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This is to certify that the

thesis entitled

Parasitoid Phenology, Ovicides, And Damage-
Yield Relationships Of The Spotted Tentiform
Leafminer (Lepidoptera: Gracillariidae) on
Apples

presented‘by

John Patrick Hayden

has been accepted towards fulfillment
of the requirements for

M.S. _ Entomology
degreein

 

 

’\ move 9 . \ W36,

Major professor

 

Date November 13, 1985

0-7639 MS U is an Aflimative Action/Equal Opportunity Institution

 

 

MSU

LIBRARIES
M

\—

RETURNING MATERIALS:

 

 

 

 

Place in book drop to
remove this checkout from
your record. FINES will
be charged if book is
returned after the date
stamped below.

 

’va 3 my

 

 

PARASITOID PHENOLOGY, OVICIDES, AND DAMAGE-YIELD
RELATIONSHIPS OF THE SPOTTED TENTIFORM LEAFMINER
(LEPIDOPTERA: GRACILLARIIDAE) ON APPLES

By
John Patrick Hayden

A THESIS

Submitted to
Michigan State University
in partial fulfillment of the requirements
for the degree of

MASTER OF SCIENCE

Department of Entomology

1985

ABSTRACT

PARASITOID PHENOLOGY, OVICIDES, AND DAMAGE-YIELD
RELATIONSHIPS OF THE SPOTTED TENTIFORM LEAFMINER,
(LEPODOPTERA: GRACILLARIIDAE) 0N APPLES

By
John Patrick Hayden

A study of the seasonal occurrence of the spotted

tentiform 1eafminer (STLM) Phyllonorycter blancardella (F.),

 

and its parasitoids was carried out in an unsprayed orchard
in Michigan. There were seven parasitoid species recovered.
Peak STLM adult emergence occurs before peak emergence of the

braconid, Pholetesor ornigis, in all three generations.

 

In laboratory experiments testing ovicidal activity,
fenvalerate, permethrin and methomyl were successful. In
field applications, fenvalerate and diflubenzuron were effec-
tive ovicides (100.0 and 70.7% mortality, respectively).

In a study using punched holes to simulate leaf mines,
no significant differences in apple weight gain were found be-
tween 0, 15 and 30% defoliation on 'Red Delicious' fruiting
spurs in 1983. In 1984, girdled 'Golden Delicious' branches
with 10:1, 15:1, and 20:1 1eaf:fruit ratios were subjected
to different levels of simulated damage with up to three second
and five third generation simulated mines/leaf. The effect
of 1eaf:fruit ratio on weight gain was highly significant,
but the effect of different simulated infestation levels was

not significant.

ACKNOWLEDGMENTS

sincerest thanks to my major professor Gus Howitt and
to committee members, George Ayers, Jim Flore, and Fred Stehr
for their guidance and encouragement. Thanks also to the
staff of M.S.U. Trevor Nichols Experiment Station, especially
my wife Nancy, for technical and moral support.

I gratefully acknowledge the Crane family, Robert Osman,
and Andy Jager as grower cooperators; as well as the financial

assistance of the Michigan Apple Committee.

ii

TABLE OF CONTENTS

page
LIST OF TABLES........................................iv
LIST OF FIGURES....................................... V
INTRODUCTION.......................................... 1

I. SEASONAL OCCURRENCE OF THE SPOTTED TENTIFORM
LEAFMINER (LEPIDOPTERA: GRACILLARIIDAE) AND
ITS MAJOR PARASITOIDS IN MICHIGAN.

ABSTRACT.................................... 4
INTRODUCTION................................ 6
MATERIALS AND METHODS....................... 9
RESULTS.....................................12
DISCUSSION..................................24
REFERENCES..................................26

II. OVICIDAL ACTIVITY OF INSECTICIDES ON THE
SPOTTED TENTIFORM LEAFMINER (LEPIDOPTERA:
GRACILLARIIDAE).

ABSTRACT....................................28
INTRODUCTION................................29
MATERIALS AND METHODS.......................31
RESULTS AND DISCUSSION......................35
REFERENCES..................................40

III. THE EFFECT OF SIMULATED SPOTTED TENTIFORM
LEAFMINER (LEPIDOPTERA: GRACILLARIIDAE)
DAMAGE, AFTER FRUIT SET, ON APPLE SIZING.

ABSTRACT....................................42
INTRODUCTION................................44
MATERIALS AND METHODS.......................47
RESULTS.....................................51
DISCUSSION..................................64
REFERENCES......... ........ .................67

CONCLUSIONOOOOOCOC ..... 00...... ........ O ........ 0.....69

LIST OF REFERENCES............ ........... .. ..... ......72

iii

Table

Table

Table

Table

Table

Table

Table

Table

Table

Table

Table

10.

11.

LIST OF TABLES

Parasitoid and hyperparasitoid species
recovered from STLM mines in Southwest
Michigan, 1983-1984.. ......... .... ........

Contents reared from 100 cohort mines/
generation from an unsprayed orchard,
1983-1984.00.00.0000000 .......... O ........

Average number of mines/leaf for each
generation in an unsprayed orchard
during 1983-1984 oooooo ooooo ooooooooooooooo

Laboratory evaluation of ovididal
activity of several insecticides on
spotted tentiform leafminer ...............

Ovicidal activity of field applications
of selected insecticides on spotted
tentiform leafminer ............ . ..........

Effects of girdling and defoliation
of spurs on apple weight gain, 1983 .......

Interactive effects of crop load and
simulated leafminer damage on change
in apple weight (grams) from 7/16 to 8/27.

Interactive effects of crop load and
simulated leafminer damage on change
in apple weight (grams) from 7/16 to 9/23.

Mean squares showing the effects of
1eaf:fruit ratio and different infestation
levels on apple weight gain ........ . ..... .

Defoliation level effects on apple weight
gain (averaged across 1eaf:fruit ratios)..

Leaf:fruit ratio effects on apple weight
gain (averaged across defoliation levels).

iv

..... l7

..... 18

..... 18

..... 36

.....37

..... 53

..... 57

..... 58

..... 59

..... 60

..... 61

Figure

Figure

Figure

Figure

Figure

Figure

Figure

Figure

Figure

Figure

Figure

Figure

10.

ll.

12.

LIST OF FIGURES

Seasonal occurrence of STLM and parasitoid
life stages within the leaf mines, 1983-l984...l3

Average weekly pheromone trap counts, 1983
and 1984......0..0.IOOOOOOOOOOOOOOOOOOOOOOO0.0.14

Seasonal occurrence of g. ornigis life
stages within the mine ...... ...................15

Seasonal occurrence of S, marylandensis
life Stages Within the mineOOOOOOOOOOOOI0.0.00016

 

Spring brood emergence of STLM and major
parasitoids from emergence trap......... ..... ..21

First generation emergence of STLM and
major parasitoids from emergence trap..........22

Second generation emergence of STLM and
major parasitoids from tagged mines on

treeSDO..OOOOOOOOOOOOOOIO00.000.000.0000000000023

Prediction equations for apple weight
based on surface area. 1983 -
'Red Delicious'........................ ........ 52

Effect of leaf area per fruit on weight
gain. Treatment to 8/16/83....................54

Effect of leaf area per fruit on weight
gain. Treatment to harvest (9/24/83)..........55

Prediction equations for apple weight
based on surface area. 1984 -
'GOIden DeliCiouSIOOOOOOOO00.0.0000...000......62

Effect of leaf area per fruit on weight
gain.'Golden Delicious' 1984... .............. ..63

INTRODUCTION

From an ecological point of view, the monocultures
of modern agriculture are highly artificial. Their lack
of diversity make pest outbreaks an inherent problem.
Several general strategies have been used to protect crops
from insects. The most important of these are chemical,
biological and cultural control methods. In the past, and
still to a large extent, chemical control of insects using
broad spectrum insecticides is popular because of its ease,
relative low cost, and short term effectiveness (Luckman
and Metcalf 1975).

Traditionally, regular preventive pesticide applica-
tions, whether the pest is present or not, have been the
mainstay of apple pest management programs. This is because
apples have a low tolerance for damage due to high consumer
appeal and expectations (Croft 1975). Heavy reliance on
chemical control, however, has resulted in long term problems.
Among these are resistance (Hough 1963), destruction of bene-
ficial species resulting in secondary pest outbreaks
(Huffaker et a1. 1969), and environmental contamination
(Luckman and Metcalf 1975).

Integrated Pest Management (IPM) is a concept that

has gained popularity recently (Hoyt and Burts 1974). IPM

emphasizes the use of biological and cultural pest manage-
ment strategies in conjunction with chemical strategies,

to maintain pests below economic injury levels. The main
goal of IPM is to optimize the economic gain of the grower
while minimizing the unfavorable consequences of broad spec-
trum insecticide use.

Three of the prerequisites to the successful
development of an IPM program are an understanding of: the
organisms and their interactions; how inputs will affect
the agro-ecosystem; and damage-yield relationships necessary
to set economic injury thresholds.

The following thesis is a set of three papers that
are aimed at increasing understanding of the spotted tenti-
form leafminer (STLM) problem on apples and improving manage-
ment strategies.

The first paper deals with the phenology of the pest
and its parasitoids, and the impact of parasitoids on a
population in an unsprayed system. The goal of this research
was to study the interactions of the organisms throughout
the season and to formulate hypotheses relative to the effect
of timing and selection of chemical treatments.

The second paper investigates the ovicidal pr0per-
ties of certain insecticides and discusses the possibility
of a new management strategy that could decrease the number
of insecticide sprays used to control STLM, as well as

decrease their impact on beneficial species in the orchard.

The third paper investigates the damage-yield
relationships of second and third generation infestations.
To achieve various levels of infestation, artificial de-
foliation was carried out using a hole punch to simulate
leaf mines. Localized effects were studied by girdling
specific parts of the trees. This type of study has impli-
cations for setting economic thresholds for foliage feeding
insects.

