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6/01 cJClRC/Dateouopes-sz

 

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BIOLOGICAL CONTROL OF OBLIQUEBANDED LEAFROLLER,
CHORISTONEURA ROSACEANA (HARRIS) (LEPIDOPTERA: TORTRICIDAE), IN
MICHIGAN APPLE ORCHARDS
By

Tammy K. Wilkinson

A THESIS

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

MASTER OF SCIENCE

2002

af

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ABSTRACT
BIOLOGICAL CONTROL OF OBLIQUEBANDED LEAFROLLER,
CHORISTONEURA ROSACEANA (HARRIS) (LEPIDOPTERA: TORTRICIDAE), IN
MICHIGAN APPLE ORCHARDS
By

Tammy K. Wilkinson

The Obliquebanded leafroller (OBLR), Choristoneura rosaceana (Harris), is one Of the
major arthropod pests in Michigan apple production, due to OBLR’S resistance to
organophosphate insecticides. In 1999 and 2000 we conducted a survey of the parasitoid
community of OBLR in Michigan apple orchards. A total of 9,044 OBLR larvae were
collected of which 2,229 were parasitized. The most abundant parasitoids were Bassus
dimidiator (Braconidae), Macrocentrus linearis (Braconidae), Colpoclypeusﬂorus
(Eulophidae), Nilea erecta (Tachinidae), and Actia interrupta (Tachinidae). Insecticide
bioassays were conducted testing the direct effects of ﬁve insecticides currently used for
control of OBLR on adult B. dimidiator and M. linearis. Ranking of the insecticides from
least toxic to most toxic resulted in control (water) = Intrepid < Provado = Asana =
SpinTor < Guthion. A ﬁnal study was conducted to determine when adult B. dimidiator
and M. linearis are present in the orchard. Parasitoid occurrence was compared to OBLR
adult ﬂight data. A total of 13 parasitoids were recovered from sentinel larvae 11 were an
Enytus sp. and two were M. linearis. Only three B. dimidiator were captured in yellow
bucket traps. Macrocentrus linearis appeared to have been present in the orchards Shortly
after peak OBLR adult ﬂight that occurred in mid June. Bassus dimidiator appeared to be

present in the orchards during peak OBLR ﬂight.

ACKNOWLEDGEMENTS

I would like to thank Doug Landis, Larry Gut, Suzanne Lang, and Rufus Isaacs,
for their guidance and patience as I worked towards my Masters degree at Michigan State
University. I would also like to thank the Staff at the USDA Niles Plant Protection center
for their cooperation and for supplying me with the many parasitoids that made my
research possible. I would also like to thank M. Sharkey, M. Schauff, J. O’Hara, K.
Ahlstrom, and P. Marsh for identiﬁcation of parasitoids, and Gary Parsons for helping me
ﬁnd the museum specimens I needed. I would like to thank my fellow graduate Students
Tyler Fox, Matt O’Neal and Alejandro Costamagna for any help that they could lend, and
for making me laugh. I would like to thank Chris Sebolt, Pete McGhee, Mike Haas, John
Wise, Janice Howard, and Ryan VanderPoppen for technical support and sound advice. I
would especially like to thank the undergraduate students: Alison Gould, Andrea
McMillian, Sandra Clay, Christie Hemrning, Michelle Smith, Meghan Burns, Matt
Lenart, Chris Cervany, and Tim Schutz that I was fortunate enough to work with. They
sacriﬁced weekends and worked from early morning until late at night at times, they
worked in the sweltering heat, and the pouring rain just to lend me a hand. Without these
workers I would not have been able to go home. I would like to thank my husband,
Frederick Wilkinson, for his support, understanding, and patience while I pursued my
Masters degree. I would also like to thank my Parents and family for all the

encouragement they have given me throughout my long career as a student.

iii

TABLE OF CONTENTS

LIST OF TABLES ............................................................................ vi
LIST OF FIGURES ........................................................................... ix
Chapter 1: Literature Review ................................................................ 1
Impact Of Obliquebanded leafroller on Michigan Apple Production ......... 1

OBLR Biology ........................................................................ 1

OBLR Insecticide Resistance ....................................................... 3
Integrated Pest Management in Fruit Production ................................. 4
Biological Control and the Orchard Ecosystem .................................. 5

OBLR Control and Potential Impacts on Parasitoids ........................... 7

OBLR Parasitoids ..................................................................... 8
Parasitoids of OBLR in Michigan .................................................. 11
Bassus dimidiator .............................................................. 11
Macrocentrus linearis ......................................................... 13

Conclusions ............................................................................ 13
Objectives of Study ................................................................... 14
References .............................................................................. 15

Chapter 2: Parasitism of LarvalObliquebanded Leafroller, Choristoneura rosaceana
(Harris) (Lepidoptera: Tortricidae), in Commercially Sprayed Michigan Apple Orchards

........................................................................................... 20
Abstract ................................................................................. 20
Introduction ............................................................................ 21
Methods ................................................................................. 23

Parasitoid Identiﬁcation ....................................................... 26

Statistical Analysis ............................................................. 26
Results .................................................................................. 27
Discussion .............................................................................. 3 1
Conclusion ............................................................................. 34
References .............................................................................. 66

Chapter 3: The direct effects of ﬁve insecticides on survival Of Bassus dimidiator (NeeS.)
and Macrocentrus linearis (Nees.)(Hymenoptera: Braconidae), parasitoids of the
obliquebandedleafroller, Choristoneura rosaceana (Harris) (Lepidoptera:

Tortricidae) ...................................................................................... 69
Abstract ................................................................................. 69
Introduction ............................................................................ 7 1
Methods ................................................................................. 75

Bassus dimidiaror Exposed to Residues on Petri Dishes ................. 76
Bassus dimidiator Exposed to Residues on Leaves ....................... 77

Macrocentrus linearis Exposed to Residues on Petri Dishes and Leaves 78

iv

Statistical Analysis ............................................................. 79

Results .................................................................................. 79
Bassus dimidiator Exposed to Residues on Petri Dishes .................. 79
Females: residues dried 1h ............................................. 80

Males: residues dried 1h ................................................ 81

Bassus dimidiator Exposed to Residues on Petri Dishes and Leaves... 82
Females: residues on Petri dishes dried 1h ........................... 82

Males: residues on Petri dishes dried 1h .............................. 83

Females: residues on Petri dishes dried 24h ......................... 85

Males: residues on Petri dishes dried 24h ............................ 86

Females: residues on apple leaves dried 1h .......................... 86

Males: residues on apple leaves dried 1h ............................. 87

Females: residues on apple leaves dried 24h ........................ 89

Males: residues on apple leaves dried 24h ........................... 89
Macrocentrus linearis Exposed to Residues on Petri Dishes and Leaves 9O
Females: residues on Petri dishes dried 1h ........................... 91

Males: residues on Petri dishes dried 1h .............................. 92

Females: residues on Petri dishes dried 24h ......................... 93

Males: residues on Petri dishes dried 24h ............................ 94

Females: residues on apple leaves dried 1h .......................... 95

Males: residues on apple leaves dried 1h ............................. 96

Females: residues on apple leaves dried 24h ........................ 97

Males: residues on apple leaves dried 24h ........................... 98
Discussion .............................................................................. 99
Conclusion .............................................................................. 102
References .............................................................................. l 19

Chapter 4: Phenology Of Adult Bassus dimidiator (Nees.) and Macrocentrus linearis
(Nees.) (Hymenoptera: Braconidae), in Commercially managed Michigan apple

orchards ......................................................................................... 122
Abstract ............................................................................... 122
Introduction ........................................................................... 123
Methods .............................................................................. 125
Results ................................................................................ 128
Discussion and Conclusion ........................................................ 130
References ......... ' .................................................................. 141

Appendix 1 ........................................................... 142

LIST OF TABLES

Table 2.1. Orchard location and number of blocks sampled for overwintering and ﬁrst
generation OBLR during 1999 and 2000.

Table 2.2. Percent parasitism and total overwintering and ﬁrst generation OBLR
collected from apple orchards in the Southwest and Fruit Ridge regions of Michigan
during 1999 and 2000.

Table 2.3. Percent parasitism of overwintering and ﬁrst generation OBLR for each apple
orchard located in the Southwest and Fruit Ridge regions of Michigan during 1999.

Table 2.4. Percent parasitism of overwintering and ﬁrst generation OBLR for each apple
orchard located in the Southwest and Fruit Ridge regions of Michigan during 2000.

Table 2.5. Parasitoids recovered from overwintering and ﬁrst generation OBLR collected
from apple orchards in the Southwest region of Michigan during 1999.

Table 2.6. Parasitoids recovered from overwintering and ﬁrst generation OBLR collected
from apple orchards in the Southwest region of Michigan during 2000.

Table 2.7. Parasitoids recovered from overwintering and ﬁrst generation OBLR collected
from apple orchards in the Fruit Ridge region of Michigan during 1999.

Table 2.8. Parasitoids recovered from overwintering and ﬁrst generation OBLR collected
from apple orchards in the Fruit Ridge region of Michigan during 2000.

Table 2.9. Parasitoids attacking overwintering and ﬁrst generation OBLR in apple
orchards from the Southwest and Fruit Ridge regions of Michigan during 1999.

Table 2.10. Parasitoids attacking overwintering and ﬁrst generation OBLR in apple
orchards from the Southwest and Fruit Ridge regions Of Michigan during 2000.

Table 2.11. Hymenopteran parasitoids that comprised less than 5% of the total parasitoid
complex attacking overwintering and ﬁrst generation OBLR from apple orchards located
in the Southwest and Fruit Ridge regions of Michigan during 1999 and 2000.

Table 2.12. Percentage of species comprising the complex of Tachinidae attacking
overwintering and ﬁrst generation OBLR from apple orchards located in the Southwest
and Fruit Ridge regions of Michigan during 1999 and 2000.

Table 2.13. Number of overwintering and ﬁrst generation OBLR that were parasitized or
un-parasitized from apple orchards in the Southwest and Fruit Ridge regions of Michigan
during 1999 and 2000.

vi

Table 3.1. The formulated product of ﬁve insecticides currently used for control Of
OBLR in apple orchards their class, chemical names, and highest recommended ﬁeld
rates (Wise et al. 2002)

Table 3.2. Survival analysis results for B. dimidiator exposed to residues Of ﬁve
insecticides and water controls dried lh on Petri dishes.

Table 3.3. Mean (:SE) proportion of B. dimidiator males and females surviving to 4, 24,
48, and 120h time after exposure to the residues Of ﬁve insecticides dried 1h on Petri
dishes. The total number of parasitoids (It) used at the start of each experiment over ﬁve
weeks. Chemicals followed by different letters are Signiﬁcantly different (p50.05)
determined by survival analysis.

Table 3.4. Survival analysis results for B. dimidiator exposed to residues of ﬁve
insecticides and a water control on Petri dishes or apple leaves dried 1h or 24h.

Table 3.5. Total mean (tSE) proportion of B. dimidiator males and females surviving to
4, 24, 48, 72, 96, and 120h time after exposure to the residues of ﬁve insecticides dried
1h on Petri dishes. The total number of parasitoids (n) used at the Start of each
experiment over ﬁve weeks. Chemicals followed by different letters are signiﬁcantly
different (p_<_0.05) determined by survival analysis.

Table 3.6. Total mean (:SE) proportion of B. dimidiator males and females surviving to
4, 24, 48, 72, 96, and 120h time after exposure to the residues of ﬁve insecticides dried
24h on Petri dishes. The total number of parasitoids (11) used at the start of each
experiment over ﬁve weeks.

Table 3.7. Mean (iSE) proportion of B. dimidiator males and females surviving to 4, 24,
48, 72, 96, and 120h time after exposure to the residues of ﬁve insecticides and a water
control dried 1h on apple leaves. The total number of parasitoids (n) used at the start of
each experiment over ﬁve weeks. Chemicals followed by different letters are
signiﬁcantly different (pS0.05) determined by survival analysis.

Table 3.8. Mean (:SE) proportion of B. dimidiator males and females surviving to 4, 24,
48, 72, 96, and 120h time after exposure to the residues of ﬁve insecticides and a water
control dried 24h on apple leaves. The total number of parasitoids (11) used at the start of
each experiment over ﬁve weeks.

Table 3.9. Results of survival analysis for M. linearis exposed to ﬁve insecticides and a
water control dried lb or 24h on Petri dishes or apple leaves.

vii

Table 3.10. Mean (:SE) proportion of M. linearis males and females surviving to 4, 24,
48, 72, 96, and 120h time after exposure to the residues of ﬁve insecticides and a water
control dried 1h on Petri dishes. The total number of parasitoids (n) used at the start of
each experiment over ﬁve weeks. Chemicals followed by different letters are
signiﬁcantly different (p50.05) determined by survival analysis.

Table 3.11. Mean (:SE) proportion of M. linearis males and females surviving to 4, 24,
48, 72, 96, and 120h time after exposure to the residues of ﬁve insecticides and a water

control dried 24h on Petri dishes. The total number of parasitoids (11) used at the start of
each experiment over ﬁve weeks.

Table 3.12. Mean (:SE) proportion of M. linearis males and females surviving to 4, 24,
48, 72, 96, and 120h time after exposure to the residues Of ﬁve insecticides and a water

control dried 1h on apple leaves. The total number of parasitoids (n) used at the start of

each experiment over ﬁve weeks.

Table 3.13. Mean (:SE) proportion of M. linearis males and females surviving to 4, 24,
48, 72, 96, and 120h time after exposure to the residues of ﬁve insecticides and a water
control dried 24h on apple leaves. The total number of parasitoids (11) used at the start of
each experiment over ﬁve weeks.

Table 4.1. Number of sentinel larvae and parasitoids recovered from three apple orchards
located in Allegan, Kent, and Van Buren counties, Michigan.

