Agriculture, Ecosystem and Environment 57 (1996) 35-47

examined. Samples of fruit and foliage from interior
trees were taken in an X pattern across the block. In
each case, the proportion of fruit or leaves with or
without the characteristic injury or arthropod in ques-
tion was recorded (the only exception was leafmin-
ers, where the number of mines per leaf was counted).
Leaves containing leafminer larvae were brought to
the laboratory to determine the proportion of miners
parasitized by hymenopterous larvae. Finally, to
monitor penetration of apple maggot flies into the
interior of second-level and first-level blocks, one
unbaited sticky red sphere trap was hung about 5 m
inward from each comer of each block. In addition,
four such traps were hung near the center of each
block.
Student's t-test at the P = 0.05 level of signifi-
cance was used to compare mean levels of fruit
injury and arthropod pest and natural enemy popula-
tions in second-level and first-level IPM blocks.
Separate comparisons were made for each year as
well as across all 4 years combined. In the case of
foliar pest and natural enemy populations, mean
population levels per block per year were calculated
by taking the percentage of sampled leaves or shoots
containing the arthropod in question for each sam-
pling date from its first to last appearance in samples
and averaging these mean percentages across all
samples. In addition, for each block, the percentage
sampled leaves or shoots containing the arthropod in
question when it was at its peak population for the
year was determined. In no case was there any
discrepancy between a mean population index and a
peak population index in terms of pattern of signifi-
cant difference between second- and first-level
blocks. Data are presented in terms of mean rather
than peak population levels.
3. Results
Table 1 shows the mean dosage equivalents of
pesticide used in second-level and first-level IPM
blocks for each of the 4 years of the study. Amounts
of pesticide applied against fruit-damaging insects
before mid-June averaged the same (2.4 dosage
equivalents) in both types of blocks; after mid-June,
however, first-level blocks were the only blocks to
receive pesticide against such insects (average of 1.4
dosage equivalents). Against foliar-damaging arthro-
pods, amounts of pesticide used before mid-June
averaged slightly greater in second-level than first-
level blocks (2.5 vs. 1.9 dosage equivalents). Of
these amounts, 1.5 dosage equivalents in each type
of block were in the form of pre-bloom horticultural
oil sprays against overwintering European red mite
eggs; 0.5 dosage equivalents in second-level blocks
were mistakenly applied by growers against leafmin-
ers when leafminer populations were still below

Table 1
Mean dosage equivalents a of pesticide used against fruit and foliar pests in six second-level and six first-level IPM blocks
Year IPM level Fruit insects Foliar arthropodsb
Before mid-June After mid-June
Before mid-June After mid-June M LM LH A M LM LH A
1991 ~d 2.0 0.0 1.9 1.0 0.I 0 0.5 0.0 0.2 0
1st 2.1 1.0 1.7 0.2 0.1 0 0.8 0.2 0.2 0
1992 ~d 2.4 0.0 0.9 1.1 0.2 0 0.0 0.0 0.0 0
1st 2.2 2.0 1.1 0.4 0.0 0 0.1 0.0 0.0 0
1993 2nd 2.7 0.0 1.8 0.3 0.0 0 0.4 0.0 0.2 0
1st 2.2 1.0 1.4 0.0 0.0 0 0.6 0.0 0.2 0
1994 ~d 2.6 0.0 1.6 0.3 0.3 0 0.0 0.0 0.3 0
1st 2.9 1.7 1.6 0.7 0.3 0 0.3 0.0 0.4 0
Avemge ~d 2.4 0.0 1.6 0.7 0.2 0 0.2 0.0 0.2 0
1st 2.4 1.4 1.5 0.3 0.1 0 0.5 0.1 0.2 0

a Dosage equivalent = actual amount of pesticide applied per hectare per application relative to amount recommended per application in the
1991 New England Apple Pest Management Guide
b M, mites; LM, leafminers; LH, leafhoppers; A, aphids.
 RJ. Prokopy et al.// Agriculture, Ecosystem and Environment 57 (1996) 35-47 39