While this research deals with specific aspects of
a specific pest in the apple system, and represents only
small portion of the apple ecosystem, these are the type
of basic studies that need to be done when laying the ground-

work for a total IPM program for apples.

I. SEASONAL OCCURRENCE OF THE SPOTTED TENTIFORM
LEAFMINER (LEPIDOPTERA: GRACILLARIIDAE) AND
ITS MAJOR PARASITOIDS IN MICHIGAN.

ABSTRACT

The seasonal development of the spotted tentiform

leafminer (STLM), Phyllonorycter blancardella (F.) and its

 

major parasitoids were studied in an unsprayed orchard in
Michigan during 1983 and 1984. Mines from weekly leaf
samples were dissected to observe parasitoid development.

The contents of 100 cohort mines from each generation were
reared to determine percent parasitism and composition of

the parasitoid complex. STLM has three distinct generations
in Michigan. Parasitoid development begins with the 'tissue-
feeding' stage of each generation. Of the parasitoids

successfully reared, 57% were Sympiesis marylandensis Girault,

 

37% were Pholetesor ornigis (weed), 3% were Sympiesis

 

 

sericeicornis (Nees) and 2% were Sympiesis bimaculatipennis

 

 

(Girault). Pnigalio maculipes (Crawford), Horismenus

 

 

fraternus (Fitch) and a Hypopteromalus sp. were also recovered

 

 

from STLM mines. Parasitism within generations ranged from
30 to 65%. STLM populations were kept well below action
threshold levels by natural mortality factors over the 2 year
study period.

Studies using adult emergence traps and tagged mines
show that for all three generations peak STLM emergence occurs

before peak P. ornigis emergence (20, 7, and 4 days)

for spring brood, first generation and second generation
emergence, respectively). P. ornigis is a larval parasitoid
whose emergence is synchronized with the development of STLM
larvae. These occurrences could be exploited by correctly

timed short residual sprays targeted at STLM adults and eggs.

INTRODUCTION

The spotted tentiform leafminer (STLM),

Phyllonorycter blancardella (F.) has become a sporadic, yet

 

important pest in Michigan apple orchards (Dutcher and
Howitt 1978). It was first reported in Michigan by Hutson
(1938). Damage to the leaves is caused by the mining of the
larval stages. This feeding reduces chlorophyll content and
the photosynthetic rate of the leaves (Proctor et al. 1982).
Heavy infestations can lead to early leaf abscission (Maeir
1983), a reduction in terminal growth, fruit growth stunting,
premature ripening and fruit drop, and a reduction of fruit
set the year following infestation (Kremer 1963, Pottinger
and LeRoux 1971, Reissig et al. 1982).

STLM has three generations per year in Michigan.
The third-generation overwinters as pupae in the leaf litter.
In April, the spring brood of adults emerges and lays eggs
on the underside of the unfolding leaves. There are five
larval instars (Pottinger and LeRoux 1971). The first three
are passed as sap-feeding larvae, which are dorso-ventrally
compressed and feed by shearing cells and ingesting the cell
contents. After the third instar, larvae undergo a hyper-
metamorphosis, becoming more cylindrical and developing thor—

acic legs and prolegs. Their feeding habit changes to chewing

6

out irregular patches of mesophyll cells on the upper in-
side surface of the mine. Silken threads are spun and
attached to both sides of the mine. As these threads dry
they cause an arching of the mine that results in a tenti-
form appearance (Pottinger and LeRoux 1971).

STLM has a rich parasitoid complex that is usually

dominated by the braconid Pholetesor ornigis (Weed) and/or

 

the eulophid Sympiesis marylandensis Girault (Pottinger and

 

LeRoux 1971, Maier 1984). Species previously found in
Michigan by Dutcher and Howitt (1978) are P. ornigis,
S. marylandensis, Sympiesis sericeicornis (Nees) (=Sympiesis

 

 

 

conica (Provancher)), and the eulophid Pnigalio flavipes

(Girault).

 

Parasitoids are more prevalent and play a more
important role in regulating populations of leafminers in
unsprayed orchards than in sprayed orchards (Pottinger and
LeRoux 1971, Johnson et a1. 1976, Van Driesch 1983, Meier
1984). Their ineffectiveness in controlling STLM populations
in some commercial orchards may be due to the timing of
insecticide applications (during parasitoid emergence and
oviposition periods) (Maier 1984), or differences in suscept-
ibility of parasitoids and adult STLM to certain cover
sprays (Weires 1977, Dutcher and Howitt 1978, Free et a1.
1980, Hagley et a1. 1981).

The purpose of this research is to further explore

the relationships between STLM and its parasitoids in Michigan,

and to look for possible means of enhancing the effective-
ness of the natural enemies by selective timing of insecti-

cide applications or other conservation methods.

MATERIALS AND METHODS

The seasonal development of leafminers and parasi-
toids was monitored in an unsprayed apple orchard near
Fennville, MI that was taken out of production in 1982. Leaf
samples were taken from April to October in 1983 and 1984.

In 1983, six leaves from heights of 1.5 m.and 2.5 m at each of
the four compass points (N, E, S, W), for a total of 48 leaves
per tree, were sampled weekly from.each of 16 'Red Delicious'
trees. In 1984, leaves were sampled by pruning 10 clusters
from each of five apple trees every seven days. The sampling
procedure was changed from 1983 to 1984 to increase the sample
size (number of leaves) and to better correlate data with
other research that uses the cluster as the basic sampling
unit (Pottinger and LeRoux 1971, Dutcher and Howitt 1978,
Johnson et a1. 1976, Maier 1984). Samples were stored in a
refrigerator at 4°C in sealed plastic bags, for up to seven
days, until they were processed. Each leaf was examined
under a dissecting microscope for all life stages of STLM.
Mines were opened to search for parasitoid eggs, larvae or
pupae. STLM 'tissue-feeding' larvae were dissected in a
droplet of water against a black background to determine the
presence of endoparasitoids.

To determine the species composition of the parasitoid

complex, as well as percent parasitism, 100 mines were

10

collected from each generation during 1983 and 1984, when
STLM pupae were first observed. The mines were excised from
the leaves and placed in groups of five in disposable plastic
petri dishes with moistened filter paper and a Parafilm seal.
They were held for 14-21 days at 21-27°C and natural photo-
period to encourage emergence. Emerged specimens were
collected and all mines were opened to match emerged adults
with the mine contents. This was done to account for dead
specimens that had not emerged and to become familiar with
the characteristic pupal exuviae, cocoons (in the case of P.
ornigis), meconia, frass and emergence holes of each species.
Emergence of STLM and parasitoid adults from the
overwintering 3rd generation and first generation was moni-
tored by the use of emergence traps in a commercial orchard
near Fennville, MI and in a commercial orchard near Pullman, MI,
respectively in 1984. The pyramidal traps were .3 m high with
.24 m2 open bases, supported by a wooden frame and covered
with nylon netting. The traps were placed over piles of in-
fested leaves on the orchard floor and were checked every
2-3 days. Traps were covered during pesticide application.
Emerged specimens were aspirated through an opening in the
side of the trap. The emergence of second generation adult
STLM and parasitoids was monitored in the unsprayed orchard
near Fennville, MI, by tagging and observing mines. On July
25, 250 late sap-feeding or early tissue-feeding mines that

appeared not to have been preyed upon (l/leaf) were tagged.

11

At 2-3 day intervals each mine was examined for evidence of
emergence (protruding STLM pupal cases, or circular parasi-
toid emergence holes), or predation (host feeding by parasi-
toids as described by van Driesche and Taub (1983)). Mines
that showed evidence of emergence or predation were brought
back to the lab and opened under a dissecting microscope.
Previous inhabitants were determined by their pupal exuviae,
cocoons, frass, meconia, or cadavers (in the case of preda-
tion). STLM adult emergence was also monitored by weekly

pheromone trap counts in the unsprayed orchard in 1983 and 1984.

RESULTS

The three generations of STLM in Michigan were clearly
represented by three distinct peaks of abundance for each
life stage on the leaf (Figure 1) and by the three distinct
peaks of pheromone trap catches (Figure 2), during 1983 and
1984. The impact of the major parasitoids, as seen by the
peaks of abundance for their life stages within the mine,
(Figure 1), coincides with the appearance of 'tissue-feeding'
mines over the three STLM generations. Parasitism of 'sap-
feeders' was extremely rare. When parasitoid development by
life stages within the mine is examined (Figures 3 and 4), the
three generations that develop on the leafminer host become
more distinct.

0f the species recovered from STLM mines (Table l),

Pholetesor ornigis, S, marylandensis and Pnigalio maculipes

 

 

 

(Crawford), were observed as primary parasitoids of STLM.

Sympiesis sericeicornis and S. bimaculatipgnnis (Girault)

 

 

were observed to be parasitoids of STLM or hyperparasitoids

on P. ornigis. Horismenus fraternus (Fitchjand a Hypoptero-

 

 

malus g2, were observed only as hyperparasitoids on P. ornigis.
Maier (1984) reported H. fraternus to parasitize STLM as well

 

as P. ornigis and a Sympiesis g2. As far as the author knows,

 

S. bimaculatipennis, P, maculipes and H. fraternus are new

 

 

 

records for Michigan.

12

Percent of Total Live Mines

l3

 
 
  

&-—a 1983

o—-—0 1984

 

 

100'

50«

 

 

100~
q Pupae

50-4

 

 

 

PARASITOIDS
100~
- Pholetesor ornigi_s_
50* ‘
0 Air-1 Y*~“‘A __v v -‘ ‘l/
100- . . . . .
§yflpte5Is marylandensus (8 other ectoparasntouds)
1 /\\
504 . r’ \
I \\
-< [I \‘ «\
’bs‘ AA
- I. f,

 

 

O V Y Y jfi‘fiY Y1 Y I T T 1' 7i Y Y 1 Vi] ; T V

MGY 16 June 20 July 25 August 30 Oct. 3

Sampling Date

Figure 1: Seasonal occurrence of STLM and parasitoid
life stages within the leaf mines, 1983-1984.