Table 4.2. Total number of Hymenoptera further broken down into the number of bees,

wasps (including B. dimidiator), number of B. dimidiator, and ants, and the total number
of Diptera collected in yellow bucket traps that had been placed into three apple orchards
located in three Michigan counties (Allegan, Kent, and Van Buren).

viii

LIST OF FIGURES

Figure 2.1. Michigan counties where survey of parasitoids attacking OBLR in apple
orchards was conducted during 1999 and 2000. Where Montcalm, Kent, and Ottawa
counties are located in the Fruit Ridge region and Van Buren and Bem’en counties are
located in the Southwest region of the state. The Trevor Nichols Research Center is
located in Allegan County.

Figure 2.2. Percentage of parasitoid species attacking overwintering generation OBLR in
apple orchards located in the Southwest and Fruit Ridge regions of Michigan during
1999.

Figure 2.3. Percentage of parasitoid species attacking ﬁrst generation OBLR in apple
orchards located in the Southwest and Fruit Ridge regions of Michigan during 1999.

Figure 2.4. Percentage of parasitoid species attacking overwintering generation OBLR in
apple orchards located in the Southwest and Fruit Ridge regions of Michigan during
2000.

Figure 2.5. Percentage Of parasitoid Species attacking ﬁrst generation OBLR in apple
orchards located in the Southwest and Fruit Ridge regions of Michigan during 2000.

Figure 2.6. Percent of overwintering (OW) and ﬁrst (F1) generation OBLR parasitized
either high or low in the apple tree canopy in the Southwest and Fruit Ridge regions of
Michigan during 1999 and 2000.

Figure 3.1. Insecticide bioassay arena where both the top and bottom Petri dishes have
been sprayed with insecticide and allowed to dry.

Figure 3.2. Insecticide bioassay arena where the leaf was sprayed with insecticide and
allowed to dry.

Figure 4.1. Counties where sample orchards were located (n=1/county) in Michigan.
Yellow bucket traps and sentinel larvae were used to identify the time when adult B.
dimidiator and M. linearis are present in commercially sprayed apple orchards. Kent
county is located in the “Fruit Ridge” region and Van Buren county is located in the
“Southwest” region of the state, two of the major apple producing regions of Michigan.

Figure 4.2. A sentinel station consisting of (a.) 2L pop bottle support suspended from an

apple branch with plastic cable ties and (b.) a station with cup containing cut apple
branches and OBLR larvae.

ix

Figure 4.3. Placement of sentinel OBLR larvae stations and yellow bucket traps in apple
trees. Sentinel larvae stations (circles) were located in trees Opposite of one another in
different rows and yellow bucket traps (squares) were located in a single row on either
side of a sentinel larvae station.

Figure 4.4. The number of Enytus sp. and M. linearis recovered from sentinel larvae and
the dates that the larvae had been placed in the orchard located in Allegan county,
Michigan, along with the number of adult OBLR caught in pheromone traps. The timing
of codling moth (CM) Spray and leafroller (LR) spray applications are indicated by
dashed and solid arrows respectively.

Figure 4.5. The number of B. dimidiator caught in yellow bucket traps located in an
apple orchard in Van Buren county, Michigan, and the dates that the buckets were left in
the orchard, along with the number of OBLR adults caught in pheromone traps. The
tinting of codling moth (CM) spray and leafroller (LR) spray applications are indicated
by dashed and solid arrows respectively.

 

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Chapter 1
Literature Review

Impact of Obliquebanded Leafroller on Michigan Apple Production

The biology Of the Obliquebanded leafroller (OBLR), Choristoneura rosaceana
(Harris), coupled with its resistance to organophosphate insecticides has made this insect
one of the most economically important pests in Michigan apple production. Michigan is
the third leading apple producing state in North America, with 49,000 acres of working
apple orchards (Klewno & Matthews 2001). Feeding damage from OBLR larvae causes a
considerable amount Of fruit loss. More than 15% of harvested fruit is unﬁt for retail
distribution because of OBLR cosmetic damage (Ho 1996). Fruit that is damaged early in
its development by OBLR feeding usually drops Off from the tree before harvest. The
most severe fruit damage occurs after petal fall as larvae feed on the developing fruit
(Reissig 1978). As fruit increases in Size it is more likely to stay on the tree until harvest
because OBLR damage does not interfere with fruit development. Madsen et al. (1984)
classiﬁes this type of injury as either “early season,” where fruit has deep “russetted”
scars, or “summer” injury characterized by shallow feeding scars. A great amount of
effort and resources are put into insect control with insecticides being the number one
cost in fruit production (Brunner 1996).
OBLR Biology

The Obliquebanded leafroller is a Tortricid moth native to North America,
occurring throughout the United States and into southern Canada (Reissig 1978, Howitt
1993). The versatility Of leafroller host plant utilization, their high fecundity, and their

ability to disperse both as adults and larvae have contributed to their broad range pest

 

 

 

 

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Status in fruit production (Howitt, 1993, Suckling et al., 1998). OBLR larvae are
phytophagous, commonly feeding on plants in the Rosaceae family, including apple,
pear, cherry, peach, plum, rose, gooseberry, currant, Strawberry, blueberry, and various
weeds (Reissig 1978, Howitt 1993, Ohlendorf 1999).

A single egg mass contains an average of approximately 200 eggs, however a
Single adult female OBLR is capable of producing up to 900 eggs during her lifetime
(Howitt 1993). To avoid competition after eclosion, larvae disperse from oviposition sites
by ballooning away on Silk strands (Howitt 1993). Therefore, OBLR larvae infesting
orchards may have originated from a different host location, such as a bordering woodlot
or an abandoned neighboring orchard (Mayer and Beime 1974). Croft (1982) suggests
that the more mobile an insect, the more it is to be exposed to insecticide levels that
would provide sufﬁcient selective pressure thereby increasing the probability of
developing resistance.

Michigan OBLR are bivoltine (having two generations per year) while those at
higher latitudes are univoltine and those in southern latitudes are multivoltine (Chapman
et al. 1968). Differences in the number of generations per year at varying latitudes
correspond to the differences in temperature and time available to complete a lifecycle.
Insects like OBLR with multiple generations and high reproductive rates develop
resistance to insecticides at a faster rate than those without these attributes (Croft 1982).

OBLR has a total of ﬁve instars and overwinter as second or third instar larvae
between late August and late September (Howitt 1993). Overwintering OBLR can be
found beneath the bark of the apple tree within a tightly spun silk shelter called a

hibemaculum. From late April into early May overwintering larvae will emerge from the

hibemaculum and begin feeding on developing fruit, leaves and ﬂower parts (Reissig
1978, Howitt 1993, Ohlendorf 1999). Emergence of overwintering larvae is bimodal
(AliNiazee 1986), which explains the occurrence of adults and late instars well into July.
In Michigan, the ﬁrst adult OBLR ﬂight peaks from mid-June into July and the second
ﬂight occurs in the latter part of August into early September (Howitt 1993).

Larvae characteristically build leaf Shelters for protection from parasitism,
predation, and other environmental conditions. Leaf shelters are constructed by rolling
the leaf over so that there is an opening at each end and binding it with Silk. Larvae will
also bind several leaves together or to nearby fruit to feed in the safety of the shelter
(Howitt 1993, Ohlendorf 1999). When disturbed, OBLR larvae will drop down from the
leaf surface on a strand of Silk and later pull themselves back up onto the leaf they had
previously abandoned
OBLR Insecticide Resistance

Organophosphate (OPS) and carbamate insecticides have been the leading method
of insect control in Michigan orchards for 40 years (Gut et al. 1998). These insecticides
have gradually become less effective throughout North America and in Canada, due to
the development of insecticide resistance. Problems with increasing OBLR damage and
declines in effectiveness of control started appearing in New York in the 1970’s but were
not documented until the 1980’s, and only recently has resistance been reported in
Canada (Lawson et al.1997, Smirle et al. 1998). Resistance by OBLR to OP insecticides
was ﬁrst detected in Michigan in the 1970’s (Howitt 1993). In New York orchards,

Reissig et al. (1986) found that OBLR resistant colonies were 115 times more resistant to

 

 

 

 

 

 

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more resistant to OPS than susceptible colonies (Gut et al. 1998).

Fitness costs associated with OBLR resistance include a decline in fecundity,
decreased pupal and larval weight, and increased development time. The latter may
increase mortality by providing more Opportunities for parasitism and predation (Carriere
et al. 1994), or decrease mortality by allowing OBLR to avoid exposure to insecticides
(Carriere et al. 1995). New insecticides have been developed over the years for OBLR
control but with continuous use these also are becoming ineffective. Waldstein and
Reissig (2000) have detected resistance to the newest insect growth regulators (IGRS),
tebufenozide, which interrupt the molting process by interfering with the insect’s molting
hormone, 20-hydroxy ecdysone.

Integrated Pest Management in Fruit Production

Traditionally, insecticides were applied regardless of insect abundance as a means
of preventing damage (Prokopy et al. 1994). This practice was altered when resistance
became evident, which led in part to the development of integrated pest management
(1PM) in the 1960’s (Croft 1982). At its beginning, IPM consisted of the application of
insecticides only as needed, when population levels neared economic threshold, which is
the point where insect damage causes unacceptable economic loss (Van Driesche et
al.1998). Although this more prudent use of insecticides was a step in the right direction,
the continued dependence on chemicals was far from sustainable and insufﬁcient to solve
the problem of resistance.

IPM in apple production has gradually evolved due to the inadequacies of relying

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enemy populations. In the last 20 years IPM has been approached from a more
ecologically based method of insect control, reducing the use of broad-Spectrum
insecticides and using methods more favorable to biological control systems (Gruys
1982). Current alternatives to broad-spectrum materials for OBLR control include
pheromone mating disruption (Gut et al. 1999), selective insecticides such as the IGRS
(Sun et al. 2000), changes in cultural practices (Lawson et al. 1998), and biological
control (Viggiani 2000). These methods must be properly integrated in order to be truly
effective; no one method can stand alone. Insecticides, although decreasing in their
effectiveness Still remain the most immediately sought after method for quickly
controlling increasing pest populations. Insecticide use is a short-term solution that can
result in long-term reduction of natural enemies and ultimately a resurgence of the pest
population. Growers Should Strive for long—term sustainable control practices where pests
can be maintained below economic threshold by their natural enemies when low levels of
insecticides are used along with pheromone mating disruption or other selective control
tactics. Biological control of orchard pests has not been widely implemented in the past,
but parasitoids naturally occurring in the orchard ecosystem can be a major mortality
factor of OBLR with low insecticide use (Brunner 1998).
Biological Control and the Orchard Ecosystem

The frequent use of insecticides, fungicides and herbicides used to maintain tree
health and increase fruit crop yields make the orchard ecosystem a highly disrupted and
unfriendly place for natural enemies. Insecticides are probably the greatest limiting factor
affecting the success of parasitoids and other natural enemies already present or entering

the orchard in regulating pest populations. Landis and Menalled (1998) consider the

 

 

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“management of insecticide impacts as the most important conservation measure to
preserve viable and effective parasitoid communities.” Diversity of parasitoids is also
dependent on the diversity of the vegetation in and around the orchard. According to the
Natural Enemies Hypothesis, an increase in plant diversity may increase the number of
natural enemies and reduce herbivore density (Root 1973). Orchards with a greater
degree of vegetational diversity(even with a high level of disturbance) have a larger
number of natural enemies than those with low vegetational diversity (Szentkiralyi and
Kozar 1991). This is most likely due to the differences in the available refuge and food
resources. The parasitoid communities present in these refuges are an important source
for recolonization and replacement of parasitoids lost to insecticide treatments within the
orchard (Landis and Menalled 1998). Van Driesche et al. (1998) reported that the greatest
concentration of parasitoids is at the perimeter of an orchard, due either to movement
within the orchard between blocks or from an inﬂux of parasitoids from outside the
orchard. Some OBLR parasitoids may be entering the orchard in search of hosts to
overwinter in. Maltais et al. (1989) reported that the parasitoid, Meteorus trachynotus
Veireck, which attacks the spruce bud worm, Choristoneurafumiferana (Clemens), uses
OBLR as its host for overwintering. The OBRL parasitoid, Colpoclypeusﬂorus (Walker),
on the other hand, must leave the orchard in order to locate suitable overwintering hosts
(Gruys and Vaal 1984, Dijkstra 1986). Pfannenstiel et al. (2000) have found that C. ﬂorus
is able to use the strawberry leafroller, Ancylis comprana Froelich, as an overwintering
host. Collectively, these are examples of how the types of vegetation surrounding the

orchard ecosystem can affect parasitoid numbers and diversity. Vegetational diversity in

 

 

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commercial orchards is kept to a minimum by mowing and herbicide applications in
order to decrease competition between trees and weed species, and avoid yield reduction.

Biological control usually focuses on establishing Stable populations of already
existing parasitoids (Landis and Menalled 1998). If stable populations of parasitoids are
to be maintained in an orchard ecosystem, more attention needs to be paid to the types of
insecticides used and the effect they have on parasitoids as well as the provision of
appropriate vegetational diversity.
OBLR Control and Potential Impacts on Parasitoids

The International Organization of Biological Control, West Palaearctic Region
Section, created the working group, “Pesticides and Beneﬁcial Organisms” to develop
standard methods for testing the effects of insecticides on parasitoids and to determine if
any are suitable for use in IPM (Hassan 1998). Testing the effects of agricultural
chemicals on natural enemies is mandatory in several countries before the chemicals can
be registered for use (Hassan 1998). Such testing of insecticides on parasitoids prior to
use in the orchard should be an integral part of all IPM programs. Growers could then
avoid using insecticides harmful to natural enemies and thereby achieve high levels of
pest suppression by parasitoids already present in the orchard. Houk (1954) reported
parasitoid releases in Michigan orchards from the 1930’s until 1943 when DDT became a
dominant form of insecticide control.

Alternative methods for OBLR control are actively being developed as OP’S are
being Slowly phased out as a result of the Food Quality Protection Act (1996). These
methods include pheromone mating disruption (Gut et al. 1999), microbial insecticides

(Bacillus thuringiensis or Bt) (Li et al. 1995), and insect growth regulators (Sun et al.