threshold levels. After mid-June, amounts of pesti-
cide used against foliar-damaging arthropods aver-
aged 0.4 dosage equivalents in second-level blocks
(in the form of emergency treatments of propargite
against European red mites and insecticidal soap
against rose leafhoppers) and 0.8 dosage equivalents
in first-level blocks.
Combined injury on harvest fruit samples by in-
sects causing damage up to mid-June (plant bugs,
sawfly, plum curculio, fruitworms) averaged essen-
tially the same (2.0 vs. 1.9%) for second-level and
first-level blocks. Except for sawfly in 1994, there
were no significant differences between block types
in injury levels caused by any of these pests, either
within a single year or across all 4 years (Fig. 1).
The majority of injury in both types of blocks was
caused by tarnished plant bug.
Combined injury on harvest fruit samples by in-
sects initiating damage after mid-June (codling moth,
lesser appleworm, leafrollers, apple maggot and San
Jos6 scale) averaged somewhat greater for second-
level than first-level blocks (2.6 vs. 1.2%). Except
for lesser appleworm and leafrollers in 1994 and
lesser appleworm across all 4 years, there were no
significant differences between block types in injury
levels caused by any of these pests (Fig. 2). No fruit
injury by San Jos~ scale was found in any block in
any year. Of concern was the increase in codling
moth, lesser appleworm, leafroller and apple maggot
injury to fruit in second-level blocks during the last 2
years compared with the first 2 years (Fig. 2). To
illustrate, average injury levels in second-level blocks
for 1991 and 1992 combined versus 1993 and 1994
combined were 0.0 vs. 0.3% for codling moth, 0.0

Tarnished Plant Bug European Apple Sawfly

4

3.5 3.5

3 3

2.5 2.5

2 2

1.5 1.5

1 1

0.5 0.5

0 0
91 92 93 94 AV 91 92 93 94 AV
Year Year

Plum Curculio Green Fruit Worm

4

3.5

2.5

1.5

0.5

0 , , ' 0
91 92 93 94 AV 91 92 93 94 AV
Year Year

Fig. I. Percent injury ( ± SE) to fruit in harvest samples by insects causing damage before mid-June (1991-1994). In the case of tarnished
plant bug, 70% of the fruit injured exhibited injury (dimples) too slight to cause reduction in grade. Therefore, we report here only the 30%
that received injury sufficient to cause downgrading. Black bars = second-level IPM blocks; gray bars = first-level IPM blocks. * denotes a
significant difference between second-level and first-level blocks.
40 R.J. Prokopy et al. // Agriculture, Ecosystem and Enoironment 57 (1996) 35-47

vs. 1.4% for lesser appleworm, 0.2 vs. 1.2% for
leafrollers and 0.2 vs. 2.1% for apple maggot. Except
for apple maggot, there was no such marked trend
toward increased injury from the first 2 years com-
pared with the last 2 years in first-level blocks (Fig.
2). For apple maggot, captures on unbaited red sphere
monitoring traps averaged 16.9 vs. 12.3 per trap in
second-level versus first-level blocks across all 4
years (a significant difference), suggesting some dif-
ference between block types in number of flies pene-
trating the block interior. On average, 5901 apple
maggot flies per block per year were intercepted on
perimeter-tree baited red spheres in second-level
blocks, indicating high population pressure.
Among foliar pests, there were no significant
differences between second- and first-level blocks,
either within any year or across all years, in mean
population levels of apple aphids and spirea aphids
(combined), woolly apple aphids, European red mites
or two-spotted spider mites (Fig. 3). On the other
hand, each year leafminers averaged numerically
fewer in second-level than in first-level blocks, with
significant differences in 1991 and 1993 and across
all 4 years (Fig. 4). White apple leafhoppers were
significantly more abundant in second-level than in
first-level blocks in 1991 but not thereafter nor across
all 4 years (Fig. 4). Rose leafhoppers were signifi-
cantly more abundant in second-level than in first-
level blocks during both years in which they were
sampled (1993 and 1994) (Fig. 4). Potato leafhop-
pers were significantly more abundant in second-level
than in first-level blocks in 1992 and 1994 and
across all 4 years (Fig. 4).
Among natural enemies of foliar pests, predators
of aphids were very abundant in both types of blocks,
with no significant differences between block types

Codling Moth Lesser Apple Worm

4
3.5 3.5
3 3
2.5 2.5
•_~ 2 •_~ 2
N 1.5
N 1.5
1 1
0.5 0.5
0 0
91 92 93 94 AV
91 92 93 94 AV
Year Year

Leafrollers Apple Maggot Fly

4

3.5 3.5

3 3

2.5 2.5

2 2

1.5 1.5

1 1

0.5 0.5

0 0
91 92 93 94 AV 91 92 93 94 AV
Year Year
Fig. 2. S a m e as Fig. 1 except d a m a g e w a s c a u s e d b y insects active after mid-June. There w a s n o injury in a n y b l o c k c a u s e d b y San Jos~
scale.
 RJ. Prokopy et al./ Agriculture, Ecosystem and Environment 57 (1996) 35-47 41