Number of males captured

3000}

ZSOOT

2000‘

1500‘

1000-

500‘

 

14

.—-—--o 1983
o———o1984

 

 

 

 

 

 

I I I I l
4/18 5/2‘ 5/16 5/30 6/13 6727 7/11 7/25 8/8 3122 9/6 9119 10/3 10/17
DATE

Figure 2: Average weekly pheromone trap counts, 1983

and 1984.

Number observed per weekly leaf sample

20.4

10—

 

15

Larvae

 

1984 ----- Cocoons

 

 

501

40-

30‘

20"1

10"

 

O

1983

 

 

\

 

 

4/118 I 5/116]

    

l L I | I
6/131 7/11 8/8 I 9/6 I 10/3
5/2 5/30 6/27 7/25 8/22 9119 10117

Date

Figure 3: Seasonal Occurrence of E.- ornigis

life stages within the mine.

Number observed in weekly leaf sample

16

 

 

.............. Eggs
Larvae

_-_.._ Pupae

15 q 1984

10~

5 .1

0-1

I 1 W I

 

10"

 

 

0-1

T I 7 I fl I I 7 I _

4/18 | 5/16 [ 6/13 I 7/11 I BIBT 9/6 110/3 l

5/2 5/30 6/27 7/25 8’22 9/19 10/17
Date

 

 

Figure 4: Seasonal occurences of §_;_ marylandensls
life stages within the mine.

 

17

Table l: Parasitoid and hyperparasitoid species recovered from STLM mines in
Southwest Michigan, 1983-1984.

 

Pholetesor ornigis (W cod)
Sxmnicsis mamlandsnsis Girault

S . . . . . (Nees)
Sympiesis bimaculatipennis, (Girault)
Enigalio mm (Crawford)
Horismenus fmtsmns (Fitch)
W .12.

 

18

Table 2: Contents reared from 100 cohort mines/generation from an unsprayed orchard,

 

 

 

 

1983-1984.
1983 1984
Genl Gen2 Gen3b Genl Gen2 Gen3a
STLM 4 8 50 32 8 54
Parasitoids
2.9mm. 7 6 24 31 16 27

S. W 48 39 8 22 49 3

Hyperparasitoids
S. sericeicornis l l 0 0 5 3
SW 2 o o 1 4 0
other 1 0 0 0 1 3

Mortality other than

apparent parasitism 37 46 18 14 17 10

 

aOverwintering generation mines collected from leaf litter in November 1983 and 1984
bSamples partially destroyed by fungi (numbers are estimates from remains).

Table 3: Average number of mines/leaf for each generation in an unsprayed orchard
during 1983-1984.

 

1983 1984

 

 

Gen 1 Gen 2 Gen 3 Gen 1 Gen 2 Gen 3

 

.07 .27 .51 .05 .10 .30

 

19

Of the parasitoids successfully reared out in 1983

and 1984, 57% were S, marylandensis, 37% were S. ornigis,

 

3% were S. sericeicornis, and 2% were S, bimaculatipennis.

 

 

Total percent parasitism (measured by successfully reared
parasitoids)on a generational basis ranged from 30 - 65%,
with an average of 47%. Mortality by causes other than
successful parasitism (host feeding, predation, disease, etc.)
ranged from 10 - 46%, with an average of 25% (Table 2). In
both years the second generation had the highest percent
mortality, and the third generation had the largest numbers
of successful adult STLM. Overwintering third generations
were collected and reared in the fall and do not reflect over-
wintering mortality.

2. ornigis were the more abundant parasitoids of STLM
'tissue-feeders' in the first and third leafminer generations

except for the first generation in 1983, while S, marylandensis

 

were more abundant in the second generation (Table 2). This
is consistent with Dutcher and Howitt's (1978) work and.with
reports from.Massachusets (Van Driesche and Taub 1983) and
Connecticut (Maier 1984).

Throughout the six generations that were studied over
this two year period, STLM populations were always kept low
by parasitism and other natural mortality factors. In both
years there was an increase in density (measured by
mines/leaf) from the first generation to the third generation
(Table 3), but they never approached the recommended action

thresholds of one mine/leaf for first generation or two

20

mines/leaf for second generation (Weires 1981, Reissig et al.
1982).

The results from the adult emergence studies showed
that for all three generations studied in 1984, peak adult
STLM emergence occurred earlier than peak emergence for
either parasitoid species (Figures 5, 6, and 7). The time
differences were the greatest for spring brood emergence (20
days between peak STLM and peak S. ornigis emergence), and
the smallest for second generation emergence (4 days between
peak STLM and peak S. ornigis emergence). S. ornigis
emergence is more synchronous with the occurrence of 'tissue-

feeding' hosts than is S. marylandensis emergence. The peak

 

emergence trap catches of STLM match up well with peak

pheromone trap catches for the same generations.

21

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DISCUSSION

In an unsprayed orchard, S. ornigis and S. marylandensis

 

were major causes of STLM mortality. S. marylandensis not

 

only parasitizes 'tissue-feeders' but also feeds on them with-
out ovipositing (Van Driesche and Taub 1983). The impact of
this action on the pest population is often lumped together
with other mortality factors. The two species act compli-
mentarily over the season on STLM populations. The first

and third generations are usually dominated by S. ornigis
while the second generation is usually dominated by S.

marylandensis. Any modification of management practices

 

designed to conserve these beneficial insects could help to
alleviate the STLM problem.

Johnson et a1. (1976) discuss the existence of a
"biological window", or a time during the life cycle of the
pest where application of a control measure will not affect
the natural enemies. They showed a 20 day gap between spring
emergence of STLM adults and emergence of S. ornigis. The
data confirms the existence of this window during spring
emergence for both parasitoid species. Shorter biological
windows also seem to be present between peak STLM and peak
S. ornigis in both first and second generation emergence.

These occurrences could be exploited by using a relatively

24

25

short residual spray that has adulticidal and ovicidal acti-
vities (see chapter 2). The problem.with implementing this
as a management strategy for spring brood emergence is that

a petal fall spray would take place during the critical
period after parasitoid emergence but before oviposition and
would most likely be deleterious to the STLM parasitoids.

The petal fall spray is considered one of the most critical
and necessary sprays of the season by many growers. Other
possible means of conserving parasitoid populations could

be the use of chemicals less toxic to the parasitoids, reduced
dosages, or less complete coverage by spraying alternate rows
(Van Driesche and Taub 1983).

When making management decisions concerning STLM that
are based on action thresholds of numbers of mines/leaf,
parasitism rates should be taken into account. Pest managers
need to be trained to recognize the parasitoids of STLM and
their symptoms. Ideally, we should be able to predict the
impact that the next generation of parasitoids will have on
STLM populations, based on the present parasitoid generation
numbers. Until we reach that point, however, action thres-

holds should be based on number of unparasitized mines/leaf.

REFERENCES

Coli, W.M. and R.J. Prokopy, 1982. Biology, monitoring and
control of leafminers in Massachusetts, 88th Ann.
Meeting Mass. Fruit Growers Assoc., Inc., Proc. 88:
30‘440

Dutcher, J.D. and A.J. Howitt. 1978. Bionomics and control
of Lithocolletis blancardella in Michigan. J. Econ.
EntomoI. 7I:736-738.

Hagley, E.A.C. 1985. Parasites recovered from the overwinter-

. ing generation of the spotted tentiform leafminer,
Phyllonorycter blancardella (Lepidoptera: Gracillariidae)
in pest-management apple orchards in southern Ontario.
Can Ent 117: 371-374.

 

Hagley, E.A.C., D.J. Free and C.M. Simpson. 1981. Toxicity
of insecticides to parasites of the spotted tentiform

leafminer (Lepidoptera: Gracillariidae). Can. Entomol.
113: 899-906.

Hutson, R. 1938. Nicotine sulfate and summer oil for control
of tentiform leafminer. J. Econ. Entomol. 31: 455.

Johnson, E.F., J.E. Laing and R. Trottier. 1976. The seasonal
occurrence of Lithocolletis blancardella (Gracillariidae),
and its major natural enemies in Ontario apple orchards,
Entomol. Soc. Ont., Proc., 107:31-45.

 

 

Johnson, E.F., R. Trottier and J.E. Laing. 1979. Degree
day relationships to the development of Lithocolletis
blancardella (Lepidoptera: Gracillariidae) and its
parasite Apanteles orni is (HymenOptera: Braconidae).
Can. Entomol. 111: II77-I184.

 

 

Kramer, F.R. 1963. Major leaf miner species occurring in
the South Tirolean fruit-farming region, and their con-
trol. Pflanzenschutz-Nachrichten (Bayer) 16: 1-16.

Maier, C.T. 1981. Seasonal occurrence, abundance, and leaf
damage of the apple blotch leafminer, Phyllonorycter
cratae ella, in Connecticut apple orcharHS} Environ.
EntomoI. I0: 645-649.

Maier, C.T. 1982. Parasitism of the apple blotch leafminer,

 

26

27

Phyllonorycter crataegella, on sprayed and unsprayed
appIe trees In Connecticut. Environ. Entomol. 11:
603-610.

 

Maier, C.T. 1984. Seasonal development and flight activity
of the spotted tentiform leafminer, Phyllonorycter
blancardella (Lepidoptera: Gracillariidaé), in
COnnecticut. Can. Ent. 116: 435-441.

 

 

Maier, C.T. 1984. Abundance and phenology of parasitoids
of the spotted tentiform leafminer, Phyllonorycter
blancardella (Lepidoptera: Gracillariidae), in
Connecticut. Can. Ent. 116: 443-449.

 

 

Pottinger, R.P. and E.J. LeRoux, 1971. The biology and dynamics
of Lithocolletis blancardella (Lepidoptera:
Gracillariidae , on apple in Quebec. Entomol. Soc.

Can. Mem. 77: 1-437.