2000). In addition summer pruning and thinning Of apples (Lawson et al. 1998) and
biological control (Viggiani 2000) have been explored. The level of safety for natural
enemies exposed to the new selective insecticides is questionable, while there is little
doubt that pheromone mating disruption and the cultural practices of summer pruning and
thinning for OBLR control have no impact on natural enemy health. Summer pruning and
thinning reduces OBLR damage by removing its favored food source, succulent leaves;
in addition the removal of fruit clusters forces OBLR to search more actively for other
fruit to damage (Lawson et al. 1998). Lawson et al. (1998) also demonstrated that these
practices improve fruit quality, giving fruit greater access to the sun and more room to
grow. Gut et al. (1999) have found that orchards where pheromone mating disruption was
used incurred less OBLR feeding damage than those that used insecticides as their only
means of control.
OBLR Parasitoids

Parasitoids require an insect host in order to complete their lifecycle. Competition
between parasitoids is reduced by differential resource utilization, by attacking different
life stages and by attacking different species. The Trichogrammatidae, for instance,
parasitize the host’s eggs, preventing larval emergence and thus parasitism by a larval
parasitoid. More importantly parasitoids have diverged into two distinct evolutionary
pathways: endoparasitism and ectoparasitism (Mills 1992). Ectoparasitoids develop
outside of the host’s body and endoparasitoids develop within the host’s body. These two
groups can be categorized further into idiobionts, which terminate the host’s development
upon ovipostion and koinobionts, which allow the host to continue development after

oviposition (Mills 1992). Ectoparasitoids are primarily idiobionts, and most

 

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endoparasitoids are koinobionts (Mills 1992). Both lifestyles have their advantages and
disadvantages. Koinobionts have a longer development time because the host is allowed
to grow as the parasitoid develops; however, extended development time increases the
chances of predation. Idiobionts often have a more rapid development time because they
lack the protection that koinobionts have within the host’s body. Ectoparasitoids have an
advantage in that they do not have to contend with its host’s immune responses and
therefore they can have a broader host range than endoparasitoids (Mills 1992). The
widest host ranges occur in egg and pupal parasitoids (Mills 1992), because hosts at these
two stages in their development are undergoing rapid morphological change, which
impairs immune responses.

Parasitoids can be further divided into guilds depending on the life stage of the
host they attack, whether they are endo- or ecto- parasitoids and whether development is
continuous or extended (Mills 1992). Eleven different guilds of parasitoid, which attack
all life stages of Tortricid hosts have been identiﬁed (Mills 1993).

The host’s vulnerability to attack by parasitoids is inﬂuenced by its feeding Sites.
An insect housed within a gall is vulnerable to fewer parasitoids than one exposed on a
leaf surface (Hawkins 1994). Although OBLR make shelters by rolling leaves, they are
highly vulnerable to parasitoid attack when they leave this shelter to feed. Even within
the conﬁnes of their leaf rolls OBLR are vulnerable to attack by parasitoids adapted to
ovipositing through the leafroll structure. Host density also can increase the chance Of
parasitoid attack. Mills (1993) noted that host density may increase the amount of volatile
cues given Off by a plant subjected to feeding damage thereby attracting a searching

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Knowing the relative densities of parasitoid populations compared with host
populations is important for an IPM approach that is parasitoid friendly. During an
outbreak of a pest species the number of individual parasitoids and their species richness
increases (Balazs 1997). Subsequently, as the pest population declines these parasitoids
help establish and maintain the pest under economic threshold (Balazs 1997). The
majority of parasitoids found in orchards are native species (Viggiani 2000). Surveys of
the parasitoids attacking OBLR have been conducted in apple orchards, raspberry ﬁelds,
and in wild host vegetation in Canada (Donganlar and Beime 1978, Hagley and Barber
1991, Li et al. 1999, Vakenti et a1. 2001) and the United States (Pogue 1985, Biddinger et
al. 1994, Brunner 1996, Ho 1996). OBLR is attacked by several guilds of parasitoids
including the egg parasitoid Trichogramma spp., which is being monitored for their level
of success in suppressing leafroller populations in raspberries (McGregor et al. 1997). Li
et al. (1999) collected OBLR from raspberry ﬁelds in British Columbia, Canada, and
recovered 13 Hymenopteran species, 11 from larvae and 2 from pupae, and 1 Dipteran
Species from pupae. Vakenti et al. (2001) recovered 18 parasitoid Species from OBLR
collected from wild host plants. OBLR collected from unmanaged apple orchards in
Ontario, Canada, were parasitized by 16 parasitoid species, 14 Hymenoptera and 2
Diptera (Hagley and Barber 1991). Donganlar and Beirne (1978) recovered 9 Species of
parasitoid from OBLR in apple orchards in the Vancouver district of British Columbia,
Canada. OBLR are also routinely collected and assessed for parasitism in the State of
Washington (Brunner 1996). Pogue (1985) reared 11 hymenopterous parasitoids from
OBLR and two other leafroller pests, Archips argyrospilus (Walker) and Anacampsis

innocuella (Zeller), collected from Shelterbelts in Wyoming, United States. Biddinger et

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al. (1994) found that OBLR may be an alternate host for parasitoids that attack the tufted
apple bud moth, Plarynota idaeusalis (Walker), in Pennsylvania, United States, orchards.
Parasitoids of OBLR in Michigan

Ho (1996) conducted a survey of the parasitoids attacking OBLR in Michigan
apple orchards during 1995 but recovered small numbers of parasitoids from three main
families. This was the ﬁrst parasitoid survey of this kind conducted in Michigan. During
the spring and summer of 1999 a second survey of parasitoids attacking OBLR in
Michigan apple orchards was initiated (Chapter 2). This survey resulted in the discovery
of two important parasitoids, Bassus dimidiator (Nees.) and Macrocentrus linearis
(Nees.) (Hymenoptera: Braconidae).

Bassus dimidiator

When considering the usefulness of a parasitoid species as an effective biological
control agent in an orchard ecosystem it is vital to understand its life cycle and biology so
that the appropriate tinting of insecticides can be determined in order not to limit the
fecundity and success of the parasitoid. Bassus dimidiator (Nees.) is a solitary
endoparasitoid previously only collected from the eye-spotted bud moth, Spilonota
ocellana (Denis and Schifferrnuller) (Krombein et al. 1979). The eye-Spotted bud moth
was introduced from Europe via nursery Stock in the 1800’s (Howitt 1993).

Dondale (1954) has reported the complete biology of this parasitoid as it occurs
within the eye-spotted bud moth, which should be Similar to its biology in OBLR.
Dondale (1954) found that B. dimidiator overwinters within the host and resumes its
development in the spring with the emergence of the host. This parasitoid lays its egg in

the ganglion of the ventral nerve cord (Dondale 1954). The host larva is able to feed and

11

develop normally as B. dimidiator feeds on “non-vital” structures. AS the host nears the
pupal stage and ends feeding, B. dimidiator consumes the host’s entrails at a faster pace,
exits the hosts body and ﬁnishes its meal externally, then pupates (Dondale 1954).
Female B. dimidiator lays one egg per host and may parasitize between 15 and 20 hosts
(Dondale 1954). Dondale (1954) observed this parasitoid visiting wild carrot, suggesting
that it served as a possible source of nectar, and noted that B. dimidiator was able to live
for greater than a week when supplied a 25% sugar cane solution. Asman and Lee
(unpublished data) found that the days of survival of both B. dimidiator and
Macrocentrus linearis were signiﬁcantly lengthened when supplied a 50% honey solution
compared to those parasitoids given water only. Although food resources are a possible
limiting factor for these parasitoids given current weed control methods (mowing and
herbicide use) within orchards, the more prevalent limitation to this parasitoids success
may be the effects of broadly toxic insecticides.

The vulnerability of B. dimidiator to insecticides appears to depend on the
chemical and the length of time that chemical has been in use. Stultz (1954) found that in
areas where DDT was used for more than a year Agar/It’s laticinctus (Cresson) or B.
dimidiator (Nees.) was able to parastitize up to 90% of the bud moth population. At this
time bud moths were becoming resistant to DDT. The possibility of resistance to DDT by
the parasitoid is unknown however, B. dimidiaror populations were not affected by other
chemicals, such as nicotine sulphate, which had a great impact on several other important

parasitoids (Stultz 1955).

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Macrocentrus linearis

No literature was found describing the biology of Macrocentrus linearis (Nees.)
Speciﬁcally, although my observations indicate it is a solitary polyembyronic
endoparasitoid. Li et al. (1999) described the biology of the polyembryonic,
Macrocentrus nigridorsis Viereck, a parasitoid of OBLR in raspberries. Polyembryony
refers to the ability of a single egg laid by a female to multiply into multiple embryos.
Parasitoids can be either haploid (males) or diploid (females). In the polyembryonic
species that yield males and females it is likely that two eggs were laid; one fertilized
(females) and one unfertilized (males) (Li et al. 1999). The OBLR that were parasitized
by M. nigridorsis had 36 parasitoids emerge from each individual host on average (Li et
al. 1999). This is an endoparasitoid that feeds on the host internally and emerges from the
host as the host nears its ﬁnal instar. The parasitoids at this time begin to feed externally
until parasitoid pupation. These parasitoids “Spin up” their cocoons Simultaneously,
binding together with silk and cocoons oriented parallel to one another (Li et a1. 1999).
Adults emerge at approximately the same time.
Conclusions

The Obliquebanded leafroller’s resistance to organophosphate insecticides has
caused Signiﬁcant economic concerns in Michigan apple production. Alternative forms of
control are being assessed and biological control along with pheromone mating
disruption Show promise as sustainable and long-term solutions for this problem. The
potential of a parasitoid as an effective biological control agent in an orchard ecosystem
is greatly limited by the use of insecticides. The effects of the most widely used

chemicals for control of OBLR on the survivability of parasitoids present in the orchard

13

ecosystem are unknown and need to be investigated. A current survey of the parasitoids
attacking OBLR in Michigan apple orchards could reveal which parasitoids may be the
most effective control agents for this pest. Phenology of these parasitoids should be 0
studied as they develop on OBLR in Michigan apple orchards. Recommendations could
then be made to Michigan apple growers that could increase the success of an integrated
pest management program for OBLR that utilizes biological control agents. Reducing the
use of insecticides and allowing for OBLR control by natural enemies will lead to a more
economical and sustainable orchard ecosystem.

Objectives of Study

1. Complete a two year survey of the parasitoids attacking OBLR in commercially
sprayed Michigan apple orchards in two important apple producing regions.

2. Test the direct effects of ﬁve of the principal insecticides currently used in
Michigan apple orchards for control of OBLR or other fruit pests on the survival
and longevity of adult B. dimidiator and M. linearis.

3. Determine the time at which adult parasitoids B. dimidiator and M. linearis are

present in commercially sprayed apple orchards in Michigan.

14

 

 

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References

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17

 

 

In ”I! In

In

(I) ’1'!!!)

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18

 

 

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Vakenti, J .M., J .E. Cossentine, B.E. Cooper, M.J. Sharkey, C.M. Yoshimoto, and L.B.M.
Jensen. 2001. Host-plant range and parasitoids of Obliquebanded and three-lined
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19

 

 

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Chapter 2

Parasitism of Larval Obliquebanded Leafroller, Choristoneura rosaceana (Harris)
(Lepidoptera: Tortricidae), in Commercially Sprayed Michigan Apple Orchards.

Abstract

The Obliquebanded leafroller (OBLR), Choristoneura rosaceana (Harris), is one
of the major arthropod pests in Michigan apple production. In 1999 and 2000 a survey of
the parasitoid community of OBLR in commercially sprayed apple orchards in Michigan
was conducted to determine the species present and their importance to OBLR population
management. A total Of 9,044 OBLR larvae were collected of which 2,229 were
parasitized. Parasitism of OBLR was found to increase from the overwintering generation
to the ﬁrst generation for both regions and both years. In 1999 11% of the 1,126
overwintering OBLR collected were parasitized, while 29% of the 3,749 ﬁrst generation
OBLR collected were parasitized. In 2000 8% of the 489 overwintering OBLR collected
were parasitized, while 26% of the 3,680 ﬁrst generation OBLR collected were
parasitized. A total of approximately 21 species of parasitoids from 9 families were
recovered from OBLR, composed of Hymenopteran and Dipteran parasitoids. The most
abundant Hymenopteran parasitoids were Bassus dimidiaror (Braconidae) comprising
47% of the parasitism, followed by Colpoclypeusﬂorus (8% of the total) (Eulophidae)
and Macrocentrus linearis (2% of the total) (Braconidae). Dipteran parasitoids
(Tachinidae) accounted for 37% of the parasitism, and were largely comprised of Nilea
erecta (30%) and Actia interrupra (22%). These collections include new host records for
B. dimidiator (Braconidae) and Hyphantrophaga blanda and Comsilura concinnata
(Tachinidae). The parasitoid C. ﬂorus (Eulophidae) was also reported from Michigan for

the ﬁrst time.

20

Introduction

The Obliquebanded leafroller (OBLR), Choristoneura rosaceana (Harris), is a
Tortricid moth native to North America (Reissig 1978). In Michigan, OBLR has two
generations per year, overwintering as second or third instar larvae and emerging from
overwintering hibemaculae in late April to early May (Howitt 1993). First adult ﬂight of
OBLR occurs in late June or early July and second adult ﬂight at the end of August
(Howitt 1993). OBLR larvae can be easily Spotted in the apple tree canopy by the
presence of their leaf Shelters. Larvae create Shelters by folding over a leaf and binding it
with silk. Larvae will also bind several leaves together or to nearby fruit and feed within
the safety of the shelter (Howitt 1993, Ohlendorf 1999). OBLR larvae are phytophagous,
commonly feeding on plants in the Rosaceae family, including apple, pear, cherry, peach,
plum, rose, raspberry, gooseberry, currant, strawberry, blueberry, and various weeds
(Reissig 1978, Howitt 1993, Ohlendorf 1999). In apple, OBLR larvae feed on ﬂower
buds, leaves, and developing fruit (Reissig 1978, Howitt 1993, Ohlendorf 1999). The
greatest damage to fruit occurs after petal fall as fruit increases in Size (Reissig 1978,
Howitt 1993). Fruit injury caused by overwintering larvae early in the season is
characterized by deep scars while injury caused during the summer can be recognized by
Shallow feeding scars (Madsen et a1. 1984, Howitt 1993, Ohlendorf 1999). As a result of
its damage to fruit and resistance to pesticides, OBLR is one of the most economically
important pests of apple causing more than 15 % damage to harvested fruit in some
orchards (Ho 1996).