either within or across years (Fig. 5). For each block in abundance of either type of predator, either within
type, - 73% of observed aphid predators were lar- or across years (Fig. 5). Of the several hundred mite
vae of Aphidoletes aphidimyza (Rondani). Nearly all predators identified to species, all phytoseiids were
of the remainder were larvae of Syrphus spp. For Amblyseius fallacis (Garman) and nearly all stig-
each year in which they were sampled (1993 and maeids were Zetzellia mali (Ewing).
1994), parasitoids of second-generation leafminer
larvae were significantly more abundant in second-
level than in first-level blocks (Fig. 5). For each 4. Discussion
block type, ~ 70% of parasitized leafminer larvae
were parasitized by larvae of Sympiesis marylanden- Up to mid-June, second-level IPM blocks in this
sis Girault. Most of the remainder were parasitized 4-year pilot project were treated with pesticide against
by larvae of Pholetesor ornigis (Weed). Although fruit-damaging insects and foliar-damaging arthro-
phytoseiid mite predators were numerically less pods to essentially the same extent as first-level IPM
abundant in second-level than in first-level blocks in blocks. Thereafter, behavioral, cultural and biologi-
1992, 1993 and 1994 and stigmaeid mite predators cal control tactics were substituted completely for
were numerically more abundant in second-level than pesticide use against fruit-damaging insects and
in first-level blocks in 1991, 1992 and 1994, there largely so against foliar-damaging arthropods. As
were no significant differences between block types expected, the extent of injury to fruit by insects

Apple & Spirea Aphids Woolly AppleAphids

60 60

t
55 55
50

_-== 45
40
~
~ 4o
45

35 ~ as
2 30 2 30
25 ~- 2s
20 ® 20
i 15
10 ~ 10
5 5
0 0
92 93 94 AV 91 92 93 94 AV
Year Year

European Red Mites Two Spotted Mites

60 . . . . . 60
55 . . . . . 55 - -
50'~ - . . . . . . 50
45 ~ 45
40
=e
_= 35 _= 35
30 30 . . . . .
25 -- -
2O 20 . . . . . . .
15 15 . . . .
10 10
5
0 0 --- i - I -- i
91 92 93 94 AV 91 92 93 94 AV

Year Year
F i g . 3. M e a n p o p u l a t i o n l e v e l s ( + S E ) o f f o l i a r a r t h r o p o d p e s t s in s e c o n d - l e v e l I P M b l o c k s ( b l a c k b a r s ) a n d f i r s t - l e v e l I P M b l o c k s ( g r a y
bars) (1991-1994). *denotes a significant difference between second- and first-level blocks.
42 RJ. Prokopy et al. / Agriculture, Ecosystem and Environment 57 (1996) 35-47

causing damage before mid-June did not differ be-
tween second- and first-level blocks. Injury to fruit
caused by insects active after mid-June was about
the same in both types of blocks during the first 2
years of the project but was somewhat greater in
second-level than first-level blocks during the last 2
years. Comparative abundance of foliar pests and
their natural enemies in each block type varied ac-
cording to species.
Many tree fruit researchers have predicted that
grower implementation of more advanced levels of
IPM may be accompanied by increased amounts of
pest injury to fruit as pesticide use is reduced or
eliminated. Results of 3- or 4-year studies in which
practices equivalent to those of second- or third-level
IPM were applied in California or Washington apple
orchards support this prediction (Caprile et al., 1994;
Vossen et al., 1994; Knight, 1995). Likewise, find-
ings here are consistent with this prediction.
For codling moth, the amount of injury increase
above that which occurred in first-level IPM blocks
was only slight, even during the 4th year, when it
reached a marginally acceptable level of 0.3%. But
data trends suggest that if second-level IPM practices
were to be employed continuously for 5 or more
years, control of second-generation codling moth
solely via management of the habitat adjacent to
orchards, as practiced here, might not be sufficient to
prevent economically important fruit injury. Alterna-
tives, such as orchard treatment with mating disrup-
tion pheromone or biological control agents (eg.
virus, bacteria, parasitoids), might be required in
addition (van der Geest and Evenhuis, 1991; Howell
et al., 1992; Caprile et al., 1994; Vossen et al., 1994;
Knight, 1995).
For lesser appleworm, fruit injury in second-level
blocks rose sharply and substantially in the 4th year,
reaching an unacceptable level of 2.4% (compared

Leafminers White Apple Leafhoppers

60 60
55 55
50 5O
45 45
40 40
g 35
tO
~ 35
30 w 30
25 ~ 25
20 ~ 20
I
6 15 N 15
Z
10 10
5 5
0 0
91 92 93 94 AV 91 92 93 94 AV