 

Pree, D.J., E.A.C. Hagley, C.M. Simpson and A. Hikichi.
1980. Resistance of the spotted tentiform leafminer,
Phyllonorycter blancardella (Lepidoptera: Gracillariidae),
to organophosphorous insecticides in southern Ontario.
Can. Entomol. 112: 469-474.

 

Proctor, J.T.A., J.M. Bodner, W.J. Blackburn, and R.L. Watson.
1982. Analysis of the effects of the spotted tenti-
form 1eafminer (Phyllonorycter blancardella) on the
photosynthetic characteristics EI—apple leaves. Can.
J. Bot. 60: 2734-2740.

Reissig, W.H., R.W. weires and C.G. Forshey. 1982. Effects
of gracillariid leafminers on apple tree growth and
production. Environ. Entomol. 11: 958-963.

 

 

Trimble, R.M. 1983. Reliability of degree-day indices for
predicting spring emergence of the spotted tentiform

leafminer, Phyllonorycter blancardella (Leipidoptera:
Gracillariidae), in Ontario. Can. Ent. 115: 393-398.

 

 

Van Driesche, R. and G. Taub. 1983. Impact of parasitoids
on Phyllonorycter leafminers infesting apple in
Massachusetts, ULS.A. Prot. Ecol. 5: 303-317.

 

Weires, R.W., D.R. Davis, J.R. Leeper, and W.H. Reissig. 1980.
Distribution and parasitism of Gracillariid leafminers
on apple in the northeast. Ann. Entomol. Soc. Am. 73:
541-546.

Weires, Raw., 1981. Bionomics and control of spotted tenti-
form leafminer and San Jose scale. 87th Ann. Meet.
Mass. Fruit Growers Assoc., Inc., Proc. 87: 64-72.

II. OVICIDAL ACTIVITY OF INSECTICIDES ON THE
SPOTTED TENTIFORM LEAFMINER (LEPIDOPTERA:
GRACILLARIDAE) .

ABSTRACT

Several insecticides were tested for ovicidal acti-

vity on spotted tentiform leafminer (STLM), Phyllonorycter

 

blancardella (F.). In one laboratory experiment, fenvalerate

 

and methomyl caused 88 and 72% egg mortality, respectively,
while endosulfan was less effective (29.6% egg mortality).
The control (water) had the lowest egg mortality (8%). In a
second laboratory experiment, fenvalerate, permethrin, and
methomyl caused 92, 92, and 77% egg mortality, respectively,
while the control showed low egg mortality (13%). In field
applications, fenvalerate and diflubenzuron were effective
ovicides (100 and 70.7% egg mortality, respectively). Single-
tree applications of fenvalerate and diflubenzuron showed
both treatments to be ovicidal at low rates. Insecticides
targeted at the egg stage and applied before hatch add a new

dimension to STLM management.

28

INTRODUCTION

The spotted tentiform leafminer (STLM), PSyllonorycter

 

blancardella (F.), has become a sporadic, yet important

 

pest in Michigan apple orchards (Dutcher and Howitt 1978).
Damage to the leaves is caused by mining of the larval
stages. This feeding reduces chlorophyll content and the
photosynthetic rate of the leaves (Proctor et a1. 1982).
Heavy infestations can lead to early leaf abscission (Maier
1983), a reduction in terminal growth, fruit growth stunting,
premature ripening and fruit drop, and a reduction of fruit
set the year following infestation (Kramer 1963, Pottinger
and LeRoux 1971, Reissig et a1. 1982).

STLM has three generations per year in Michigan.
The third-generation overwinters as pupae in the leaf litter.
In April, the spring brood of adults emerges and lays eggs
on the underside of the unfolding leaves. There are five
larval instars (Pottinger and LeRoux 1971), the first three
are passed as sap-feeding larvae, which are dorso-ventrally
compressed and feed by shearing cells and ingesting the cell
contents. After the third instar, larvae undergo a hyper-
metamorphosis, becoming more cylindrical and developing
thoracic legs and prolegs. Their feeding habit changes to

chewing out irregular patches of the mesophyll cells of the

29

30

upper inside surface of the mine. As these threads dry
they cause an arching of the mine that results in a tentiform
appearance (Pottinger and LeRoux 1971).

Previous work on management of gracillariid 1eaf-
miners with insecticides has been aimed at controlling the
adult and larval life stages (Dutcher and Howitt 1978, Free
et a1. 1980), Weires 1981, Coli and Prokopy 1982). Our
work was undertaken to determine the activity of selected

insecticides on STLM eggs.

MATERIALS AND METHODS

Laboratory Experiments. The first laboratory experi-
ment was conducted in May 1983. Twelve one year-old 'Red
Delicious' apple seedlings were potted and placed in a growth
chamber to induce leaf growth. Once fully leafed, the seed-
lings were put in a large screened cage and exposed to adult
STLM, which had been collected as overwintering pupae found
in the previous year's apple leaf litter. Four days later,
when each seedling had a minimum of 25 eggs, the eggs were
counted with the aid of a stereomicroscope and marked by
flagging the petiole of each leaf that had eggs. Leaves with
one to four eggs were used in the experiment, excess eggs were
removed. Four treatments with three replicates each were
applied in a completely randomized design to the 12 seedlings.
The chemicals were measured using micropipets, then mixed
with 3,785 m1 of water in proportions corresponding to recom-
mended field rates. To simulate a dilute application by an
airblast sprayer, treatments were applied with hand held plant
misters until the point of spray runoff.

After 10 days at room.temperature, when all healthy
eggs would have hatched, each egg was examined microscopically,
and classified as dead or having hatched (both live and dead

larvae were classified as hatched eggs). Data was transformed

31

32

to arcsin l? before performing an analysis of variance to
test for treatment differences.

A second experiment was conducted in July 1983, using
the same design as the previous experiment, except that four
replicates of each treatment were applied. The STLM adults
used to provide the eggs were from first-generation mines
that had been collected from an unsprayed orchard and reared

at room temperature.

Field Experiments. Fenvalerate was so successful in
laboratory experiments (see Table 4), that we decided it
would be appropriate to test its ovicidal effect under field
conditions in 1984. The insect growth regulator diflubenzuron,
which had been observed to be ovicidal on STLM (J.G. Connell,
personal communication), was also tested.

The first experiment was set up in a heavily infested
orchard near Pullman, Michigan that contained 'Red Delicious'
and 'Golden Delicious' trees set on a spacing of 5.5 m between
trees and 6.4 m.between rows. There were 15 trees in each
0.05 ha plot. Treatments were assigned in a randomized com-
plete block design with three replicates. Diflubenzuron was
applied on 23 June, during second adult flight period, but
before second-generation eggs had been observed on the leaves
(it is recommended that diflubenzuron be applied to the leaves
before egg deposition (J.G. Connell, personal communication)).
Fenvalerate was applied on 26 June, after eggs had been

observed on the leaves. The treatments were applied with an

33

air blast sprayer with 1,640 liters of water per ha.

On 28 June, a small branch at an average height of
2 m was pruned from the west side of the central tree of each
plot. The branches were brought back to the laboratory,
examined microscopically, and 25 eggs from each sample were
chosen for future observation. The location of each egg was
marked by placing a hole in the leaf 5 mm from the egg on
the leaf margin side of the egg and on a line perpendicular
to the leaf's mid vein. The branches were placed in water
as bouquets and stored in a growth chamber at 24°C and a
16:8 (L:D) photoperiod. On 8 July, the marked eggs were exam-
ined microscopically and classified as dead or having hatched.
An analysis of variance was performed to test for treatment
differences.

The second experiment was designed to test the efficacy
of three rates of diflubenzuron as an ovicide. In an adjacent
orchard, treatments were assigned to single 'Red Delicious'
trees as a completely randomized design with 4 replicates.
Treatments were applied on 23 June with a high pressure hand-
gun to the point of spray runoff. On 28 June, sample branches
were pruned and eggs marked and stored as described in the
previous experiment. Egg mortality was evaluated on 8 July,
in the same manner as described in the previous experiment.

The third experiment was designed to test the efficacy
of fenvalerate at three different rates on third-generation

eggs. Treatments were assigned to single 'Red Delicious'

34

trees in a completely randomized design with four replicates.
Treatments were applied on 14 August, after third-generation
egg deposition had been observed. When the sprays had

dried, small branches were pruned and the same procedure for
marking and storing the eggs was followed as in the earlier
field experiments. Egg mortality was evaluated on 23 August,

in the same manner as described for the first field experiment.

RESULTS AND DISCUSSION

In the laboratory, fenvalerate and permethrin worked
well as ovicides (Table 4). Methomyl was less effective, and
endosulfan was the least effective. The control, using water
as a treatment, had a relatively low egg mortality in both
experiments.

In the orchard blocks in which the efficacy of
fenvalerate and diflubenzuron were tested, fenvalerate was an
excellent ovicide (Tablefi). Diflubenzuron also had ovicidal
activity.

The single-tree plots showed that fenvalerate and
diflubenzuron were ovicidal, even at reduced rates (Table 5).

All treatments were applied at dilute rates, thus en-
suring good coverage. We do not know whether concentrate
sprays would be effective.

In the past, two strategies of chemical control of
gracillariid leafminers have been recommended; sprays targeted
at the adults and timed to their emergence, or systemic
insecticides timed to control the sap-feeding larvae (Dutcher
and Howitt 1978, Free et a1. 1980, Weires 1981, Coli and
Prokopy 1982).

Control of adults is often difficult because of their

prolonged emergence and may require multiple sprays. The

35

36

Table 4: Laboratory evaluation of ovicidal activity of several insecticides on spotted

 

 

tentiform leafminer
Material and formulationa Rate- gAI/378 liteer Mean % egg mortalityc
Experiment 1
Fenvalerate 2.4EC 21 88.8 a
Methomyl 1.8EC 204 72.0 a
Endosulfan 3EC 231 29.6 b
Water (control) - 8.0 0
Experiment 2
Fenvalerate 2.4EC 21 92.0 a
Permethrin 213C 23 92.0 a
Methomyl 1.8EC 204 77.0 a
Water (control) - 13.0 b

 

aEC, emulsifiable concentrate.

bSprays based on dilute rate of 3740 liters/hectare.

cMeans followed by the same letter are not significantly different at the P=0.05 level
(Duncan's (1955) new multiple range test).