In the past, organophosphate (OP) insecticides such as azinphos-methyl, have

been widely used for control of OBLR. AS a result OBLR has deveIOped resistance to OP

21

in~

01

Fe

di~

l9

t‘ni

ha

1m

111‘:

an

3P

M:

I'CC

let

“'6

beg

(D.

am

191

DU
B

ri

 

insecticides in Canada, New York and Michigan (Reissig et al. 1986, Smirle et al. 1998,
Gut et al. 1998). Alternative methods for OBLR control are actively being developed as
OP’S are being slowly phased out as a result of the Environmental Protection Agency’s
Food Quality Protection Act (1996). These methods include pheromone mating
disruption (Gut et al. 1999), microbial insecticides (Bacillus thuringiensis or Bt) (Li et al.
1995), and insect growth regulators (Sun et al. 2000). In addition, summer pruning and
thinning of apples (Lawson et al. 1998) as well as biological control (Viggiani 2000)
have been explored.

Reduction of broad-Spectrum insecticide use in orchards should result in an
increase in natural enemy populations. In the absence of these toxic materials, parasitoids
are known to cause signiﬁcant mortality in OBLR populations (Pfannenstiel et al. 1998)
and have the potential to become a Signiﬁcant form of control of OBLR in Michigan
apple orchards. Ho (1996) was the ﬁrst to survey the parasitoids attacking OBLR in
Michigan. However, he was unable to collect large numbers of OBLR and therefore
recovered only parasitoids from two Hymenopteran families, Braconidae and
Ic‘hnuemonidae, and one Dipteran family, Tachinidae. None of the parasitoids recovered
were identiﬁed to Species. More fruitful surveys of the parasitoids attacking OBLR have
been conducted in apple orchards, raspberry ﬁelds, and in wild host vegetation in Canada
(Donganlar and Beime 1978, Hagley and Barber 1991, Li et al. 1999, Vakenti et al. 2001)
and production areas in the US. (Pogue 1985, Biddinger et al. 1994, Brunner 1996, Ho
1996). Li et a1. (1999) recovered 13 Hymenopteran species, 11 from larvae and 2 from
pupae, and 1 Dipteran Species from pupae of OBLR collected from raspberry ﬁelds in

British Columbia, Canada. Vakenti et al. (2001) recovered l8 parasitoid species from

22

 

 

 

OI:

im:

fOL

1110

par

 

IIUI

art;

313;

OBLR collected from wild host plants. OBLR collected from unmanaged apple orchards
in Ontario, Canada, were parasitized by 16 parasitoid Species, 14 Hymenoptera and 2
Diptera (Hagley and Barber 1991). Donganlar and Beime (1978) recovered 9 Species of
parasitoid from OBLR in apple orchards in the Vancouver district of British Columbia,
Canada. OBLR are also routinely collected and assessed for parasitism in the state of
Washington (Brunner 1996). Pogue (1985) reared 11 hymenopterous parasitoids from
OBLR and two other leafroller pests, Archips argyrospilus (Walker) and Anacampsis
innocuella (Zeller), collected from Shelterbelts in Wyoming. Biddinger et al. (1994)
found that OBLR maybe an alternate host for parasitoids that attack the tufted apple bud
moth, Platynota idaeusalis (Walker) in Pennsylvania orchards. Though many of the same
parasitoids were recovered from OBLR in the surveys cited above there were differences
in the species that made up the largest percentage of the parasitoid complex as well as in
numbers recovered from OBLR.

The objective of this study was to complete a two year survey of the parasitoids
attacking OBLR in commercially sprayed Michigan apple orchards in two of the largest
apple producing regions of the state. The results of the survey will be used to determine
Species occurrence, abundance, and impact of OBLR parasitoids in these regions and to
assess the potential for biological control of OBLR in Michigan.

Methods

During the 1999 and 2000 growing seasons, parasitoids attacking OBLR were
surveyed in commercially sprayed apple orchards located in two main apple producing
regions of Michigan (Fruit Ridge and Southwest). The Fruit Ridge region is comprised of

ca. 15,000 acres (Kleweno and Matthews 2001) of orchard in Kent, Ottawa, and

23

Montcalm counties (Figure 2.1). The Southwest region refers to suite of ca. 11,000 acres
(Kleweno and Matthews 2001) of orchards located in Van Buren and Berrien counties
(Figure 2.1). Data from the Allegan County orchard was included with that from orchards
located in the Fruit Ridge region during 1999 (Figure 2.1). In all locations, parasitoids
were surveyed by collecting overwintering generation and ﬁrst generation OBLR larvae
from orchards once per week and rearing on artiﬁcial diet until an adult OBLR or
parasitoid emerged, or the host died.

OBLR were collected from a total of 15 orchards in 5 counties during 1999 and
10 orchards in 4 counties during 2000 (Table 2.1). Orchard blocks within each orchard
where OBLR were collected were chosen based on OBLR population pressure the
previous year as well as by preliminary observation of large numbers of OBLR shelters in
the collection year. Blocks in each orchard, therefore, varied in size, variety, and
management Strategy. The number of blocks sampled per orchard for both the
overwintering and ﬁrst generations of OBLR in 1999 and 2000 are given in Table 2.1.
Overwintering generation OBLR were sampled until the beginning of the ﬁrst ﬂight of
adult OBLR and ﬁrst generation OBLR were sampled until the second ﬂight of adult
OBLR. During 1999 the overwintering and ﬁrst generation OBLR larvae were sampled
from May 21 until June 10 and from July 6 until August 12 respectively (Table 2.1).
Overwintering and ﬁrst generation OBLR larvae were sampled during 2000 from May 24
until June 8 and from July 12 until August 17 respectively (Table 2.1).

OBLR were sampled each week by a crew of four to ﬁve individuals. Each person
was assigned a row according to the size of the block being surveyed and was equipped

with a pole pruner that extended to 3.048 m (ARS Company, Japan), 1 oz. diet cups with

24

 

 

i1

\\

Vt

101

 

the

Phi

 

lids, and a zip lock bag. Rows were selected to Space sampling over the entire block.
Crew members walked Slowly while visually searching for OBLR shelters in the interior
and exterior of the apple canopy, searching both the upper and lower half of the tree. Pole
pruners were used to clip branches and remove Shelters that were high in the tree canopy.
OBLR shelters were individually examined and those containing larvae were placed
individually into cups and the lids were marked with the row number and height (upper
or the lower half of the tree canopy). Cups were then placed within a zip lock bag, which
was labeled with the orchard name, block name, and date. The length of time spent
searching for OBLR depended on the number of samplers and the abundance of OBLR
within a block. In order to ensure a uniform sampling effort, all samples were based on 2
person hours/block; i.e. the total time Spent searching in each block by individual
samplers equaled two hours. In addition, the sampling method sought to ensure that at
least 30 larvae were collected per sample. Blocks that were unlikely to yield this
minimum sample Size were quickly eliminated from sampling by the following
procedure. Each block was initially sampled for 10 minutes at which point the crew
leader would determine the total number of Shelters collected. If the rate of shelter
collection fell below the minimum required to achieve a total sample Size of 30 shelters
in 2 person hours further collection from the block was terminated. In this way a decision
to terminate or continue the search could be made within the ﬁrst 10 minutes, increasing
the numbers of productive blocks sampled. Bags containing the cups with larvae were
placed in a cooler with ice packs and taken to the USDA APHIS Niles Plant Protection

Center, Niles, Michigan where APHIS staff reared OBLR on a modiﬁed pinto bean diet

25

(Shorey and Hale 1965) in the laboratory at 26°C, 60% RH, and 16 Light (L): 8 Dark (D)
until the emergence of an adult OBLR or parasitoid.
Parasitoid Identification

Parasitoids were identiﬁed to species by comparison with Specimens in the A.J.
Cook Arthropod Museum at Michigan State University, East Lansing, Michigan and
continued by specialists in particular taxa. Host and hymenopteran parasitoid records
were found in Krombein et al. (1979) and updated Species names in Poole (1996).
Unknown specimens were sent to K. Ahlstrom (Braconidae), NCDA & CS Plant
Protection Section, Raleigh, North Carolina; J. O’Hara (Tachinidae) ECORC, Systematic
Entomology Section, Ontario, Canada; M.J. Sharkey (Braconidae), University of
Kentucky, Lexington, Kentucky; M. E. Schauff (Eulophidae), Systematic Entomology
Laboratory, Washington DC, Maryland; and RM. Marsh (Braconidae), Systematic
Entomology Laboratory, Washington DC, Maryland. Voucher specimens have been
deposited in the A.J. Cook Arthropod Museum at Michigan State University, East
Lansing, Michigan and at the Niles Plant Protection Center, Niles, Michigan. Specimens
were also left with each of the systematists that made the identiﬁcations. Specimens that
are in the process of being identiﬁed by specialists will be deposited as vouchers in the
A.J. Cook Arthropod Museum at Michigan State University at a later date. Specimens
that were lost or damaged have either been identiﬁed to family or have been described as
unknowns, parasitoids that never developed into adults are also described as unknowns.
Statistical Analysis

To test the hypothesis that percent parasitism was independent of the position in

the tree where larvae were collected, 1 compared the number of parasitized and

26

unparasiti /'_
Chi-Squar.
Results
Du
collected v
and the per
the Southxt
1999 11‘}
3 Q of the
489 oxem
first gener.
Per
in the 501“
(Table 2,3J

Orchards ir

 

1999 (Tabl
O‘Chmds i .
(Table 24,
OTChardS ir
(Table 2.4

Nu
orchardS ir

YEgion in 1

unparasitized OBLR that were collected either high or low in the tree canopy by Pearson
Chi-Square Test (SAS 2000). The exact P-value for each comparison is reported.
Results

During the course of this two-year study a total of 9,044 OBLR larvae were
collected of which 2,229 were parasitized (Table 2.2). The number of OBLR collected
and the percent parasitism increased from the overwintering to ﬁrst generations in both
the Southwest and Fruit Ridge/Allegan regions during 1999 and 2000 (Table 2.2). In
1999 11% of the 1,126 overwintering generation OBLR collected were parasitized, while
29% of the 3,749 ﬁrst generation OBLR collected were parasitized. In 2000 8% of the
489 overwintering generation OBLR collected were parasitized, while 26% of the 3,680
ﬁrst generation OBLR collected were parasitized.

Percent parasitism of overwintering OBLR ranged from 4% to 23% for orchards
in the Southwest and from 1% to 11% in the Fruit Ridge/Allegan region during 1999
(Table 2.3). Percent parasitism of ﬁrst generation OBLR ranged from 8% to 52% for
orchards in the Southwest and from 10% to 81% in the Fruit Ridge/Allegan region during
1999 (Table 2.3). Percent parasitism of overwintering OBLR ranged from 0% to 25% for
orchards in the Southwest and from 0% to 29% in the Fruit Ridge region during 2000
(Table 2.4). Percent parasitism of ﬁrst generation OBLR ranged from 5% to 29% for
orchards in the Southwest and from 24% to 52% in the Fruit Ridge region during 2000
(Table 2.4).

Numbers of parasitoid species attacking OBLR also varied considerably between
orchards in both regions and years (Tables 2.5 — 2.8). For example in the Southwest

region in 1999 a Single Species was recovered from overwintering OBLR larvae in Kugel

27

orchard “ if
orchiird {Ti
generalik’n
R. \k'inkel I
from 0V?”
Southuest (
in a single }
orchard> 1“
App:
oxem'interii
scren famili
hyperparasit-
H}'men0pter.
Duri|
the total para
region follov
[toplectis (‘01
region during

Oi'ent'interih

 

59} 0f the lot
regions 8. d;

attacking ﬁr.

 

 

orchard while approximately 9 species were recovered from larvae in Calderwood
orchard (Table 2.5). Approximately 2 Species of parasitoid were recovered from ﬁrst
generation OBLR in Page] orchard while approximately 6 Species were recovered from
R. Winkel orchard during 1999 (Table 2.5). Numbers of parasitoid Species recovered
from overwintering and ﬁrst generation OBLR also varied between orchards in the
Southwest during 2000 (Table 2.6). The greatest number of parasitoid species recovered
in a Single year, 12, was recorded for ﬁrst generation collections of OBLR in R. Winkle
orchards in 2000 (Table 2.6).

Approximately 14 Species of parasitoids from 6 families were recovered from
overwintering and ﬁrst generation OBLR during 1999 (Table 2.9) and 19 species from
seven families were recovered from OBLR during 2000 one of which was a Tachinid
hyperparasitoid (Table 2.10). The parasitoid community was composed of Dipteran and
Hymenopteran parasitoids.