Year Year

Rose Leafhoppers Potato Leafhoppers

60 60
55 55
50 5O
45
40 ~ 40
35
~ 35
m 2 30
30
8> ~- 2s
25
~ 20
20
15 N 10
5
5 0
0 92 93 94 AV
93 94 AV
Year
Year
Fig. 4. S a m e as Fig. 3.
 R.J. Prokopy et al. /Agriculture, Ecosystem and Environment 57 (1996) 35-47 43

with only 0.2% in first-level blocks) and suggesting
that management of the habitat adjacent to orchards
might be less reliable for control of second-genera-
tion lesser appleworms than second-generation
codling moths. The host range of lesser appleworm
is broader than that of codling moth (Chapman and
Lienk, 1971). Thus, populations of lesser appleworm
may have built up on host species which were not
removed from within 100 m of borders of second-
level blocks. Much less is known about the biology
and management of lesser appleworm than codling
moth. Presently, there appear to exist few proven
pesticidal alternatives for effective lesser appleworm
control, although mating disruption via pheromone
treatment may be a future possibility (Pfeiffer and
Killian, 1988).
Leafrotler injury in second-level blocks reached
an unacceptable level of 1.1% by the 4th year (com-
pared with 0.1% in first-level blocks). The vast
majority of such injury was caused by obliquebanded
leafrollers and redbanded leafrollers. No overt mea-
sures were taken to control leafrollers in second-level
blocks. In view of this fact and the much greater
economic problems caused by leafrollers in other
locales, both nearby (Agnello, 1992) and more dis-
tant (Pfeiffer et al., 1993), it is perhaps comforting
that leafroller injury in second-level blocks rose to
no greater heights than it did. Use of pheromone to
disrupt leafroller mating (Agnello, 1992; Pfeiffer et
al., 1993; Blommers, 1994) could be a viable alterna-
tive to pesticides for leafroller control should leafrol-
ler populations in Massachusetts orchards practicing

2nd Generation Leafminer

Aphid Predators Parasitoids
6O 60
55 55
~ 5o 50
45
40 40
~ as 35
£ 30 30
~- 2s 25
~ ao 20
~ 15 15
N 10 10
5 5
0 0
91 92 93 94 AV 93 94 AV
Year Year