37

Table 5: Ovicidal activity of field applications of selected insecticides on spotted

 

 

tentiform leafminer
Material and formulationa Rate- gAI/hab Mean % egg mortalityc
Blocks
Fenvalerate 2.4EC 336 100.0 a
Diflubenzuron 25WP 210 70.7 b
Control - 12.0 c
Single trees
Diflubenzuron 25WP 280 71.0 ab
Diflubenzuron 25WP 210 57.0 b
Diflubenzuron 25WP 140 76.0 a
Control - 12.0 0
Single trees
Fenvalerate 2.4EC 224 73.0 a
Fenvalerate 2.4EC 168 68.5 a
Fenvalerate 2.4EC 112 68.0 a
Control - 9.0 b

 

aEC, emulsifiable concentrate; WP, wettable powder.

bSprays applied at 1640 liters/hectare.
cMeans followed by the same letter are not significantly different at the P=0.05 level
(Duncan's (1955) new multiple range test).

38

pyrethroids fenvalerate and permethrin are often used as

adulticides, especially for spring brood emergence. Sprays
generally start at tight cluster (blossom buds exposed, but
tightly appressed (Chapman 1966)), for first emerging moths.

Using an insecticide that acts as both an adulticide
and an ovicide can cut the number of spring brood treatments
to one well-timed spray at full pink (1-3 days before bloom
(Chapman 1966)), before egg hatch. This spray can control
existing eggs, as well as adults with egg laying potential.
Although STLM eggs are less than 0.4 mm wide (Pottinger and
LeRoux 1971), it may be feasible for growers or pest manage-
ment specialists to monitor egg deposition with a magnifying
hand lens, or by examining leaf samples microscopically, and
to make spray decisions based on an expected number of mines
per leaf;

Although fenvalerate was effective as an ovicide
against second-/ and third-generation STLM, this ovicide/
adulticide strategy is best suited for first-generation control,
when good coverage is more easily obtained because the trees
are not fully leafed, and when a pyrethroid spray is least
disruptive to STLM parasitoids and mite predators.

Diflubenzuron is not currently registered for use on
apples, but it showed promise as an ovicide. As an insect
growth regulator, it is probably not effective as an adulticide,
but its use as a second-/ or third-generation ovicide could

be advantageous because it would be less harmful to the adult

39

parasitoids of STLM larvae than are conventional chemical con-

trols.

REFERENCES

Chapman, P.J. 1966. Standard names for key apple bud stages,
Proc. N.Y.S. Hort. Soc. 111: 146-149.

Coli, W.M. and R.J. Prokopy, 1982. Biology, monitoring and
control of leafminers in Massachusetts. Proc. 88th

Annu. Meet. Mass. Fruit Growers Assoc., Inc. 88:
30-44.

Duncan, D.B. 1955. Multiple range and multiple F tests.
Biometrics 11: 1-41.

Dutcher, J.D. and A.J. Howitt. 1978. Bionomics and control
of Lithocolletis blancardella in Michigan. J. Econ.
EntomOIo JI: 736-738.

Kremer, F.R. 1963. Major leaf miner species occurring in the
South Tirolean fruit-farming region, and their control.
Pflanzenschutz-Nachr. 16: 1-16.

 

Maier, C.T. 1983. Effect of the apple blotch leafminer
(Lepidoptera: Gracillariidae) on apple leaf abscission.
J. Econ. Entomol. 76: 1265-1268.

Pottinger, R.P. and E.J. LeRoux. 1971. The biology and
dynamics of Lithocolletis blancardella (Lepidoptera:
Gracillaridae) on apple in'Quebec. FMem. Entomol.
Soc. Can. 77: 1-437.

 

Pree, D.J., E.A.C. Hagley, C.M. Simpson and A. Hikichi. 1980.
Resistance of the spotted tentiform leafminer,
Phyllonorycter blancardella (Lepidoptera: Gracillariidae),
to organopfibsphorous insectICides in southern Ontario.
Can. Entomol. 112: 469-474.

 

Proctor, J.T.A., J.M. Bodnar, W.J. Bladkburn, and R.L. watson.
1982. Analysis of the effects of the spotted tenti-
form 1eafminer (Phyllonorycter blancardella) on the
photosynthetic characteristiCs of apple leaves. Can.
J. Bot. 60: 2734-2740.

Reissig, W.H., R;W. Weires, and C.G. Forshey. 1982. Effects

of gracillariid leafminers on apple tree growth and
production. Environ. Entomol. 11: 958-963.

40

41

Weires, R.W. 1981. Bionomics and control of spotted tenti-
form leafminer and San Jose scale. Proc. 87th Annu.
Meet. Mass. Fruit Growers Assoc., Inc. 87: 64-72.

III. THE EFFECT OF SIMULATED SPOTTED TENTIFORM
LEAFMINER (LEPIDOPTERA: GRACILLARIIDAE)
DAMAGE, AFTER FRUIT SET, ON APPLE SIZING.

ABSTRACT

In 1983, fruiting spurs on 'Red Delicious' trees
were girdles or left ungirdled, and 0, 15, or 30% of their
leaf area was removed with a paper hole punch after 'June
drop' to determine the effect of defoliation on fruit size.
Apple weights at the time of treatment were estimated from
a curve relating fruit diameter to fruit weight. Changes in
weight by August 16 and harvest were measured. Ungirdled
spurs had significantly larger fruit than girdled spurs, but
there were no significant differences in fruit size among the
defoliation levels. In 1984, 50-90 cm.branches on 'Golden
Delicious' trees were girdled and adjusted to 10:1, 15:1, or
20:1 1eaf:fruit ratios after 'June drop'. Different levels
of second and third generation spotted tentiform leafminer
infestations were simulated with an elliptical hole punch
that was similar in size (80 mmz) and shape to a 'tissue-feeding'
mine. Changes in weight by August 27 and harvest were measured.
The effect of 1eaf:fruit ratio on weight gain was highly sig-
nificant. The effect of different infestation levels on weight
gain was not significant, even with three second generation
and five third generation mines/leaf. In both experiments
there were significant correlations between leaf area remaining

after defoliation and weight gain of apples. This type of

42

43

research is important for establishing damage-yield relation-

ships for foliage feeding insects.

INTRODUCTION

Establishing an economic injury level is one of the
priorities of any Integrated Pest Management program.

Stern et al. (1959) considered the economic injury level to
be "the lowest pest population density that will cause
economic damage". The ability to predict damage-yield
relationships is of primary importance in determining an
economic injury level for a pest.

Establishing damage-yield relationships is especially
difficult for apple pests that do not directly attack the
fruit, but are foliage feeders. Studying the economic sig-
nificance of damage-yield relationships in apples is further
complicated by the fact that growers are not trying to obtain
maximum yield for their inputs. Apple size is important in
determining marketability and therefore the profitability of
the crop. TEEggigglthelfruig (increasing the 1eaf:fruit
ratio) digggggeswyield,but increases fruit size and quality.
The apple grower is interested in reaching the point where
size is optimum, but yield is not decreased too much.

The effects of leaf area on fruit sizing have been
well studied (Haller and Magness 1925, Magness 1928, Link
1973, Williams 1979), and thinning recommendations are based
on these studies. The effects of defoliation caused by in-

sects and mites are less clear.

44

45

In the past, the effects of leaf damage on fruit
yield have been inferred by studying the effect on photo-
synthetic capacity of the leaves (Pn) in the laboratory.

Hall and Feree (1976) found that losses in leaf area by
artificial defoliation of up to 7.5% had no significant effect
on Pn. They also found that insect feeding simulated by
many small holes resulted in a larger decrease in Pn than an
equal area removed by large holes. The suggestion has been
made that the remaining leaf area is able to compensate for
lost area by increasing its photosynthetic efficiency (Flore
and Irwin 1983, Proctor et al. 1982). Flore and Irwin (1983)
found that up to 20% of the leaf area could be removed inter-
veinally without a significant reduction in Pn. Correlating
losses in Pn with yield reductions well enough to make pre-
dictions has yet to be done.

In the case of the spotted tentiform leafminer (STLM),

L.Phyllonorycter blancardella (F.), infestations have been

 

reported to cause a reduction in terminal growth, fruit growth

fl... wuuumhm.» -

stunting, premature ripening and fruit drop, and a reduction

WNWM'“ w.

of fruit set the year following infestation (Kremer 1963,

’1'“. P-WO‘M

Pottinger and LeRoux 1971). These reportswere based largely

on observations rather than quantitative measurements.

”W —t
5‘,“ W.

Reissig et a1. (1982) present quantitative data that indicate
a premature ripening and drop of fruit from 35+ year old
'McIntosh' trees with gracillariid leafminer infestations that

exceed 2 mines/leaf (combined lst and 2nd generation counts).

46

In one orchard of 'Red Delicious' that had an unsprayed
section with a combined first and second generation average
of over four mines/leaf, there was a reduction in average
fruit size between it and the lightly infested treated sec-
tion. Their data also indicated that a reduction in fruit
set and subsequent crop load (grams of apples per cm branch
circumference) in 'Ida Red' and 'Rome Beauty' was sometimes
associated with leafminer damage. Maeir (1983) showed that
destruction of more than 20% of the leaf surface by
gracillariid leafminers promoted early leaf abscission in
'McIntosh'.