During 1999, Bassus dimidiator (Nees.) made up the largest percentage (53%) of
the total parasitoid complex attacking overwintering generation OBLR in the Southwest
region followed by the Tachinidae (23%), Macrocentrus linearis (Nees.) (12%),
Itoplectis conquisitor (Say) (6%) and the unknowns (6%) (Figure 2.2). In the Fruit Ridge
region during 1999 the Tachinidae made up 75% of the total parasitoid complex attacking
overwintering generation OBLR, B. dimidiator made up 20% and I. conquisitor made up
5% of the total (Figure 2.2). During 1999 in both the Southwest and Fruit Ridge/Allegan
regions B. dimidiator made up 65% and 46% respectively of the parasitoid complex

attacking ﬁrst generation OBLR, Tachinidae made up 25% and 46% respectively, while

28

meunkn0\
6‘? of the 1
Du:

largest pert
tFi‘gure 3.4
oxeru interi
were .11. [In
In the Fruit
was unknov
the SQUID“:
I??? C. flan
generation C
15% B. dimrl
C0mPOsed of
and 0% of [he
and Years in‘
There

and ﬁISi gen:
A”6.91m regit

llllt’rrupm Cl

 

 

complex and

 

the unknowns made up 9% in the Southwest and Colpoclypeusﬂorus Walker made up
6% Of the parasitoid complex in the Fruit Ridge region (Figure 2.3).

During 2000 in the Southwest and Fruit Ridge regions B. dimidiator made up the
largest percentage (38% and 96% respectively) of species attacking overwintering OBLR
(Figure 2.4). In the Southwest region during 2000, 23% of the total complex attacking
overwintering generation OBLR was composed of Enytus sp., 15% were unknown, 8%
were M. linearis, 8% Apanteles polychrosidis Viereck, and 8% Tachinidae (Figure 2.4).
In the Fruit Ridge region during 2000, 4% of the complex attacking overwintering OBLR
was unknown (Figure 2.4). The parasitoid complex attacking ﬁrst generation OBLR in
the Southwest region during 2000 was composed of 51% B. dimidiator, 20% Tachinidae,
17% C. ﬂorus, and 12% unknown (Figure 2.5). The parasitoid complex attacking ﬁrst
generation OBLR in the Fruit Ridge region in 2000 was composed of 70% Tachinidae,
15% B. dimidiator, 10% C. ﬂorus, and 5% unknown (Figure 2.5). The unknowns are
composed of parasitoids that made up less than 5% of the parasitoid complex (species ID
and % of the total complex are given for these parasitoids for both, generations, regions
and years in Table 2.11), and those that were nonviable or unidentiﬁable.

There were a total of 5 identiﬁed species of Tachinidae attacking overwintering
and ﬁrst generation OBLR during 1999 and 2000 in the Southwest and FruitRidge/
Allegan regions of Michigan (Table 2.12). The Tachinids Nilea erecta (Coquillet), Actia
interrupta Curran, Hemistrumia parva (Bigot), Hyphantrophaga blanda (Osten Sacken),
and Compsilura concinnata (Meigen) ranged between 30% of the Tachinidae total
complex and 0.32% during 1999 and 2000 (Table 2.12). Unknown Tachinids made up

between 22% and 100% of the total Tachinidae complex attacking overwintering and ﬁrst

29

generatit

regions I

or were I

F

high or It
oreminte
orchards l
1999 and L
lan'ae in h
canop} for

greater par;

no Significant

§€neration 0

 

 

generation OBLR during 1999 and 2000 in the Southwest and Fruit Ridge/Allegan
regions (Table 2.12). Unknown Tachinidae were Specimens that had been lost, damaged,
or were non-viable.

Figure 2.6 shows the percent parasitism of OBLR that were collected from either
high or low in the apple tree canopy. Numbers of un-parasitized and parasitized
overwintering and ﬁrst generation OBLR collected high and low in the tree canopy from
orchards located in the Fruit Ridge/Allegan) and Southwest regions of Michigan during
1999 and 2000 can be seen in Table 2.13. Comparisons of parasitized and un-parasitized
larvae in high vs. low samples reveled Signiﬁcant differences in these positions in the tree
canopy for both overwintering and ﬁrst generation OBLR. During 1999 in the Southwest
greater parasitism of overwintering generation OBLR was found high in the tree
(x2=7.5928, dﬁl, P=0.0067) and greater parasitism of ﬁrst generation OBLR was also
found to occur high in the tree (x =5.8694, df=1, P=0.0170) (Figure 2.6 and Table 2.13).
In the Fruit Ridge/Allegan region during 1999 there were no signiﬁcant differences in the
overwintering generation of OBLR parasitized high or low in the tree (x2=0. 1813, df=1,
P=0.8168) however, there were signiﬁcantly more ﬁrst generation OBLR parasitized low
in the tree canopy (x2=4.5996, df=1, P=0.0326) (Figure 2.6 and Table 2.13). There were
no Signiﬁcant differences in parasitized and un-parasitized overwintering and ﬁrst
generation OBLR collected either high or low in apple trees during 2000 from orchards in
the Southwest region of Michigan (x =0.0822, df=1, P=0.7826, and x2=0.0625, df=1,
P=0.8070 respectively) (Figure 2.6 and Table 2.13). There were no signiﬁcant differences
in parasitized and un-parasitized overwintering and ﬁrst generation OBLR collected

either high or low in apple trees during 2000 from orchards in the Fruit Ridge region of

30

Micki
(Fjgt'Jf

Discus

generaL
Bit‘ilogit
and the r
differene
increase i
parasitoid
esfem'aler
leafrollers.
leafroller c
used routin.
(Linnaeus),
Summer as l
ami'IOI'Ora. (
acres of ﬁppi
aanUnI Of P;

 

abandOIlEd t

 

landSC‘ape S i

Michigan (1 =0.0044, df=l, P=1.0000, and x =0.000005, df=l, P=l.0000 respectively)
(Figure 2.6 and Table 2.13).
Discussion

Percent parasitism was lower for the overwintering generation than the ﬁrst
generation in both the Southwest and Fruit Ridge/Allegan regions in 1999 and 2000.
Biological factors that could account for the differences in numbers of OBLR collected
and the percent parasitism between the overwintering and ﬁrst generation are seasonal
differences in temperature, natural overwintering mortality of host and parasitoid, and an
increase in activity as temperatures increase. Insecticide use patterns may have impacted
parasitoids as well. In most locations, broadly toxic materials such as chlorpyrifos and
esfenvalerate were applied early in the season for control of aphids, leafminers, and
leafrollers. More selective insecticides such as tebufenozide and spinosad were used for
leafroller control beginning at petal fall. The organophosphate, azinphos-methyl, was
used routinely throughout the season for control of codling moth, Cydia pomonella
(Linnaeus), or apple maggot, Rhagoletis pomonella (Walsh), but tapered Off later in the
summer as harvest approached. Also during 2000 there was a severe ﬁre blight, Erwinia
amylovora, outbreak in Michigan apple orchards resulting in the loss of thousands of
acres of apple and many growers discontinued spraying for the season. Differences in the
amount of parasitism between orchards could also have been due to the differences in the
surrounding landscapes where some orchards may have been bordered by woods,
abandoned orchard, or another working orchard. Orchards that have a more diverse

landscape should have a greater number of natural enemies (Root 1973) as a result of a

31

greater an
resources :
Ma
orchards \\
(Pogue 19’
the major e
Hjmenopte
SOUIINCxl :
dimidiutor I
3.5). This 0
Bassus dimi.
attack the e}
(Krombein e
Dondale ('19.
Tach

OBLR in Mi

being the ma

 

inlt’l'rupm W
Barber 1991

blandatiost

 

 

SOUthwest a;

 

greater amount of non- crop vegetation supporting alternate hosts, and providing ﬂoral
resources for parasitoids to feed upon.

Many of the parasitoid species recovered from OBLR collected in Michigan apple
orchards were the same as those found to parasitize OBLR throughout North America
(Pogue 1985, Hagley and Barber 1991, Biddinger et al. 1994, Li et al. 1999). However
the major exception was that, B. dimidiator was the most consistently abundant
Hymenopteran parasitoid attacking overwintering and ﬁrst generation OBLR in both the
Southwest and Fruit Ridge/Allegan regions of the state during 1999 and 2000. Bassus
dimidiator made up 15% to 96% of the parasitoids attacking OBLR (Figure 2.2 — Figure
2.5). This OBLR survey represents a new host record for this highly abundant species.
Bassus dimidiator is a solitary endoparasitoid that had previously been only reported to
attack the eye-spotted bud moth, Spilonota ocellana (Denis and Schifferrnuller)
(Krombein et a1. 1979). The complete biology of B. dimidiator has been described by
Dondale (1954) under the name Agathis laticinctus (Cresson).

Tachinids were the second most consistently abundant parasitoids attacking
OBLR in Michigan apple orchards. Nilea erecta and A. interrupta followed by H. parva
being the major Species recovered (Table 2.12). The Tachinidae N. erecta and A.
interrupta were also recovered from OBLR in other parasitoid surveys (Hagley and
Barber 1991, Biddinger et al. 1994). Two specimens of the Tachinid Hyphantrophaga
blanda (Osten Sacken) were reared each from a ﬁrst generation OBLR collected in the
Southwest and Fruit Ridge regions during 2000 (Table 2.12). Hyphantrophaga blanda
has been reported only one other time to have been reared in OBLR in British Columbia,

Canada (Personal Communication Dr. J. O’Hara). Two Specimens of the widely known

32

 

generali~
OVCF“ llllt
Michigar
States as
the :1) P‘.‘
factor fro.
pret‘ioml)
T
also found
released in
li'ashingto
over 90C} I
ﬂoms was ;
0V6m'interi
ﬂonts '3 3b,,
suitable Ore:

  
   
  

leaves the or
later in the _\
Parasitoid c. '
SOUlhweSI 11'

[he Fm” thi

 

generalist Tachinidae, Compsilura concinnata (Meigen) were also recovered from
overwintering and ﬁrst generation OBLR collected from the Southwest region Of
Michigan during 1999 and 2000. Compsilura concinnata was introduced into the United
States as a biological control of various Lepidopteran pests from 1906 to 1986 especially
the gypsy moth, Lymantria dispar (L.), and has since been found to be a major mortality
factor from many non-target Lepidopteran communities (Boettner et al. 2000). It was not
previously known to attack OBLR (Amaud 1978)

The gregarious ectoparasitoid, Colpoclypeusﬂorus Walker (Eulophidae) was
also found in Michigan apple orchards for the ﬁrst time. Colpoclypeusﬂorus was
released into Ontario Canada in the 1960’s and was found for the ﬁrst time in
Washington orchards in 1992 (Brunner 1996). Colpoclypeus ﬂorus has contributed to
over 90% parasitism of leafrollers in Washington (Pfannenstiel et al. 2000). Colpoclypeus
ﬂorus was absent in both the Southwest and Fruit Ridge regions of Michigan during the
overwintering generation but was present during the ﬁrst generation. The reason for C.
ﬂorus’s absence during the overwintering generation is probably due to the lack of a
suitable overwintering host within the orchard. Because C. ﬂorus requires a late instar
host for overwintering while OBLR overwinters as a 2nd or 3rd instar, C. ﬂorus probably
leaves the orchard in search of a suitable overwintering host and does not return until
later in the season (Gruys and Vaal 1984, Dijkstra 1986). The percent composition of the
parasitoid complex composed of C. ﬂorus increased from 2% (Table 2.11) in the
Southwest in 1999 to 17 % in 2000 (Figure 2.5), and increased from 6% (Figure 2.3) in

the Fruit Ridge/Allegan region in 1999 to 10% in 2000 (Figure 2.5).

33

{55m 6;
and 31."-
attuckir
2.41. .1];
generati.
.lluc'rtit‘e
Ridge; .~\l
during 19
T."
high or 10‘
searching l
011 new grg
found hi gh
ai‘ailahility.
numbers of
10 a reductio
C0nclnsion
A Co

generation (

 

\IlChlgan 'I
Parasitode a

”WWII. Tht

 

A polyembryonic endoparasitoid, Macrocentrus linearis (Nees.) was also
recovered from overwintering and ﬁrst generation OBLR in the Southwest region in 1999
and 2000. In the Southwest M. linearis made up 12% of the total parasitoid complex
attacking overwintering generation OBLR in 1999 (Figure 2.2) and 8% in 2000 (Figure
2.4). Macrocenrrus linearis made up 4% of the parasitoids complex attacking ﬁrst
generation OBLR in the Southwest in 1999 and 0.56% in 2000 (Table 2.11).
Macrocentrus linearis were found to emerge from two ﬁrst generation OBLR in the Fruit
Ridge/Allegan region (Table 2.9) making up only 0.43% of the total parasitoid complex
during 1999 (Table 2.11).

The differences in the number of parasitized and un-parasitized OBLR collected
high or low in the apple tree could possibly be due to the differences in parasitoid
searching behavior or the pattern of OBLR dispersal into the tree. OBLR prefer to feed
on new growth and move throughout the tree during the season. Waldstein et.al. (2001)
found high rates of larval movement which may have been inﬂuenced by foliage
availability. Orchards where ﬁre blight was present in 2000 may have inﬂuenced the
numbers of OBLR that were collected from high or low in the tree during our study due
to a reduction in suitable foliage for feeding.

Conclusion

A complex of parasitoids are contributing to the control of overwintering and ﬁrst
generation OBLR in apple orchards in the Southwest and Fruit Ridge regions of
Michigan. The parasitoids B. dimidiator and the Tachinids were the most abundant
parasitoids attacking OBLR in Michigan apple orchards, followed by C. ﬂorus, and M.

linearis. There appears to be considerable potential for biological control agents to

34

contribute to
Jimidiutur Lil
used for OBI
could allou .
of controllin
should be m:
attacking fir~
ﬂoms on the
should also i
abundant th'.
Michigan or
control in M
their use \\ i1

these materi

 

 

contribute to the control of OBLR in Michigan however, studies have shown that both B.
dimidiator and M. linearis are susceptible to many of the common insecticide chernistries
used for OBLR control in Michigan (Chapter 3). Reducing the use of harmful insecticides
could allow parasitoids such as B. dimidiator and the Tachinidae to become a major form
of controlling OBLR populations in commercial apple orchards. The parasitoid C. ﬂorus
Should be monitored further to see if C. ﬂorus will become the most abundant parasitoid
attacking ﬁrst generation OBLR. The effects of the increases in the population of C.
ﬂorus on the populations of B. dimidiator and the Tachinidae Compsilura concinnata
Should also be monitored to determine if this generalist parasitoid will become more
abundant than the major Hymenopteran parasitoids currently attacking OBLR in
Michigan orchards. The effects of the new more selective insecticides used for OBLR
control in Michigan apple orchards Should be tested on natural enemies to ensure that
their use will not affect biological control of OBLR in the apple orchards managed with

these materials.