Phytoseiid Mite Predators Stigmaeiid Mite Predators

10
9
8

m
~ 5
g 4
3
~ 3
2
1
0
91 92 93 94 AV 91 92 93 94 AV
Year Year
Fig. 5. Mean population levels ( + SE) of natural enemies of arthropod pests in second-level IPM blocks (black bars) and first-level IPM
blocks (gray bars) (1991-1994). * denotes a significant difference between second- and first-level blocks.
44 R.J. Prokopy et al./ Agriculture, Ecosystem and Environment 57 (1996) 35-47
second-level IPM reach levels that economically jus-
tify such treatment.
Injury by apple maggot in second-level blocks
reached 3.0% of sampled fruit by the 4th year.
Although this amount of injury is unacceptable for
most commercial growers, two factors modify inter-
pretation of the extent of injury severity. First, apple
maggot injury in pesticide-treated first-level IPM
blocks likewise was exceptionally great (2.1%) dur-
ing 1994. Secondly, an average of more than 12500
apple maggot flies was captured on perimeter-tree
interception traps in second-level blocks in 1994,
indicating extremely high fly population pressure.
Conditions that were ideal for large build-up of apple
maggot pupae beneath wild hosts during late summer
of 1993, coupled with ideal conditions for overwin-
tering of pupae thereafter, undoubtedly contributed
strongly to the exceptional 1994 fly populations.
Furthermore, it has been established that sticky red
sphere traps lose about 25% of their fly capturing
potential each week they are not cleaned of apple
maggot flies and other insects (Duan and Prokopy,
1995). The trap servicing schedule did not permit
cleaning more often than every 2 weeks, which must
have allowed at least some proportion of alighting
flies to escape from traps and move into the interior
of blocks (possibly accounting for the average 37%
greater number of flies captured on unbaited moni-
toring traps in second-level compared with first-level
blocks). To overcome this disadvantage of sticky red
spheres and to overcome the messiness associated
with preparing and employing such spheres, develop-
ment of pesticide-treated red spheres as an alterna-
tive is being pursued (Duan and Prokopy, 1995).
With respect to foliar pests and their natural
enemies, it was gratifying but not surprising that
neither apple or spirea aphids nor foliar populations
of woolly apple aphids reached damaging numbers
in any second-level blocks in any year. In fact, the
same was true for first-level blocks. Substantial pop-
ulations of aphid predators in both types of blocks
provided excellent biocontrol. Two factors con-
tributed to this favorable outcome. First, the time of
Aphidoletes and Syrphus aphid predator peak activ-
ity in orchards coincided closely with that of build-
ing and peak pest aphid populations (mid-June to
mid-July), a period during which even first-level
IPM blocks normally receive little insecticide. Sec-
ondly, A. aphidimyza (to a lesser extent Syrphus
spp.) is somewhat tolerant of both phosmet and
azinphosmethyl (Croft, 1990), the most commonly
used insecticides during June and July in Mas-
sachusetts orchards practicing first-level IPM.
Disappointingly, populations of pest mites were
not significantly lower and populations of predatory
mites were not significantly greater in second-level
than in first-level blocks. Indeed, in both types of
blocks occasional post-bloom intervention with aca-
ricide was required (Table 1) when pest mites ex-
ceeded threshold levels following pre-bloom treat-
ment with horticultural oil. At least two factors may
have contributed to the lack of a reliable level of
predator control of pest mites in second-level blocks.
First, of the two predaceous mite species found in
second- and first-level blocks, A. fallacis is believed
to be much more capable than Z. mali of providing
effective biocontrol of moderate to high pest mite
populations (Santos, 1976; Clemens and Harmsen,
1992; Croft, 1994; Nyrop et al., 1994; Hardman et
al., 1995). However, A. fallacis appears to suffer
high mortality during New York and Massachusetts
winters (Nyrop, 1993; Hu et al., 1995), and for this
and possibly also other reasons, was not found in
samples from any block in any year until July, too
late to have affected pest mite populations that
reached damaging numbers before July. Secondly,
even though both A. fallacis and Z. mali have
developed considerable resistance to organophos-
phate insecticides of the type used in orchards in-
volved here (Croft, 1990), they and other species of
predaceous mites are known to be affected adversely
by the fungicides benomyl, mancozeb or metiram
(Baynon and Penman, 1987; Hagley and Biggs, 1989;
Ioriatti et al., 1992; Hardman et al., 1995). All three
of these materials were used in two or more spray
applications to both second- and first-level blocks
(principally during May and June) each year of this
pilot project. They may have been a principal con-
straining factor on predaceous mite build-up in both
types of blocks (Cooley et al., 1995).
Advantages of second-level over first-level IPM
practices in regard to foliar pest management were
perhaps best exemplified by the significantly greater
abundance of second-generation leafminer para-
sitoids in second-level than first-level blocks. Such
parasitoids may have been a principal factor account-