The objective of this study was to investigate the
effect of simulated STLM damage on apple sizing during the
season of infestation. Second and third generation damage,
which occur after fruit set, were chosen to be studied because
low, untreated first generation populations can typically
build up to high densities that are perceived to be damaging
in these two final generations. This large population in-
crease seems more prevalent in the case of commercial orchards
that have low parasitism rates (Coli and Prokopy 1982, Van
Driesche and Taub 1983). Since natural STLM infestations at
varied levels are difficult to obtain, damage was simulated

by artificial defoliation.

MATERIALS AND METHODS

1983 - Effect of artificial defoliation of spur leaves on

apple weight increase.

Six fruiting spurs from each compass point (N,E,S,W)
were selected on 10 eleven year old 'Red Delicious' trees
grown on M106 rootstock. The trees were between 2.7 and 3.7 m
tall, and set on a spacing of 4.3 x 6 m, in an orchard free
of STLM infestation. The length and width of each leaf was
measured, and the formula L * W * .7 was used to estimate the
leaf area of each leaf on each spur (from previous work by
J. Flore, personal communication). The following treatments
were randomized among the 6 spurs: untreated; 15% defoliation;
30% defoliation; girdled - no defoliation; girdled - 15%
defoliation; and girdled - 30% defoliation. Girdling was
carried out to isolate the spurs from.the carbohydrate
resources of the remainder of the tree, and was accomplished
by removing a 3-6 mm.wide ring of bark and phloem, down to the
cambium, from the base of each spur. Defoliation was accom-
plished using a circular paper hole punch with an area of 32 mmz.
The holes were punched interveinally in the leaves, in a ran-
dom pattern on each spur. The treatments were carried out on

July 19 and 20, and coincided with the first observations of

second generation 'tissue-feeding' mines in a nearby orchard.

47

48

Four measurements of diameter (two lengths, two
widths) were taken for each apple with a caliper micrometer
on July 21. A sample of 30 apples, not involved in the
treatments, were then measured in the same manner, picked and
weighed. The surface area of each apple was estimated by
using the formula ndz (surface area of a sphere) and was
regressed against weight. A prediction equation was generated
to estimate the weight of each apple attached to a treated
spur. On August 16, new measurements were taken and a new
prediction equation was generated to estimate the apple
weights in the same manner as described above.

Apples were checked weekly for early abscission, any
abscissed apples were deleted from the data set used to deter-
mine final change in weight. A standard pest management pro-
gram was followed throughout the season, with pesticides
applied as needed. No irrigation was available. The apples
were harvested and their final weights were determined on

September 24.
1984 - Simulated STLM damage at three crop loads.

This experiment was set up as a randomized complete
block design on five eleven year-old 'Golden Delicious
Smoothee' trees on M106 rootstocks. The trees were between
2.7 and 3.7In tall, and set on a spacing of 4.3 x 6 m. They
were in alternate rows to the trees used in the 1983 experi-

ment. Twelve branches with basal cross section diameters of

49

approximately 10-15 mm and leaf to fruit ratios of less than
10:1 were chosen and flagged in each tree. A factorial set
of treatments of 0, l, 2 and 3 mines/leaf at each of the
following leaf to fruit ratios; 10 1, 15 1, and 20 1, were
randomly assigned. The desired leaf to fruit ratio of each
branch was obtained by removing fruit or entire spurs. Term-
inals were removed. Leaves judged to have an area of less
than 140 mm? were not counted. No more than 1 fruit/spur was
left. Each branch had from 4—6 fruit. The simulated mines
were added on July 16, to coincide with fruit observations
of 2nd generation 'tissue-feeding' mines in a nearby orchard.
The mines were simulated by using a hole punch that had been
‘modified to punch an elliptical hole with an area of 80 mm2
similar in size and shape to a 'tissue-feeding' mine. The
mines were punched interveinally in a random pattern on the
leaves and within the branch (to simulate natural infesta-
tions, larger leaves often had a larger proportion of mines).
Each branch was then girdled by removing a 3-6 mm wide ring of
bark and phloem, down to the cambium, from its base.

The final leaf area for each branch was calculated
by counting the number of spur or shoot leaves, multiplying
them.by the mean area of a spur or shoot leaf from that tree,
then subtracting the defoliated area. The mean spur and shoot
leaf was estimated from.a sample of 10 shoots and 10 spurs
randomly selected from each tree. The area of each leaf was
calculated using the formula L*W*.7 (from previous work by

J. Flore, personal communication).

50

Four measurements of diameter (two lengths, two
widths) were made for each apple with a caliper micrometer
on July 17. Twenty-five apples not involved in the treat-
ments were then measured in the same manner, picked, and
weighed. The surface area of each apple was estimated using
the formula ndz (surface area of a sphere), and was regressed
against weight. A prediction equation was generated to esti-
mate the weight of each apple on a branch. On August 27, new
diameter measurements were taken, and a new prediction equa-
tion was generated to estimate the apple weights in the same
manner as described above.

On August 28 and 29, the number of leaves and simulated
mines on each branch were re-counted, and new simulated mines
were added to give a total of two, three, and five mines/leaf
on the previous treatments of one, two, and three mines/leaf,
respectively. This added defoliation was timed to coincide
with the first observed third generation 'tissue-feeding'
mines in a nearby orchard.

Throughout the experiment, all the apples were checked
weekly for early abscission. If an apple fell, the branch was
re-adjusted to its assigned leaf to fruit ratio by removing
leaves. A standard pest management program was followed
throughout the season, with pesticides applied as needed. No
irrigation was available. The apples were harvested and their

final weights were determined on September 23.

RESULTS

1983 Experiment

Using a calculated surface area to estimate the
weight of hanging 'Red Delicious' apples proved to be effec-
tive, as is seen by their significant correlations (Figure 8).

The effect of girdling vs. not girdling the spurs
was significant (Table 6). Ungirdled spurs showed a higher
weight gain (> 345% difference by harvest) than girdled spurs.

There was no significant effect of the different
defoliation levels on either girdled or ungirdled spurs, al-
though for girdled spurs there was a trend of decreasing
weight gain with higher levels of defoliation. There were no
significant girdling x defoliation interactions in this experi-
ment. The effect of blocking by trees proved to be signifi-
cant.

The importance of the leaf area remaining after de-
foliation to weight gain is evident when looking at the data
from the girdled treatments. There is a linear relationship
between the two variables within the intervals we studied
(Figures 9 and 10). The association between leaf area and
weight gain is less evident for the ungirdled treatments.

There were no observable differences in premature

fruit drop between the treatments by harvest time (September 24).

51

52

    
   

 

 

 

 

5“ 7/21/83
0
454
" 39-
3’
E; 33‘
o
3:
274
y=—13.3+.0095X
r=.987
214
15.
I T T I
3000 4000 5000 6000
‘20‘ 8/16/83
100-
15
:: 80*
..C
5?
o
g: 60‘
y=-25.7 + .012x
. r==.992
40a
20
I I 1 T
5000 7000 9000 11000

Surface Area (mm’)

Figure 8: Prediction equations for apple weight based
on surface area. 1983 - 'Red Delicious'.

53

Table 6: Effects of girdling and defoliation of spurs on apple weight gain, 1983.

 

 

 

Increase in weighta
Girdling % defoliation Treatment to 8/16 Treatment to 9/24

- 0 43.3 a 100.8 a

- 15 44.3 a 102.1 a

- 30 44.9 a 105.9 a

0 15.9 b 29.2 b

15 13.7 b 27.7 b

+ 30 12.7 b 26.8 b

 

a Means followed by the same letter are not significantly different at the P=0.05 level

(Duncan's (1955) new multiple range test).

Change in wt. (9) 7/21-8/16

(g) 7/21-8/16

Change in wt.

54

  
 

 

 

 

26- Means of subsamples
of girdled treatments
0
23«
20-
,7.
O
14-
ys1.77+.0024x
0 r=.726
11d
0
8 O
I U I l I T I l l
60‘
Means of subsamples
of ungirdled treatments
554
O
O
50- 0. o .
454
40" .
e y=40.2 +.0008X
' ’ r=.249
35~
30

 

 

1 I I I I I I I l
2000 3000 4000 5000 6000 70008000 9000 10000

Leaf area/fruit (mm’) after defoliation

Figure 9: Effect of leaf area per fruit on weight gain.
Treatment to 8/16/83.

Change in wt. (9) 7/21-9/24

Change in wt. (9) 7/21-9/24

55

   

 

 

  

 

 

451 Means of subsamples
of girdled treatments
40~ ‘
O
35-
0
30-1
25- .
. y: 11.74 +.003x
0 r=a746
20- ° ‘
O
151
2000 3000 4000 5000 6000 70b0 8000
140-
Means of subsamples
of ungirdled treatments 0
130- _—
120- ' .
1101
100-
. . . y=87.15+.003x
. ° r=A05
90‘ e . o
80
I I I I I I I I I

2000 3000 4000 5000 6000 7000 8000 9000 10000

Leaf area/fruit (mm’) after defoliation

Figure 10: Effect of leaf area per fruit on weight gain.

Treatment to harvest (9/24/83).

56
1984 Experiment

The prediction equations for the weight of hanging
apples based on calculated surface area for 'Golden
Delicious' were similar to the equations generated for 'Red
Delicious' in 1983 (Figures 8 and 11).

The interaction of crop load and simulated leafminer
damage are summarized as follows (Tables 7 and 8). In the
analysis of this factorial experiment, the effects of differ-
ent 1eaf:fruit ratios (Table 11), and blocking by tree were
highly significant (Table 9). There was no significant
effect due to different infestation levels (Table 10), nor were
there significant 1eaf:fruit ratio x infestation interactions
(Table 9).

As in the 1983 experiment, the leaf area remaining
after defoliation was important in determining the fruit
weight gain. The relationship between leaf area and weight
gain is linear within the intervals that we studied (Figure 12).

There were no observable differences in premature
fruit drop between the treatments by harvest time (September

23).

57

Table 7: Interactive effects of crop load and simulated leafminer damage on change in

apple weight (grams) from 7/ 16 to 8/27.