35

 

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References

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Boettner, G.H., J .S. Elkinton, and CJ. Boettner. 2000. Effects of a biological control
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Brunner, J .F. 1996. Discovery of Colpoclypeusﬂorus (Walker) (Hymenoptera:
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Hagley, E.A.C., and DR. Barber. 1991. Foliage-feeding Lepidoptera and their parasites
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Ho, H.L. 1996. Mating disruption if the leafroller complex (Lepidoptera: Tortricidae) in

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thesis, Michigan State University, Michigan.

66

Howitt, AH. 1993. Common tree fruit pests. Michigan State University Extension, NCR
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Kleweno, DD, and V. Matthews. 2001. Michigan agricultural statistics 2000-2001.
Michigan Department of Agriculture 2000 Annual Report. Michigan Department of
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Kleweno, DD, and V. Matthews. 2001. Michigan Rotational Survey; Fruit Inventory
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Krombein, K.V., P.D. Hurd Jr., D.R. Smith, and B.D. Burks. 1979. Catalog of
Hymenoptera in America north of Mexico. Smithsonian Institute Press Washington DC.
Volume I.

Lawson, D.S., W.H. Reissig, and A.M. Agnello. 1998. Effects of summer pruning and
hand fruit thinning on obliquebanded leafroller (Lepidoptera: Tortricidae) fruit damage in
New York State apple orchards. J. Agric. Entomol. 15: 113-123.

Li, S.Y., S.M. Fitzpatrick, and MB. Isman. 1995. Suseptibility of different instars of the
obliquebanded leafroller (Lepidoptera: Tortricidae) to Bacillis thuringiensis var. kurstaki.
J. Econ. Entomol. 88:610-614.

Li, S.Y., S.M. Fitzpatrick, J .T. Troubridge, M.J. Sharkey, J .R. Barron, and J.E.
O’Hara.l999. Parasitoids reared from the obliquebanded leafroller (Lepidoptera:
Tortricidae) infesting raspberries. Can. Entomol. 131: 399-404.

Madsen, H.F., J .M. Vakenti, and AP. Gaunce.1984. Distribution and ﬂight activity of
obliquebanded and threelined leafrollers (Lepidoptera: Tortricidae) in the Okanagan and
Similkameen valleys of British Columbia. Can. Entomol. 116: 1659-1664.

Ohlendorf, B.L.P. 1999. Integrated pest management for apples and pears. 2"d ed.
Statewide Integrated Pest Management Project, University of California Division of
Agriculture and Natural Resources Publication 3340.

Pfannenstiel, R.S., J .F. Brunner, and MD. Doerr. 1998. Biological control of leafrollers.
Wash. State Hort. Assoc. 91: 253-256.

Pfannenstiel, R.S., T.R. Unruh, and J .F. Brunner. 2000. Biological control of leafrollers:
Prospects using habitat manipulation. Wash. State Hort. Assoc. 95: 144-149.

Pogue, MG. 1985. Parasite complex of Archips argyrospilus, Choristoneura rosaceana

(Lepidoptera: Tortricidae) and Anacampsis innocuella (Lepidoptera: Gelechiidae) in
Wyoming Shelterbelts. Entomol. News. 96: 83-86.

67

Poole, R.W, and P. Gentili. 1996. Nomina insecta nearctica, A checklist of the insects of
North America, Volume 2, Hymenoptera, Mecoptera, Megaloptera, Neuroptera,
Raphidioptera, Trichoptera. Entomol. Info. Service, Rockville MD.

Reissig, W.H. 1978. Biology and control of the obliquebanded leafroller on apples. J.
Econ. Entomol. 71: 804-809.

Reissig, W.H., B.H. Stanley, and HE. Hebding. 1986. Aziphosmethyl resistance and
weight-related response of obliquebanded leafroller (Lepidoptera: Tortricidae) larvae to
insecticides. J. Econ. Entomol. 79: 329-333.

Root, RB. 1973. Organization of a plant-arthropod association in simple and diverse
habitats: The fauna of collards (Brassica oleracea). Ecol. Monographs. 43: 95-124.

Shorey, H.H., and R.L. Hale. 1965. Mass-rearing of the larvae of nine Noctuid species on
a simple artiﬁcial medium. J. Econ. Entomol. 58: 522-524.

Smirle, M.J., C. Vincent, C.L. Zurowski, and B. Rancourt. 1998. Aziphosmethyl
resistance in the obliquebanded leafroller, Choristoneura rosaceana : Reversion in the

absence of selection and relationship to detoxication enzyme activity. Pest. BioChem.
And Physiol. 61: 183-189.

Sun, X., BA. Barrett, and DJ. Biddinger. 2000. Fecundity and fertility reductions on
adult leafrollers ecposed to surfaces treated with the ecdysteroid agonists tebufenozide
and methoxyfenozide. Entomol. Exp. Appl. 94: 75-83.

Vakenti, J .M., J .E. Cossentine, B.E. Cooper, M.J. Sharkey, C.M. Yoshimoto, and L.B.M.

Jensen. 2001. Host-plant range and parasitoids of obliquebanded and three-lined
leafrollers (Lepidoptera: Tortricidae). Can. Entomol. 133: 139- 146.

Viggiani, G. 2000. The role of parasitic hymenoptera in integrated pest management in
fruit orchards. Crop Protection. 19: 665-668.

Waldstein, D.E., W.H. Reissig, and J .P. Nyrop. 2001. Larval movement and its potential

impact on the management of the obliquebanded leafroller (Lepidoptera: Tortricidae).
Can. Entomol. 133: 687-696.

68

Chapter 3

The direct effects of five insecticides on survival of Bassus dimidiator (Nees.) and
Macrocentrus linearis (Nees.) (Hymenoptera: Braconidae), parasitoids of the
obliquebanded leafroller, Choristoneura rosaceana (Harris) (Lepidoptera:
Tortricidae).

Abstract

The obliquebanded leafroller (OBLR), Choristoneura rosaceana (Harris), has
become a major pest in Michigan apple production due to its resistance to
organophosphate insecticides. New alternative insecticides are being developed for
OBLR control, inﬂuenced by the development of resistance and the increasing restriction
being implemented as a result of the Environmental Protection Agency’s Food Quality
Protection Act. Many, but not all of the new insecticides are selective and less harmful
for natural enemies. If a grower wants to conserve natural enemies present in the orchard
it is important to know which insecticides should be avoided when parasitoids are
present. The International Organization of Biological Control (IOBC) has developed
standard methods for testing the effects of insecticides on natural enemies. Insecticide
bioassays based on IOBC standards were conducted to test the effects of the residues of
formulated product of ﬁve insecticides on two important Braconid parasitoids of OBLR
in Michigan apple orchards, Bassus dimidiator (Nees.) and Macrocentrus linearis
(Nees.). The insecticides methoxyfenozide (Intrepidm), esfenvalerate (Asana®),
imidacloprid (Provado®), spinosad (SpinTorm), and azinphos-methyl (Guthion®) were
chosen to represent a range of broad-spectrum and selective chemistries. Insecticides and

a water control were sprayed onto Petri dishes or apple leaves. Methoxyfenozide caused

no change in survival of both parasitoids, while azinphos—methyl was highly toxic to

69

both species. Based on the level of toxicity azinphos-methyl should not be used in an

IPM program that integrates biological control. Imidacloprid, esfenvalerate, and spinosad
were moderately to highly toxic depending on the surface that was sprayed. The utility of
moderately toxic insecticides for control of OBLR in times of parasitoid inactivity should

be studied further.

70

Introduction

The obliquebanded leafroller (OBLR), Choristoneura rosaceana (Harris), is one
of the most serious pests in Michigan apple production (Gut et al. 1999). Larvae feed on
leaves, the developing fruit, ﬂower buds, and water sprouts (Reissi g 1978, Howitt 1993,
Ohlendorf 1999). Fruit injury caused by overwintering larvae early in the season is
characterized by deep scars while injury caused during the summer can be recognized by
shallow feeding scars (Madsen et al. 1984, Howitt 1993, Ohlendorf 1999). .Much of the
young developing fruit that is damaged by overwintering OBLR drops from the tree as
larval feeding interferes with normal fruit development (Reissig 1978, Howitt 1993,
Ohlendorf 1999). The greatest damage to fruit occurs after petal fall as fruit increases in
size (Reissig 1978, Howitt 1993). Larval feeding by ﬁrst generation OBLR has been
known to cause more than 15% damage to harvested fruit (Ho 1996).

The presence of OBLR larvae in the apple tree canopy can be easily detected by
the presence of their leaf shelters. Shelters are created by the larvae folding over a leaf
and binding it with silk. Larvae will also bind several leaves together or to nearby fruit
and feed within the safety of the shelter (Howitt 1993, Ohlendorf 1999). OBLR
completes two generations per year in Michigan with ﬁrst adult ﬂight occurring in late
June to early July and second adult ﬂight occurring late August (Howitt 1993). Second
generation OBLR larvae overwinter as 2nd or 3rd instars emerging from their
overwintering hibemacula in late April to early May (Howitt 1993).

For more than 40 years OBLR had been controlled using broad-spectrum

organophosphate (OPS) and carbamate insecticides in United States apple production

71

(Gut et al. 1999). However, OBLR resistance to OPs became evident in Michigan during
the 1970’s (Howitt 1993). More recent bioassay experiments with populations of OBLR

from Michigan apple orchards have determined that OBLR is 21x resistant to Guthion®
(azinphos-methyl) and 7x resistant to Lorsban® (chlorpyrifos) (Gut et al. 1998). Ahmad

et al. (2002) found 27x resistance at LC50 for azinphos-methyl and 26x resistance at LC50
for chlorpyrifos. OBLR resistance to CPS along with the growing restrictions on use or
the total loss of registered OPs as a result of the Environmental Protection Agency’s Food
Quality Protection Act (1996) has led to the development of alternative methods for
controlling OBLR. New methods include the use of insect growth regulators (Sun et al.
2000), microbial insecticides (Bacillus thuringiensis or Bt) (Li et al. 1995), pheromone
mating disruption (Gut et al. 1999), and biological control (Vigianni 2000).

Gut et al. (1999) also discuss some newer insecticides available for OBLR control
and their effectiveness. Azinphos-methyl (Guthion®) is a broad-spectrum
organophosphate insecticide with strong contact activity that acts via cholinesterase
inhibition causing insects to lose control of their nervous function (Ware 1994). Unlike
azinphos-methyl, and esfenvaletrate (Asana®), that are strong contact poisons, many of
the new selective insecticides including methoxyfenozide (Intrepidm), spinosad
(SpinTorm), and imidacloprid (Provado®) must be ingested to kill the target insect.
Esfenvalerate, is a pyrethroid insecticide and also affects insect nervous function , but in
a different manner than azinphos-methyl (Ware 1994). Methoxyfenozide, is an
ecdysteroid antagonist which interferes with the molting process of insect larvae and has
been found to be an effective control for Lepidoteran larvae but has low impact on non-

target organisms (Carlson et al. 2001). Spinosad, is a metabolite of the soil actinomycete,

72

Saccharopolyspora spinosa (Mertz and Yoa), which when ingested by the target insect
cause the loss of nervous function (Thompson et al. 2000). Imidacloprid, is a
neonicotinoid insecticide that is absorbed into the plant it is sprayed onto (Wise et al.
2002) and also interferes with insect’s nervous function once its ingested (Gut et al.
1999). Irnidacloprid is generally targeted at Homoptera.

With a reduction in use of broad-spectrum insecticides and greater reliance on
newer more selective insecticides for orchard pest control, natural enemy populations
may increase and become a more signiﬁcant mortality factor for OBLR populations.
However, some insecticides that are promoted based on apparent selectivity, such as
spinosad, have in some cases been found to be harmful to some natural enemies (Hill and
Foster 2000, Sub et al. 2000, Brunner et al. 2001, Cisneros et al. 2002, Mason et al.
2002). Successful biological control of OBLR in commercial apple orchards will
therefore depend on when and how each insecticide is incorporated into an Integrated
Pest Management (IPM) program.

The International Organization of Biological Control, West Palaearctic Regional
Section (IOBC/WPRS) working group on Pesticides and Beneﬁcial Organisms has
developed standards for testing insecticide effects on natural enemies (Hassan 1998). The
goal of the working group is to provide information on insecticides with reduced risks to
natural enemies for use in IPM programs (Hassan 1998). The methods developed by the
working group involve laboratory testing, semi-ﬁeld testing, and ﬁeld-testing of
insecticides (Hassan 1998). Testing of insecticide effects on natural enemies is required

in some European countries (Hassan 1998).

73

A survey of parasitoids attacking OBLR in Michigan apple orchards during 1999
and 2000 recovered approximately 21 species of parasitoids from 8 families of
Hymenoptera and 1 family of Diptera from OBLR (Chapter 2). Parasitism of OBLR
collected ranged from 3% up to 37% (Chapter 2). The most consistently abundant
Hymenopteran parasitoid for both 1999 and 2000 was Bassus dimidiator (Nees.)
(Braconidae) that constituted up to 96% of the total parasitoid complex attacking OBLR in
Michigan apple orchards (Chapter 2). A second Braconid parasitoid recovered from
OBLR during 1999 and 2000 was Macrocentrus linearis (Nees.) comprised up to 12% of
the total parasitoid complex attacking OBLR in Michigan apple orchards (Chapter 2).