 R.J. Prokopy et a l . / Agriculture, Ecosystem and Environment 57 (1996) 35-47
ing for numerically lower levels of leafminer popula-
tions in second-level blocks each of the 4 years as
well as for the fact that in no second-level block did
second- or third-generation leafminer larvae (present
in July or August) require intervention with pesticide
(Table 1). Even so, the amount of parasitism of
first-generation leafminer larvae (present in May and
June) was no different between block types (R.G.
Van Driesche, J. Mason and R.J. Prokopy, unpub-
lished data), undoubtedly reflecting high parasitoid
susceptibility to organophosphate insecticides (Pree
et al., 1994) applied before mid-June to both types of
blocks. Immigration of leafminer parasitoid adults
from nearby wild host plants (Maier, 1994; Van
Driesche et al., 1994) into second-level blocks after
mid-June and their subsequent survival there in the
absence of insecticide may largely account for the
higher levels of second-generation leafminer para-
sitism observed in these blocks. Knight (1995) found
greater levels of parasitism of leafminer larvae in
blocks that received mating disruption pheromone
for codling moth control compared with convention-
ally sprayed blocks.
Perhaps the greatest shortcoming of second-level
practices used here, with respect to arthropod foliar
pest management, involves the significant build-up
of leafhoppers after mid-June in second-level com-
pared with first-level blocks. After the 1st year,
white apple leafhoppers were not a problem in this
regard. However, rose leafhoppers and potato
leafhoppers were problems in second-level blocks
each year in which they were sampled, sometimes
requiring intervention with pesticide treatment (Ta-
ble 1). First-generation rose leafhopper nymphs de-
velop almost exclusively on rose bushes growing
outside of orchards, with adults then immigrating
into orchards from mid-June to mid-July and produc-
ing a second and third generation of nymphs in
orchards during summer (Day and Hogmire, 1993;
Straub and Jentsch, 1994). Similarly, potato leafhop-
per adults originating from far-distant sources
(southern states of the USA) immigrate into orchards
from mid-June onward, producing one or more gen-
erations of nymphs before moving to other plants.
Conceivably, immigration of rose leafhoppers could
be reduced to tolerable levels by removing rose
bushes within yet undetermined distances from or-
chard borders. Nonetheless, some other currently
45
unavailable biologically based approach will have to
be developed for managing potato leafhoppers if
Massachusetts growers practicing second-level IPM
are to cope with this pest in the absence of insecti-
cide use after mid-June.
As reported in detail elsewhere (Prokopy et al.,
1995), in second-level blocks there was variation
among cultivars in the amount of fruit injury caused
by insects active after mid-June and in abundance of
foliar pests. Thus, codling moth and apple maggot
inflicted more damage on 'Red Delicious' than on
'Cortland' or 'Mclntosh'. Lesser appleworm was
particularly injurious to 'Cortland'. Leafroller was
greater on 'Cortland' and 'Red Delicious' than on
'Mclntosh'. Mites, leafminers and leafhoppers were
most abundant on 'Red Delicious'. This suggests
that with respect to management of fruit- and foliar-
damaging arthropods, orchard blocks composed pre-
dominantly of cultivars such as 'Mclntosh' may reap
maximum benefit with minimum disadvantage from
employment of second-level IPM practices. Such
may not be the case, however, for blocks comprising
largely 'Cortland' or 'Red Delicious'.
As in this study on apple pest management, stud-
ies on the management of pests of other crops where
biologically based approaches to pest control have
been substantially or completely substituted for pes-
ticidal approaches (e.g. Trumble and Alvarado-
Rodriguez, 1993) likewise have indicated benefits.
These include greater environmental health and food
safety, build-up of certain beneficial organisms and
reduced potential for development of pest resistance
to pesticides. At the same time, however, there may
be shortcomings in terms of increased levels of
damage by some pests. To what extent might such
potential benefits and shortcomings affect grower
willingness to adopt advanced approaches to IPM?
In northeastern North America, many apple grow-
ers have gained considerable economic advantage by
engaging in chemically based first-level IPM prac-
tices compared with non-IPM practices (Prokopy et
al., 1980; Hull et al., 1983; Bostanian and Coulombe,
1986; Hardman et ai., 1987; Kovach and Tette,
1988; Agnello et al., 1994). However, costs associ-
ated with engaging in second-level IPM may exceed
those of first-level IPM and be a disincentive to
grower adoption of second-level IPM. For example,
in this study, the expenses of biologically based
46 R.J. Prokopy et al./ Agriculture, Ecosystem and Environment 57 (1996) 35-47
methods for controlling fruit-damaging insects active
after mid-June, coupled with losses of revenue result-
ing from greater damage to fruit by insects con-
trolled in this manner, resulted in about $US 260
ha- I lower net profit for second-level than first-level
IPM blocks (Acquaye et al., 1996). Hopefully, sub-