 

 

 

No. simulated LeasznIit Ratio
mines/leaf
(Gen. 2, Gen. 3) 10:1 15:1 20:]
0,0 14.6 a 22.2 be 27.4 e
1,2 11.7 a 238de 23.1bcd
2,3 11.7 a 18.0 abc 25.6 de
3,5 12.9 a 17.1 ab 28.0 e

 

Means followed by the same letter are not significantly different at the P=0.05 level
(Duncan's (1955) new multiple range test).

58

Table 8: Interactive effects of crop load and simulated leafminer damage
on change in apple weight (grams) from 7/16 to 9/23.

 

 

 

No. simulated Ixaszruit Ratio
mines/leaf
(Gen. 2, Gen. 3) 10:1 15:1 20:1
0,0 20.2 a 33.3 be 45.0 e
1,2 22.8 a 34.2 bcd 36.3 cde
2,3 16.8 a 26.8 abc 41.0 de
3,5 17.3 a 24.7 ab 45.7 e

 

Means followed by the same letter are not significantly different at the P=0.05 level
(Duncan's (1955) new multiple range test.

59

Table 9: Mean squares showing the effects of 1eaf:fruit ratio and different infestation
levels on apple weight gain.

 

 

Source of Variation df Mean Square
Tree 4 l80.26***
Treatments 11 161.03***
L:F Ratio 2 744.93***
Infestation level 3 28.88
Ratio x infestation 6 32.48
Error 44 22.04

 

*** Highly significant (P<.0001)

60

Table 10: Defoliation level effects on apple weight gain (averaged across leaf :fruit

 

 

 

ratios).
N o. simulated Increase in Weight (g)
mines/leaf

(Gen. 2, Gen. 3) by 8/27 by harvest (9/23)
0,0 21.4 32.8
1,2 21.0 31.1
2,3 19.4 29.2
3,5 18.4 28.2

 

No significant differences were found between means within columns at the P=0.05
level (Duncan's (1955) new multiple range test).

61

Table 11: Leaf:fruit ratio effects on apple weight gain (averaged across defoliation

 

 

 

levels).
Leaszruit Ratio Increase in Weight (g)21
by 8/27 by harvest (9/23)
10:1 13.8 a 19.3 a
15:1 20.3 b 29.8 b
20:1 26.0 c 42.0 c

 

a Means followed by the same letter within columns are not significantly different at the
P=0.05 level (Duncan's (1955) new multiple range test).

Weight (9)

Weight (g)

48-
42'1
36.1
30"4
244
18%

12

62
7/16/84 0

 

y: -11.5 + .0083x
r=.988

   

 

100‘

85‘

70-

55‘

40q

25‘

10

 

I I
2500 3700 4900 6000

8/16/84

   
 
 

y=-22.8 + .0109x
r=.989

 

I I I I I I I I
4000 5000 6000 7000 8000 9000 10000 11000

Surface Area (mm?)

Figure 11: Prediction equations for apple weight based

on surface area. 1984 - 'Golden Delicious'.

Mean change in wt.(g) 7/16-8/27

Mean change in wt.(g) 8/27-9l23

63

  
 
  

 

 

30~
26-4
224
y: 5.42 + .0009x
‘3“ r-.905
14-
O
10
I ’1 l I I I 1
20-1 Leaf area/fruit after 2nd Gen. Damage
17~
14-
11-
y=—.520+ .0008x
3'1 r=.869
5—
O
2

 

 

I I I I I I I
5000 9000 13000 17000 21000 25000 29000

Leaf area/fruit (mm2)after 2nd 8 3rd Gen. Damage

Figure 12: Effect of leaf area per fruit on weight gain.
'Golden Delicious' 1984.

DISCUSSION

The fact that ungirdled spurs showed a higher weight
gain than girdled spurs in the 1983 experiment shows that
girdling was necessary to study the localized effects of
defoliation. Our work agrees with other studies that have
shown that other sources within the tree provide carbohydrates
to the fruit on the ungirdled spur (Feree and Palmer 1982).

The significant correlations between leaf area and
weight gained for girdled spurs indicate that girdling res-
tricts the carbohydrate supply of the fruit to the local spur
leaves, while an ungirdled spur is free to receive carbo-
hydrates from other sources such as nearby non-bearing spurs,
stored carbohydrate in the scaffold branch, or carbohydrate
supplied from the terminal shoots.

Even with our treatments of 30% defoliation in 1983,
and three and five simulated second and third generation
mines in 1984 (approximately 22 and 36% reduction in spur
leaf area, respectively), we did not reach a threshold where
significant differences could be seen in apple sizing. This
may be attributed to compensation by increased photosynthetic
activity of the remaining leaf tissue (Flore 1983, Proctor et
al. 1982). The data do seem to indicate that under our

specific conditions the recommended action threshold of two

64

65

mines/leaf for second generation populations of STLM (Weires
1981, Reissig et al. 1982) was too conservative. However,

we were not able to measure the effect of second generation
mining on next year's fruit bud formation, nor did we fully
investigate the effect on fruit drop, because of our relativ-
ely early harvest dates.

Rainfall during the months of July, August and
September of 1983 and 1984 were below average. This is
reflected in the relatively small size of the fruit for both
years.

Both years' data show that the leaf area remaining
after defoliation is important in determining final fruit
size, even when defoliation occurs after fruit set. This has
important implications when setting thresholds for leaf feed-
ing insects. Ames et al. (1984) showed differential effects
of mite feeding at different crop loads on fruit size and
other parameters affecting crop value. Crop load should play
an important role in deciding the impact of foliage feeders
on fruit sizing, and economic thresholds or treatment strate-
gies should be varied accordingly.

The block effect was important in both experiments.
This shows that the potential for fruit sizing varies from
tree to tree, even with similar leaf area to fruit relation-
ships. The potential for larger fruit may depend on the pre-
vious vigor of the tree and previous stored carbohydrates.
This is yet another variable to be considered when establish-

ing damage~yield relationships.

66

When simulated mines are compared to actual mines,
there may be important physical and physiological differences
that could affect the results obtained in this type of ex-
periment. Ethylene is produced by damaged tissue, and is
important in regulating fruit abscission (Edgerton 1971).
Mines simulated with a hole punch remove the area of the
'damaged' leaf tissue, while actual STLM mines leave this
tissue intact, and could therefore be producing more ethylene.
In the case of an actual mine the damage is sealed within the
leaf epidermis. This may cause more ethylene to be trans-
located rather than volatilized. Simulated mines may have a
more drastic effect on Pn over time because the whole area is
removed at once, while with an actual mine the area is slowly
eaten away. Simulated mines may also cause more water loss
by the leaf because of the cut area around the mine perimeter
contrasted with the sealed STLM mine.

Photosynthetic efficiency will vary depending on the
light trapping efficiency of the tree (Hall and Feree 1976),
as will the impact of STLM infestations. The pruning prac-
tices and the planting densities of orchards will determine
light trapping efficiency. Weather, scion-rootstock inter-
actions (Feree and Barden 1971), and cultural practices
(Feree 1978) also affect net photosynthesis of apple trees.
To be able to accurately predict damage-yield relationships
of STLM and other foliage feeders under varying conditions,
more joint research needs to be carried out between horti-

culturalists and entomologists.

Ames, G.

Barden,

Coli, W.

REFERENCES

K., D.T. Johnson, and R.C. Rom. 1984. The effect
of European red mite feeding on the fruit quality
of 'Miller Sturdeespur' apple. J. Amer. Hort. Sci.
109(6): 834-837.

J.A., 1978. Apple leaves, their morphology and
photosynthetic potential. HortScience 13: 644-646.

M. and R.J. Prokopy. 1982. Biology, monitoring and
control of leafminers in Massachusetts. 88th Ann.
Meezing Mass. Fruit Growers Assoc., Inc., Proc. 88:
30- .

Edgerton, L.J. 1971. Apple abscission. HortScience 6: 26-30.

Feree, D.C. 1978. Cultural factors influencing net photo-

synthesis of apple trees. HortScience 13(6): 650-
652.

Feree, D.C. and F.R. Hall. 1981. Influence of physical

stress on photosynthesis and transpiration of apple
leaves. J. Amer. Soc. Hort. Sci. 106(3): 348-351.

Feree, D.C. and J.W. Palmer. 1982. Effect of spur defoli-

ation and ringing during bloom on fruitin , fruit
mineral level, and net photosynthesis of Golden
Delicious' apple. J. Amer. Soc. Hort. Sci. 107(6):
1182-1186.

Feree, M.E. and J.A. Barden. 1971. The influence of

strains and rootstocks on photosynthesis, respiration,
and morphology of 'Delicious' apple trees. J. Amer.
Soc. Hort. Sci. 96(4): 453-457.

Flore, J.A. and C.C. Irwin. 1983. The influence of defoli-

Hall, F.

ation and leaf injury on leaf photosynthetic rate,
diffusive resistance, and whole tree dry matter
accumulation in apple. HortScience 18: 586. (abstr.).

R. and D.C. Feree. 1976. Effects of insect injury

simulation on photosynthesis of apple leaves. Econ.
Entomol. 69: 245-248.

67

68

Haller, M.H. and J.R. Magness. 1925. The relation of leaf
area to the growth and composition of apples. Proc.
Am. Soc. Hort. Sci. 189-196. 1925.

Kremer, F.R. 1963. Major leaf miner species occurring in
the South Tirolean fruit-farming region, and their
control. Pflanzenschutz-Nachrichten (Bayer) 16: 1-16.

Magness, J.R. 1928. Relation of leaf area to size and
quality in apples. Proc. Amer. Soc. Hort. Sci. 25:
285-288.

Maier, C.T. 1983. Effect of the apple blotch leafminer
(Lepidoptera: Gracillariidae) on apple leaf abscission.
J. Econ. Entomol. 76: 1265-1268.

Pottinger, R.P. and E.J. LeRoux. 1971. The biology and
dynamics of Lithocolletis blancardella (Lepidoptera:
Gracillariidae) on apple in Québec. *Entomol. Soc.
Can. Mem. 77: 1-437.