Bassus dimidiator (Nees.) is a solitary endoparasitoid, which had previously only
been reported from the eye-spotted bud moth, Spilonota ocellana (Denis and
Schiffermuller) (Krombein et al. 1979). A complete biology of B. dimidiator is given by
Dondale (1954) under the name Agathis laticinctus (Cresson). By dissection of S. ocellana
larvae, Dondale (1954) found that B. dimidiator lays a single egg in the ventral nerve
ganglion of the host and is capable of parasitizing between 15 and 20 hosts. The larvae of
B. dimidiator feed on the host internally and pupate outside the host’s body (Dondale
1954). Macrocentrus linearis (Nees.) is a polyembryonic endoparasitoid that lays a single
egg per host, however, that egg is able to divide into multiple embryos. Li et al. (1999)
described the biology of M. nigridorsis Viereck which is similar to that of M. linearis and
other species of Macrocentrus. Li et al. (1999) found that as many as 36 parasitoids could
emerge from a single host. Macrocentrus linearis as with M. nigridorsis larvae feed inside

the host’s body and pupate on the outside of the hosts body (Li et al. 1999). The larvae of

74

M. linearis all pupate simultaneously and spin together into a silken football shaped
cocoon as does M. nigridorsis (Li et al. 1999).

Maximizing the impacts of parasitoids like B. dimidiator and M. linearis has the
potential to contribute to sustainable control of OBLR in Michigan apple orchards.
Conservation of these parasitoids requires knowledge of the impact of insecticides used
for OBLR control on these natural enemies. The objective of this study was to test the
direct effects of ﬁve of the principal insecticides currently used in Michigan apple
orchards for control of OBLR or other fruit pests on the survival and longevity of adult B.
dimidiator and M. linearis. This information could then be used to make
recommendations to improved integrated control of OBLR.

Methods

The effects of the residues from the formulated product of ﬁve insecticides
(azinphos-methyl; Guthion®, esfenvalerate; Asana®, methoxyfenozide; Intrepid“,
imidacloprid; Provado®, and spinosad; SpinTorm) currently used for control of OBLR
and other pests in apple orchards were tested on the adult parasitoids B. dimidiator and
M. linearis. Insecticides were tested at the highest recommended ﬁeld rate in order to
give the worst-case scenario on a weekly basis for 5 weeks. The methods chosen for this
study were adapted from the standard methods developed by the IOBC/ WPRS working
group, Pesticides and Beneﬁcial Organisms (Hassan 1998).

The parasitoids (B. dimidiator and M. linearis) were initially obtained from ﬁeld
collected OBLR and then reared on a laboratory colony of OBLR at the Niles,USDA,

APHIS, Plant Protection Center in Niles, Michigan. Parasitoids were reared at 26°C, 40-

60% RH, 16:8 LzD. Parasitoid cocoons were placed individually into 1 oz diet cups with

75

lids and then cups were placed into Ziploc bags and sent to Michigan State University via
overnight mail. Upon arrival cocoons were then placed into a growth chamber set at

26°C, ~ 60% RH, 16:8 L:D until adult emergence. Adults were then placed into a

screened cage and given a 25% honey solution in a 1 oz diet cup with lid, honey water
could be freely accessed by parasitoids from a cotton dental wick placed into the lid of
the diet cup. Males and females were placed into the same cage (B. dimidiator and M.
linearis were in separate cages).
Bassus dimidiator Exposed to Residues on Petri Dishes

Insecticides were mixed with distilled water and applied at their highest
recommended ﬁeld rates (Wise et al. 2002) using an auto-load Potter Spray Tower
(Burkard Scientiﬁc). Table 3.1 lists the common name, class, chemical name, and rates
for each insecticide used. Insecticides were sprayed onto the outer top and bottom of 60 x
15mm polystyrene Petri dishes (Falcon®) and were allowed to dry for 1h. Controls were
Petri dishes sprayed in the same manner with water only. A l-l.5cm wide stainless steel
mesh ring (McMaster-Carr, Aurora) was sandwiched between the two Petri dishes in
order to create a ventilated space to enclose the parasitoids. The Petri dishes and ring
were held together using two thin strips of packaging tape on either side of the arena and
a cotton dental wick soaked in 25% honey solution was placed through a hole in the top
Petri dish (Figure 3.1). Before taping the arena together a male and female parasitoid
were placed into the arena.

The B.dimidiator adults used in the study ranged in age from a few hours to a
maximum of 72h old. All parasitoids were given the opportunity to mate and feed before

being exposed to the insecticide treatments. The number of parasitoids available for the

76

experiment each week varied and resulted in the need to block the experiment by weeks.
For arena a single male and female pair were aspirated from the larger cage and placed
into the arena containing the insecticide residue. The honey water in the dental wick was
replenished each day by pipeting new solution onto the dental wick. Mortality was
assessed at 4h, 24h, 48h, and 120h. Parasitoids were reported as being alive (actively
moving) or dead (lying on their side or back and unresponsive to touch) in order to ﬁt the
assumptions of the statistical model used.
Bassus dimidiator Exposed to Residues on Leaves

To test the effect of drying time and exposure on a natural substrate, insecticides
were applied to apple leaves and allowed to dry for either lb or 24h before parasitoids
were exposed to the residues. Insecticides and water controls were applied using the same
methods when B. dimidiator was exposed to residues on Petri dishes only. The upper
surface of an entire apple leaf was sprayed. Leaf petioles were placed in water contained
in a 1 oz diet cup with each individual leaf stem placed through a hole in the lid of a 1 oz

diet cup, the water contained four drops of Floralife® Crystal ClearTM (Floralife Inc.,

Walterboro) fresh ﬂower food in order to extend the life of the leaf. Leaves were
collected from unsprayed antique and scab resistant varieties of apple trees on the
Michigan State University Collins Road Entomology Farm in East Lansing, Michigan.
Leaves were provided water throughout the entire experiment and cups were ﬁlled as
necessary. After residues were dried, leaves were ﬁxed to the bottom of a Petri dish (60 x
15mm polystyrene Falcon®) using double sided tape with the sprayed surface of the leaf
facing upwards. The stainless steel metal ring was then set on top of the leaf and a second

Petri dish was then placed on top of the ring to complete the enclosure after a male and

77

female pair of B. dimidiator was put into the arena. Securing of the arena and parasitoid
feeding was as previously described (Figure 3.2). Parasitoids ranged in age from a few
hours old up to a maximum of 48h old. The numbers of male and female parasitoids
available varied and resulted in the need to block the experiment by weeks. Mortality was
assessed at the same time intervals as in the previously described B. dimidz’ator
experiment however, additional observations were made at 72h and 96h. Parasitoids were
reported as being either alive or dead as previously explained.

For each treatment containing a leaf with insecticide residue a single Petri dish
arena was sprayed and allowed to dry either lb or 24h. Petri dishes were sprayed the
same as previously described (Figure 3.1). A single male and female pair were aspirated
from the larger cage and placed into the arena with insecticide residue. The number of
parasitoids available varied and the experiment was blocked by week. Mortality was
assessed at the same time intervals as those exposed to residues on the leaves. A 25 %
honey solution was provided via a dental wick and was replenished each day.
Macrocentrus linearis Exposed to Residues on Petri Dishes and Leaves

Leaves and Petri dishes (Figure 3.1 and Figure 3.2) were sprayed using the same
methods as in the B. dimidiator experiments and were allowed to dry for 1h or 24h before
parasitoid exposure. Parasitoids ranged in age from a few hours old up to a maximum of
48h old. A single male and female pair were aspirated from a larger cage and placed into
the arenas with leaves or those without leaves. The number of male and female M.
linearis available for the experiments varied each week resulting in blocking the
eXperiments by week. Mortality was assessed at the same time intervals described for the

B. dimidiator experiment with leaves. Macrocentrus linearis parasitoids were also

78

provided a 25% honey solution via a dental wick with the solution being replenished
daily.
Statistical Analysis

Data were analyzed using survival analysis assuming Cox’s proportional hazards

model with a complementary log-log function in SAS® with the GENMOD procedure

(Allison 1995). Data had a binomial distribution with parasitoids either alive or dead at
speciﬁed time periods. The effects of chemical, gender, the time interval in which the
chemicals were allowed to dry, and the presence or absence of leaves were included in
the model and their signiﬁcance was tested using likelihood ratio tests. Week was
included as a blocking factor. For the trials where both leaves and Petri dishes were
sprayed, Least Squares Means were used to compare pairwise signiﬁcant effects.
Parasitoids that had escaped from the arena or where discrepancies occurred in the data
due to observational error were omitted from all analyses. For the B. dimidiator
experiment where insecticides were sprayed onto Petri dishes only, few to no parasitoids
survived to 120h, that time period was omitted from the survival analysis in order to ﬁt
the assumptions of the model. For M. linearis few to no parasitoids lived past 4h for
Guthion and that chemical therefore was omitted from the survival analysis.
Results
Bassus dimidiator Exposed to Residues on Petri Dishes

Survival analysis for female and male B. dimidiator parasitoids that had been
exposed to insecticides sprayed onto Petri dishes and allowed to dry for 1h (Table 3.2)
showed signiﬁcant effects for the time interval (x =l78.02, df=2, P<0.0001) at which data

was recorded, the chemicals used (x =267.10, df=5, P<0.0001), parasitoid gender

79

(x =6.52, df=l, P=0.0107), a chemical and gender interaction (x =l8.82, df=5, P=0.0021),
and week or blocking (x2=28.26, df=4, P<0.0001).
Females: residues dried 1h

The mean proportion of females surviving that were exposed to insecticides dried
1h on Petri dishes were calculated over each of the 5 weeks in which the experiment was
conducted (Table 3.3). At 4h female B. dimidiator exposed to the methoxyfenozide
treatment had a mean proportion of 1.00 surviving. The mean proportion of female
parasitoids surviving in the control and spinosad treatments at 4h was 0.98. Mean
proportions of females surviving in the imidacloprid, esfenvalerate, and azinphos-methyl
treatments at 4h were 0.95, 0.41, and 0.24 respectively. At 24h female B. dimidiator in
the methoxyfenozide treatments continued to have the greatest mean proportion surviving
(0.90) followed by the control (0.75), esfenvalerate (0.31), imidacloprid (0.26), spinosad
(0.21), and no females exposed to azinphos-methyl surviving. At 48h female B.
dimidiator in the control treatments had the greatest mean proportion surviving (0.50)
followed by methoxyfenozide (0.46), esfenvalerate (0.26), and imidacloprid and spinosad
which both had 0.03. The mean proportion of females surviving at 120h was greatest for
those on the controls (0.04) followed by methoxyfenozide and esfenvalerate which both
had 0.03 the rest had no survivors.

Pairwise comparisons (using contrast estimate) of the six treatments for B.
dimidiator females exposed to insecticide residues dried 1h onto Petri dishes only,
Showed that there were no signiﬁcant differences in survival between the control and
methoxyfenozide treatments (P=0.8262), esfenvalerate and imidacloprid (P=0.1479),

esfenvalerate and spinosad (P=0.1786), and spinosad and imidacloprid (P=O.9082). All

80

other combinations of treatments were signiﬁcantly different from one another (P3005).
Treatments can be ranked from the least toxic to the most toxic for B. dimidiator females
when exposed to residues dried 1h on Petri dishes where control: methoxyfenozide <
esfenvalerate = imidacloprid = spinosad < azinphos-methyl.
Males: residues dried 1h

The mean proportions of males surviving that were exposed to insecticides dried
1h on Petri dishes were calculated over the 5 weeks in which the experiment was
conducted (Table 3.3). At 4h all of the male B. dimidiator in the control,
methoxyfenozide, and spinosad treatments were surviving. The mean proportion of male
parasitoids surviving in the imidacloprid treatments at 4h was 0.84. Mean proportions of
males surviving in the esfenvalerate, and azinphos-methyl treatments at 4h were 0.26 and
0.25 respectively. At 24h male B. dimidiator in the methoxyfenozide treatments
continued to have the greatest mean proportion surviving (0.90) followed by the control
(0.84), imidacloprid (0.34), spinosad (0.13), esfenvalerate (0.10), and no males exposed
to azinphos-methyl surviving. At 48h male B. dimidiator in the control treatments had the
greatest mean proportion surviving (0.44) followed by methoxyfenozide (0.27),
esfenvalerate (0.05), imidacloprid (0.03), and spinosad and azinphos-methyl had no
survivors. The mean proportion of males surviving at 120h was 0.03 for the controls and
all other insecticides had no survivors.

Pairwise comparisons (using contrast estimate) of the six treatments for B.
dimidiator males exposed to insecticide residues dried 1h onto Petri dishes only, showed
that there were no signiﬁcant differences between the control and methoxyfenozide

treatments (P=0.4827), and spinosad and imidacloprid (P=0.1812). All other

81

combinations of treatments were significantly different from one another (pS0.0S).
Treatments can be ranked from the least toxic to the most toxic for B. dimidiator males
when exposed to residues dried 1h on Petri dishes where control: methoxyfenozide
<esfenvalerate<imidacloprid=spinosad<azinphos-methyl.
Bassus dimidiator Exposed to Residues on Petri Dishes and Leaves

Survival analysis for female and male B. dimidiator parasitoids that had been
exposed to insecticides sprayed onto Petri dishes or apple leaves and allowed to dry for
lb or 24h (Table 3.4) showed signiﬁcant effects for week (blocking) 06:31.00, df=4, P
<0.0001), the chemicals used (x2=242.61, df=5, P<0.0001), parasitoid gender (x =11.69,
df=l, P=0.0006), the presence of a leaf (x =19.33, df=l, P <0.0001), time interval
(x =139.56, df=5, P <0.0001) at which data was recorded, and a chemical and leaf
interaction (76:26.80, df=5, P <0.0001). There were no signiﬁcant effects of the time in
which insecticides were allowed to dry (x2=0.92, df=1, P=0.3374), a chemical and gender
interaction (x =6.22, df=5, P=0.2857), and a chemical and leaf and gender interaction
(x2=4.80, df=6, P=0.5700).
Females: residues on Petri dishes dried 1h

The sample size of B. dimidiator females available for treatments without leaves
was small and the number of parasitoids surviving was totaled for all ﬁve weeks and then
the mean proportion surviving was calculated (Table 3.5). The total mean proportion of
females surviving at 4h was 1.00 for parasitoids in the control, methoxyfenozide,
imidacloprid, and spinosad treatments. The total mean proportion of females surviving at
4h for the esfenvalerate and azinphos-methyl treatments was 0.60 and 0.20 respectively.