stitution of pesticide-treated spheres (Duan and
Prokopy, 1995) for sticky spheres to control apple
maggot (and consequent substantial savings in cost
of labor to employ spheres) could negate much of
the current economic disadvantage of second-level
IPM practices. As discussed by McDonald and Glynn
(1994), economic considerations actually may turn
out to be less of a concern in apple grower adoption
of second- or third-level IPM practices than other
factors. These authors suggest that in northeastern
North America, apple growers might be motivated to
adopt more advanced IPM practices largely out of
environmental concerns and associated social and
psychological rewards. The authors concur with this
assessment.
Acknowledgements
This work was sponsored by the Massachusetts
Society for Promoting Agriculture, the Northeast
Regional USDA Competitive IPM Grants Program,
State/Federal IPM funds, and the Northeast Re-
gional Sustainable Agriculture Research and Educa-
tional Program. Thanks are extended to Roy Van
Driesche for examining leafminers for evidence of
parasitism and identification of parasitoids to species
and Xingping Hu for identifying mite predators to
species.
References
Acquaye, A.K., Moffitt, J., Allen, P.G. and Prokopy, R.J., 1996.
First-level, transitional and second-level IPM budgets for
Mclntosh and other cultivars. Mass. Fruit Notes (in press).
Agnello, A.M., 1992. Status of obliquebanded leafroller
pheromone disruption trials. Proc. N. Engl. Fruit Meet., 98:
78-88.
Agnello, A.M., Kovach, J., Nyrop, J.P., Reissig, W.H., Breth, D.I.
and Wilcox, W.F., 1994. Extension and evaluation of a simpli-
fied monitoring program in New York apples. Am. Entomol.,
40: 37-49.
Baynon, G.T. and Penman, D.R., 1987. The effects of mancozeb
and metiram on the predatory mite Typhlodromus pyri. Proc.
N.Z. Weed Pest Control Conf., 1: 104-107.
Blommers, L.H.M., 1994. Integrated pest management in Euro-
pean apple orchards. Annu. Rev. Entomol., 39: 213-241.
Bostanian, N.J. and Coulombe, L.J., 1986. An integrated pest
management program for apple orchards in southwestern Que-
bec. Can. Entomol., 118: 1131-1142.
Bower, C.C., Penrose, L.J. and Dodds, K., 1993. A practical
approach to pesticide reduction on apple crops using super-
vised pest and disease control - preliminary results and prob-
lems. Plant Prot. Q., 8: 57-62.
Caprile, J., Klonsky, K., Mills, N., McDougall, S., Micke, W. and
van Steenwyk, R., 1994. Insect damage limits yield, profits of
organic apples. Calif. Agric., 48(6): 21-28.
Chapman, P.J. and Lienk, S.E., 1971. Tortricid fauna of apple.
N.Y. State Agric. Exp. Sta. Special Publ., 122 pp.
Clemens, D.R. and Harmsen, R., 1992. Stigmaeid-phytoseiid
interactions and the impact of natural enemy complexes on
plant-inhabiting mites. Exp. Appl. Acarol., 14: 327-341.
Cooley, D.R., Prokopy, R.J., Mason, J. and Wright, S., 1995.
Effects of pesticides on pest ecology in blocks of scab-re-
sistant cultivars. Mass. Fruit Notes, 60 (1): 16-19.
Corbet, P.S., 1981. Non-entomological impediments to the adop-
tion of integrated pest management. Prot. Ecol., 3: 183-202.
Croft, B.A., 1990. Arthropod Biological Control Agents and
Pesticides. Wiley and Sons, New York.
Croft, B.A., 1994. Biological control of apple mites by a phyto-
seiid mite complex and Zetzellia mali: long-term effects and
impact of azinphosmethyl on colonization by Amblyseius an-
dersoni. Environ. Entomol., 23:1317-1325.
Cross, J.V., 1996. The current status of integrated pome fruit
production in western Europe and its achievements. Pro=. Int.
Conf. Integrated Fruit Prod., 1995, Cedzyna, Poland, (in press).
Day, M.L. and Hogmire, H.W., 1993. Seasonal occurrence and
control of rose leafhopper on apples in West Virginia. Moun-
taineer Grower, 519: 22-26.
Dickler, E. and Schafermeyer, S., 1990. General principles, guide-
lines and standards for integrated production of pome fruit in
Europe. IOBC/WPRS Bull., 14(3): 1-67.
Dover, M.J., 1985. A better mousetrap: improving pest manage-
ment for agriculture. Study 4. World Resources Institute,
Washington, D.C., 80 pp.
Duan, J.J. and Prokopy, R.J., 1995. Control of apple maggot flies
with pesticide-treated red spheres. J. Econ. Entomol., 88:
700-707.
Frisbie, R.E. and Smith, J.W., 1991. Biologically intensive inte-
grated pest management: the future. In: J.J. Menn and A.L.
Steinhauer (Editors), Progress and Perspectives in the 21st
Century. Entomological Society of America, Lanham, MD,
pp. 151-164.
Hagley, E.A.C. and Biggs, A.R., 1989. Effects of three fungicides
on populations of a phytophagous and several predaceous
mites on apple. Exp. Appl. Acarol., 6: 253-256.
Hardman, J.M., Rogers, R.E.L. and Maclellan, C.R., 1987. Pesti-
cide use and levels of insect and scab injury on fruit in Nova
Scotia apple orchards. J. Econ. Entomol., 80: 979-984.
 R.J. Prokopy et al./ Agriculture, Ecosystem and Environment 57 (1996) 35-47
Hardman, J.M., Floyd, R. and Bent, E., 1995. Effects of different
integrated pest management programs on biological control of
mites on apples by predatory mites in Nova Scotia. Environ.
Entomol., 24: 125-142.
Howell, J.F., Knight, A.I., Unruh, T.R., Brown, D.F., Krysan,
J.L, Sell, C.R. and Kirsch, P.A., 1992. Control of codling
moth in apple and pear with sex pheromone-mediated mating