 

Proctor, J.T.A., J.M. Bodnar, W.J. Blackburn, and R.L. Watson.
1982. Analysis of the effects of the Spotted tenti-
form leafminer (Phyllonorycter blancardella) on the
photosynthetic characteriStics of—apple—leaves. Can.
J. Bot. 60: 2734-2740.

 

Reissig, W.H., R.W. Weires and C.G. Forshey. 1982. Effects
of gracillariid leafminers on apple tree growth and
production. Environ. Entomol. 11: 958-963.

Stern, V.M., R.F. Smith, R. van den Bosch, and K.S. Hagen.
1959. The integrated control concept. Hilgardia 29(2):
81.

Van Driesche, R. and G. Taub. 1983. Impact of parasitoids
on Phyllonorycter leafminers infesting apple in
Massachusetts, U.S.A. Prot. Ecol. 5: 303-317.

Weires, R.W. 1981. Bionomics and control of spotted tenti-
form 1eafminer and San Jose Scale. 87th Ann Meet.
Mass Fruit Growers Assoc., Inc., Proc. 87: 64-72.

CONCLUSION

The spotted tentiform leafminer is an intriguing
apple pest to study for many reasons. It is sporadic, and
its population dynamics are not well understood. In unsprayed
orchards its populations are kept under control by natural
mortality factors, yet in commercial orchards populations can
explode. This suggests that biological control could work
under proper conditions, but in view of the current management
practices for other pests, would seem almost impossible to
implement. Its interveinal leafmining habit is perceived to
be harmful to apple trees, yet damage-yield relationships are
not well understood, and economic injury levels have been set
using observations more than quantitative data. STLM will
remain a controversial pest until more of the questions con-
cerning its role in the apple system.are answered.

The objective of this thesis was to add new and perti-
nent information to the pool of knowledge on STLM, with the
hopes of bettering our management practices.

In keeping with the concept of researching an inte-
grated pest management program for STLM, it was found that
parasitoids are effective in maintaining STLM populations be-
low thresholds, and that there are certain times in the life

cycle of the pest when short residual chemical controls would

69

70

miss the susceptible parasitoids.

It was also found that the number of adulticide
sprays can be reduced by using well timed pyrethroid sprays
targeted at the adults and eggs, or by using a Dimilin spray
targeted at the eggs. By timing a spray to the adults and
eggs, rather than 'sap-feeding' larvae, parasitoids have a
better chance of escaping harm because there is more time be-
tween the spray and their emergence. Dimilin would have an
added advantage, in that being and insect growth regulator,
it would probably not adversely affect adult parasitoids. In
either case, since 100% kill is difficult to obtain, any
surviving STLM could serve as sources for future parasitoid
development.

If a spring brood adulticide/ovicide spray was cor-
rectly timed to kill STLM eggs and miss the parasitoids, it
is unlikely that second and third generations would build up
to damaging levels. we found that fruit sizing would not be
significantly decreased with 30% defoliation, or with the
simulation of three second and five third generation mines/leaf.
This is above the current recommended thresholds of two second
generation and three third generation mines/leaf, but we
recognize that damage-yield relationships will vary under
different environmental and cultural conditions. Pest managers
should take this into account as well as parasitism levels and
mortality of the previous generation when deciding whether an

insecticide application is necessary.

71

This is the essence of an Integrated Pest Management
program, to monitor a pest's development throughout the
season to see if it reaches economic thresholds, and if it
does, to know how your management action will affect the sys-
tem. Since STLM and its parasitoids are only a small part
of the apple pest complex, this work needs to be integrated

into an overall pest management system for apples.

LIST OF REFERENCES

LIST OF REFERENCES

Ames, G.K., D.T. Johnson, and R.C. Rom. 1984. The effect
of European red mite feeding on the fruit quality

of 'Miller Sturdeespur' apple. J. Amer. Hort. Sci.
109(6): 834-837.

Barden, J.A., 1978. Apple leaves, their morphology and
photosynthetic potential. HortScience 13: 644-646.

Chapman, P.J. 1966° Standard names for key apple bud
stages. Proc N.Y.S. Hort. Soc. 111: 146-149.

Coli, W.M. and R.J. Prokopy. 1982. Biology, monitoring and
control of leafminers in Massachusetts. 88th Ann.
Meeting Mass. Fruit Growers Assoc., Inc., Proc 88:
30-44.

Croft, B.A. 1975. Tree fruit pest management. In 'Intro-
duction to Pest Management'. R.L. Metcalf and W.H.
Luckman (Eds.), Wiley and Sons, New York, pp. 471-508.

Doganlar, M. and A. Mutuura. 1980. A new species of Ehyllg;
r an. (=Lithocolletis an.) (Lepidoptera:
Gracillariidae) from western North America. Can.
Entomol. 112: 311-314.

Duncan, D.B. 1955. Multiple range and multiple F tests.
Biometrics 11: 1-41.

Dutcher, J.D. and A.J. Howitt. 1978. Bionomics and control
of Lithocolletis blancardella in Michigan. J. Econ.
Entomol. 71: 736-738.

 

Dutcher, J.D. 1975. The bionomics of Lithocolletis
blancardella (Lepidoptera: GraciIIariidEe) in Michigan.
Masters Thesis. Michigan St. Univ. 43 p.

 

Edgerton, L.J. 1971. Apple abscission. HortScience 6: 26-30.

Feree, D.C. 1978. Cultural factors influencing net photo-
synthesis of apple trees. HortScience 13(6): 650-652.

Feree, D.C., F.R. Hall. 1981. Influence of physical stress

on photosynthesis and transpiration of apple leaves.
J. Amer. Soc. Hort. Sci. 106(3): 348-351.

72

73

Feree, D.C. and J.W. Palmer. 1982. Effect of spur defoli-
ation and ringing during bloom.on fruitin , fruit
mineral level, and net photosynthesis of Golden
Delicious' apple. J. Amer. Soc. Hort. Sci. 107(6):
1182-1186.

Feree, M.E. and J.A. Barden. 1971. The influence of strains
and rootstocks on photosynthesis, respiration, and
morphology of 'Delicious apple trees. J. Amer. Soc.
Hort. Sci. 96(4): 453-457.

Flore, J.A. and C.C. Irwin. 1983. The influence of defoli-
ation and leaf injury on leaf photosynthetic rate,
diffusive resistance, and whole tree dry matter
accumulation in apple. HortScience 18: 586. (abstr.).

Hagley, E.A.C. 1985. Parasites recovered from the overwinter-
ing generation of the spotted tentiform leafminer,
éggpédgptera: Gracillariidae). Can. Entomol. 113:

- o .

Hall, F.R. and D.C. Feree. 1976. Effects of insect injury
simulation on photosynthesis of apple leaves. Econ.
Entomol. 69: 245-248.

Haller, M.H. and J.R. Magness. 1925. The relation of leaf
area to the growth and composition of apples. Proc.
Am. Soc. Hort. Sci. 189-196. 1925.

Haynes, D.L., S.H. Gage and W. Fulton. 1974. Management of
the cereal leaf beetle ecosystem. Quaest. Entomol.
19: 165-176.

Hough, W.S. 1963. Resistance to insecticides by codling moth

and red banded leafroller. Va. Agr. Exp. Sta. Tech.
Bull. 166. 32pp.

Hoyt, S.C. and E.C. Burts. 1974. Integrated control of
fruit pests. Annu. Rev. Entomol.. 19: 231-252.

Huffaker, C.B., M; van de Drie, and J.A. McMurty. 1969.
The ecology of tetranychid mites and their natural
control. Annu. Rev. Entomol. 14: 125-174.

Hutson, R. 1938. Nicotine sulfate and summer oil for control
of tentiform leafminer. J. Econ. Entomol. 31: 455.

Johnson, E.F., J.E. Laing and R. Trottier. 1976. The seasonal
occurrence of Lithocolletis blancardella (Gracillariidae),
and its major naturaI enemies in Ontario apple orchards.
Entomol. Soc. Ont., Proc., 107: 31-45.

 

74

Johnson, E.F., R. Trottier and J.E. Laing. 1979. Degree day
relationships to the development of Lithocolletis
blancardella (Lepidoptera: Gracillariidae) and its

parasite A anteles orni is (Hymenoptera: Braconidae).
Can. Entomol. III: II77-II84.

 

 

,. Kremer, F.R. 1963. Major leaf miner species occurring in

the South Tirolean fruit-farming region, and their
control. Pflanzenschutz-Nachrichten (Bayer) 16: 1-16.

Luckman, W.H. and R.L. Metcalf. 1975. The pest-mane ement
concept. In 'Introduction to Pest Management .
R.L. Metcalf and W.H. Luckman (Eds.), Wiley and Sons,
New York, pp. 3-35.

Magness, J.R. 1928. Relation of leaf area to size and
ggality in apples. Proc. Amer. Soc. Hort. Sci. 25:
5-288.

Maier, C.T. 1981. Seasonal occurrence, abundance, and leaf
damage of the apple blotch leafminer. Phyllonorygter

cratae ella, in Connecticut apple orchards. EnVIron.
EntomoI. 10: 645-649.

Maier, C.T. 1982. Parasitism of the apple blotch leafminer,
Phyllonorycter crataegella, on sprayed and unsprayed

apple trees in Connecticut. Environ. Entomol. 11:
603-610.

Maier, C.T. 1983. Effect of the apple blotch leafminer
(Lepidoptera: Gracillariidae) on apple leaf abscission.
J. Econ. Entomol. 76: 1265-1268.

 

 

Maier, C.T. 1984. Seasonal development and flight activity of
the spotted tentiform leafminer, Phyllonorycter
blancardella (Lepidoptera: Gracillariidae), in
ConnectICut. Can. Ent. 116: 435-441.

 

 

Maier, C.T. 1984. Abundance and phenology of parasitoids of
the spotted tentiform leafminer, Phyllonorycter
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