disruption. J. Econ. Entomol., 85: 918-925.
Hu, X.P., Prokopy, R.J. and Mason, J., 1995. Populations of
predatory and pest mites in first- level and second-level com-
mercial apple orchard blocks in Massachusetts. J. Appl. Ento-
mol., (in press).
Hull, L.A., Hickey, K.D. and Kanour, W.W., 1983. Pesticide use
patterns and associated pest damage in commercial apple
orchards of Pennsylvania. J. Econ. Entomol., 76: 577-583.
loriatti, C., Pasqualini, E. and Toniolli, A., 1992. Effects of
fungicides mancozeb and dithianon or mortality and reproduc-
tion of the predatory mite Amblyseius andersoni. Exp. Appl.
Acarol., 15: 109-116.
Knight, A., 1995. Evaluating the impact on apple pest manage-
ment of adopting mating disruption for codling moth in Yakima
Valley, Washington. J.B.C. Soc. Entomol., (in press).
Kovach, J. and Tette, J.P., 1988. A survey of the use of IPM by
New York apple producers. Agric. Ecosystems Environ., 20:
101-108.
Maier, C.T., 1994. Biology and impact of parasitoids of Phyllono-
rycter blancardella and P. crataegella in northeastern North
American apple orchards. In: C.T. Maier (Editor), Integrated
Management of Tentiform Leafminers in North American
Apple Orchards. Thomas Say Public. Entomol. Soc. Am.,
Lanham, MD, pp. 6-24.
McDonald, D.G. and Glynn, C.J., 1994. Difficulties in measuring
adoption of apple IPM: a case study. Agric, Ecosystems
Environ., 48: 219-230.
Miller, A., 1983. Integrated pest management: psychological con-
straints. Prot. Ecol., 5: 253-268.
Nyrop, J.P., 1993. Biological control of European red mites in
apple orchards. N.Y. Fruit Q., 1: 13-15.
Nyrop, J.P., Minns, J.C. and Herring, C.P., 1994. Influence of
ground cover on dynamics of Amblyseius fallacis Garman in
New York apple orchards. Agile. Ecosystems Environ., 50:
61-72.
Oberhofer, H., 1991. Integrated fruit production in South Tyrol.
Proc. N.Y. State Hort. Soc., 136: 53-62.
Pfeiffer, D.G. and Killian, J.C., 1988. Disruption of olfactory
communication in oriental fruit moth and lesser appleworm in
a Virginia peach orchard. J. Agric. Entomol., 5: 235-239.
Pfeiffer, D.G., Kaakeh, W., Killian, J.C., Laehance, M.W. and
Kirsch, P., 1993. Mating disruption to control damage by
leafrollers in Virginia apple orchards. Entomol. Exp. Appl.,
67: 47-56.
Pree, D.J., Marshall, D.B., Whitty, K.J. and Archibald, D.E.,
1994. Management of insecticide resistance in Phyllonorycter
spp. and effects on their parasitoids. In: C.T. Maier (Editor),
Integrated Management of Tentiform Leafminers in North
47
American Apple Orchards. Thomas Say Public. Entomol. Soc.
Am., Lanham, MD, pp. 52-66.
Prokopy, R.J., 1993. Stepwise progress toward IPM and sustain-
able agriculture. IPM Pract., 15(3): 1-4.
Prokopy, R.J., 1994. Integration in orchard pest and habitat man-
agement: a review. Agric. Ecosystems Environ., 50: 1-10.
Prokopy, R.J. and Croft, B.A., 1994. Apple insect management.
In: R.L. Metcalf and W.H. Luckmann (Editors), Introduction
to Insect Pest Management. 3rd edn., Wiley and Sons, New
York, pp. 543-585.
Prokopy, RJ., Coli, W.M., Hislop, R.G. and Hauschild, K.I.,
1980. Integrated management of insect and mite pests in
commercial apple orchards in Massachusetts. J. Econ. Ento-
mol., 73: 529-535.
Prokopy, R.J., Johnson, S.A. and O'Brien, M.T., 1990. Second-
stage integrated management of apple arthropod pests. Ento-
mol. Exp. Appl., 54: 9-19.
Prokopy, R.J., Leahy, K. and Coli, W.M., 199l. Thirteenth An-
nual March Message to Tree Fruit Growers Cooperative Ex-
tension, Univ. Mass., Amherst, (unpublished).
Prokopy, R.J., Cooley, D.R., Autio, W.R. and Coli, W.M., 1994.
Second-level integrated pest management in commercial apple
orchards. Am. J. Alt. Agric., 9: 148-156.
Prokopy, R.J., Mason, J. and Wright, S., 1995. Second-level IPM
for arthropods in apple orchards: performance according to
type of cultivar. Mass. Fruit Notes, 60(3): 11-13.
Rajotte, E.G., 1993. From profitability to food safety and the
environment: shifting the objectives of IPM. Plant Dis., 77:
296-299.
Santos, M.A., 1976. Evaluation of Zetzellia mali as a predator of
Panonychus ulmi and Aculus schlechtendali. Environ. Ento-
mol., 5: 187-191.
Straub, R.W. and Jentsch, P.J., 1994. Relationship of the white
apple leafhopper, Typhlocyba pomaria, and the rose leafhop-
per, Edwardsiana rosae, on apple in the Hudson Valley region
of New York. J. Agric. Entomol., 11: 301-309.
Trumble, J.J. and Alvarado-Rodriguez, B., t993. Development
and economic evaluation of an IPM program for fresh market
tomato production in Mexico. Agric. Ecosystems Environ., 43:
267-284.
van der Geest, L.P.S. and Evenhuis, H.H., 1991. Tortricid Pests:
Their Biology, Natural Enemies and Control. Elsevier, Ams-
terdam.
Van Driesche, R.G., Prokopy, R.J. and Christie, M., 1994. Effect
of second-stage IPM practices on parasitism of apple blotch
leafminer larvae in Massachusetts apple orchards. Environ.
Entomol., 23: 140-146.
Vossen, P., Jolly, D., Myer, R., Varela, L. and Blodgett, S., 1994.
Disease, insect pressures make organic production risky in
Sonoma County. Calif. Agric., 48(6): 29-36.
Wearing, C.H., 1988. Evaluating the IPM implementation process.
Annu. Rev. Entomol., 33: 17-38.
Zalom, F.G., 1993. Reorganizing to facilitate the development and
use of integrated pest management. Agric. Ecosystems Envi-
ron., 46: 245-256.