At 24h the control and methoxyfenozide treatments had a total mean proportion of 1.00

82

females surviving. Females in the spinosad treatment had the second highest total mean
proportion surviving (0.80) at 24h followed by esfenvalerate (0.60), imidacloprid (0.50),
and no surviving females in the azinphos-methyl treatments. At 48h 0.80 females
survived in the controls and intrepid treatments, 0.40 surviving in the esfenvalerate and
spinosad treatments, and no females surviving in the imidacloprid and azinphos-methyl
treatments. The total mean proportion of females surviving at 72b in the control,
methoxyfenozide, and esfenvalerate treatments was the same as at 48h the proportion
surviving in the spinosad treatments was 0.20. At 96h and 120h the control had the
greatest survival (0.80) followed by methoxyfenozide (0.60), esfenvalerate (0.40), and all
others had no surviving females.

Pairwise comparisons (using least squares means) of the six treatments for B.
dimidiator females exposed to insecticide residues dried 1h onto Petri dishes, showed that
there were no signiﬁcant differences between the control and methoxyfenozide
treatments (P=0. 1278), esfenvalerate and control (P=0.0797), esfenvalerate and
methoxyfenozide (P=0.7925), esfenvalerate and imidacloprid (P=0.0833),
methoxyfenozide and imidacloprid (P=0.0539), spinosad and imidacloprid (P=0.8776),
esfenvalerate and spinosad (P=0.0902) and spinosad and methoxyfenozide (0.0580). All
other treatments were signiﬁcantly different from one another (p50.05). Treatments
ranked from the least toxic to the most toxic for B. dimidiator females when exposed to
residues dried 1h on Petri dishes where control: methoxyfenozide =esfenvalerate=
spinosad = imidacloprid <azinphos-methyl.

Males: residues on Petri dishes dried 1h

83

The mean proportion surviving was calculated for males in treatments without
leaves as previously described for females (Table 3.5). The total mean proportion of
males surviving at 4h was 1.00 for parasitoids in the control, methoxyfenozide,
imidacloprid, and spinosad treatments. The total mean proportion of males surviving at
4h for the esfenvalerate and azinphos-methyl treatments was 0.60. At 24h the control had
a total mean proportion of 1.00 males surviving. Males in the methoxyfenozide and
spinosad treatment had the second highest total mean proportion survived (0.60) at 24h
followed by imidacloprid (0.50), esfenvalerate (0.40), and no surviving males in the
azinphos-methyl treatments. At 48h 0.80 males survived in the controls, 0.60 males in the
methoxyfenozide treatments survived, 0.20 surviving in the esfenvalerate treatments, and
no males surviving in the imidacloprid, spinosad, and azinphos-methyl treatments. The
total mean proportion of males surviving at 72h in the control and esfenvalerate
treatments were the same as at 48h the proportion surviving in the methoxyfenozide
treatments was 0.20. At 96h the control had the greatest survival (0.80) followed by
methoxyfenozide (0.20), and all others had no surviving males. At 120h the total mean
proportion of males surviving in the control was 0.60, and 0.20 surviving for
methoxyfenozide.

Pairwise comparisons (using least squares means) of the six treatments for B.
dimidiator males exposed to insecticide residues dried lh onto Petri dishes, showed that
there were no signiﬁcant differences between the esfenvalerate and spinosad treatments
(P=0.4065), esfenvalerate and methoxyfenozide (P=0.3810), spinosad and imidacloprid
(P=0.1488), and spinosad and methoxyfenozide (P=0.0952). All other treatments are

signiﬁcantly different from one another (P5005). Treatments ranked from the least toxic

84

to the most toxic for B. dimidiator males when exposed to residues dried 1h on Petri
dishes where control< methoxyfenozide =esfenvalerate= spinosad = imidacloprid
<azinphos-methyl.
Females: residues on Petri dishes dried 24b

The mean proportion surviving was calculated for females in treatments without
leaves dried 24h as previously described for females and males in treatments without
leaves dried 1h (Table 3.6). At 4h females in the control, methoxyfenozide, imidacloprid,
and spinosad treatments had a total mean proportion of 1.00 surviving. Females in the
esfenvalerate and azinphos-methyl treatments had a total mean proportion of 0.75 and
0.25 respectively surviving at 4h. Females in the control and methoxyfenozide treatments
had a total mean proportion of 1.00 surviving at 24h, 0.75 surviving for females in the
esfenvalerate, imidacloprid, spinosad treatments, and no females in the azinphos-methyl
treatments were surviving. At 48h the control had the greatest total mean proportion of
females surviving (0.80), followed by methoxyfenozide (0.75), esfenvalerate and
imidacloprid both had 0.50 surviving, and no females in apinosad surviving. At 72h the
same proportion surviving in the control as at 48h. Methoxyfenozide and esfenvalerate
both had a total mean survival of 0.50 at 72h and 0.25 surviving in the imidacloprid
treatments. At 96h and 120h the total mean proportion of surviving females in the control
was 0.80, in methoxyfenozide 0.50, and esfenvalerate and imidacloprid had 0.25
surviving.

Survival analysis showed no signiﬁcant differences for the time in which the
insecticides were allowed to dry therefore the least squares means results for treatments

allowed to dry 24h are the same as those dried 1h and so are the toxicity rankings.

85

Males: residues on Petri dishes dried 24h

The mean proportion surviving was calculated for males in treatments without
leaves dried 24h as previously described for females (Table 3.6). At 4h and 24h all males
were surviving in the control, methoxyfenozide, and spinosad treatments a mean
proportion of 1.00. At 4h a mean proportion of 0.60 males were surviving in the
esfenvalerate treatment, 0.75 in the imidacloprid treatment, and 0.25 in the azinphos-
methyl treatment. At 24h 0.40 males in the esfenvalerate treatment was surviving and no
males were surviving in the imidacloprid and azinphos-methyl treatments. The control
had the greatest total mean proportion surviving (0.80) at 48h followed by
methoxyfenozide (0.75), esfenvalerate (0.40), and spinosad (0.50). The mean proportion
of males in the controls stayed at 0.80 for 72, 96, and 120h. The mean proportion of
males in the methoxyfenozide treatment decreased from 0.50 at 72h to 0.25 at 96 and
120h. The mean proportion of males surviving in the esfenvalerate treatments remained
at 0.20 for 72, 96, and 120h. No males were surviving in the spinosad treatment at 72h.

Survival analysis showed no signiﬁcant differences for the time in which the
insecticides were allowed to dry therefore the least squares means results for treatments
allowed to dry 24h are the same as those dried lb and so are the toxicity rankings.
Females: residues on apple leaves dried 1h

Parasitoid sample size was larger than in the B. dimidiator treatments without
leaves dried 1 or 24h and the mean proportion of surviving females was calculated over
the ﬁve weeks in which the experiment was conducted (Table 3.7). At 4h females in all
treatments except for in esfenvalerate (0.90) and azinphos-methyl (0.70) had a mean

proportion of 1.00 surviving. The control had a mean proportion of 0.90 females

86

surviving at 24h followed by methoxyfenozide with a mean proportion of 0.95 surviving,
0.80 in imidacloprid, 0.75 in esfenvalerate, 0.50 in spinosad, and no survivors in
azinphos-methyl. At 48h the control had the greatest mean proportion of females
surviving (0.90) followed by imidacloprid (0.80), methoxyfenozide (0.75), esfenvalerate
(0.65), and spinosad (0.25). At 72 and 96h the control had the greatest mean proportion
of females surviving (0.80) followed by methoxyfenozide (0.75). Females in the
imidacloprid treatment had a mean proportion of 0.65 surviving at 72h decreasing to 0.45
at 96h and 0.40 at 120h. Females in the esfenvalerate treatment had a mean proportion of
0.50 surviving at 72, 96, and 120h. A mean proportion of 0.25 females were surviving at
72h decreasing to 0.05 at 96 and 120h.

Pairwise comparisons (using least squares means) of the six treatments for B.
dimidiator females exposed to insecticide residues dried 1h onto apple leaves, showed
that there were no signiﬁcant differences between the control and methoxyfenozide
treatments (P=O.9742), esfenvalerate and methoxyfenozide (P=0.0865), esfenvalerate and
control (P=0.0609), and esfenvalerate and imidacloprid (P=0. 1930). All other treatments
are signiﬁcantly different from one another (P_<_0.05). Treatments ranked from the least
toxic to the most toxic for B. dimidiator females when exposed to residues dried 1h on
apple leaves where control: methoxyfenozide =esfenvalerate= irnidacloprid<spinosad
<azinphos-methyl.

Males: residues on apple leaves dried 1h

The mean proportion of males surviving with leaves dried lh was calculated as

described for females with apple leaves dried 1h (Table 3.7). At 4h males in the control,

methoxyfenozide, imidacloprid, and spinosad treatments had a mean proportion of 1.00

87

surviving. The mean proportion of males surviving at 4h in the azinphos-methyl and
esfenvalerate treatments was 0.65 and 0.60 respectively. At 24h males in the control,
methoxyfenozide, and imidacloprid treatments had a mean proportion of 1.00 surviving.
A mean proportion of 0.40 males were surviving in the esfenvalerate treatments, 0.33 in
the spinosad treatments and 0.05 in the azinphos-methyl treatments at 24h. The control
and methoxyfenozide treatments had the greatest mean proportion (0.80) of males
surviving at 48h followed by imidacloprid (0.75), esfenvalerate (0.30), spinosad (0.05),
and no survivors in the azinphos-methyl treatment. At 72h the control, azinphos-methyl,
and esfenvalerate treatments all had the same mean proportion of males surviving as at
48h. At 72h the mean proportion of males surviving in the imidacloprid treatment was
0.60 and no males were surviving in spinosad treatments. At 96h methoxyfenozide had
the greatest mean proportion of males surviving (0.80) followed by the control (0.70),
imidacloprid (0.50), and esfenvalerate (0.30). At 120h methoxyfenozide had the greatest
mean proportion of males surviving (0.73) followed by the control (0.65), imidacloprid
(0.40), and esfenvalerate (0.30).

Pairwise comparisons (using least squares means) of the six treatments for B.
dimidiator males exposed to insecticide residues dried 1h onto apple leaves, showed that
there were no signiﬁcant differences between the control and methoxyfenozide
treatments (P=0.7422), methoxyfenozide and imidacloprid (P=0.1174), and imidacloprid
and control (P=0.0521). All other treatments are signiﬁcantly different from one another
(P3005). Treatments ranked from the least toxic to the most toxic for B. dimidiator
males when exposed to residues dried 1h on apple leaves where control:

methoxyfenozide = imidacloprid< esfenvalerate <spinosad <azinphos-methyl.

88

Females: residues on apple leaves dried 24h

The mean proportion of females surviving with leaves dried 24h was calculated as
described for females and males with apple leaves dried 1h (Table 3.8). At 4h females in
the control, methoxyfenozide, imidacloprid, and spinosad treatments had a mean
proportion of 1.00 surviving. The mean proportion of females surviving at 4b in the
esfenvalerate and azinphos-methyl treatments was 0.95 and 0.94 respectively. At 24h
females in the methoxyfenozide had a mean proportion of 1.00 surviving while 0.93
surviving in the control, 0.88 in spinosad, 0.85 in esfenvalerate, 0.81 in imidacloprid, and
0.19 in the azinphos-methyl treatments. The methoxyfenozide and control treatments had
the greatest mean proportion 1.00 and 0.93 respectively of females surviving at 48h
followed by esfenvalerate (0.80), imidacloprid (0.67), spinosad (0.44), and azinphos-
methyl (0.06). At 72h methoxyfenozide treatments had the greatest mean proportion of
females surviving (0.87) followed by esfenvalerate (0.80), controls (0.79), imidacloprid
(0.67), spinosad (0.38), and no survivors in the azinphos-methyl treatment. At 96h
methoxyfenozide had the greatest mean proportion of females surviving (0.79) followed
by the control (0.67), esfenvalerate (0.65), imidacloprid (0.54), and spinosad (0.13). At
120h methoxyfenozide had the greatest mean proportion of females surviving (0.79)
followed by the control (0.67 ), esfenvalerate (0.65), imidacloprid (0.48), and spinosad
(0.13).

Survival analysis showed no signiﬁcant differences for the time in which the
insecticides were allowed to dry therefore the least squares means results for treatments
allowed to dry 24h are the same as those dried 1h and so are the toxicity rankings.

Males: residues on apple leaves dried 24b

89

The mean proportion of males surviving with leaves dried 24h was calculated as
described for females with apple leaves dried 24h (Table 3.8). At 4h males in the control,
methoxyfenozide, imidacloprid, and spinosad treatments had a mean proportion of 1.00
surviving. The mean proportion of males surviving at 4h in the azinphos-methyl and
esfenvalerate treatments was 0.75 and 0.65 respectively. At 24h males in the control,
methoxyfenozide, and imidacloprid treatments had a mean proportion of 1.00 surviving.
A mean proportion of 0.60 males were surviving in the esfenvalerate treatments, 0.52 in
the spinosad treatments and 0.08 in the azinphos-methyl treatments at 24h. The control
had the greatest mean proportion (0.80) of males surviving at 48h followed by
Imidacloprid (0.85), methoxyfenozide (0.75), esfenvalerate (0.45), azinphos-methyl
(0.08), and no survivors in the spinosad treatment. At 72h the control had the greatest
mean proportion of males surviving (0.73) followed by imidacloprid (0.71),
methoxyfenozide (0.69), esfenvalerate (0.40), and no survivors in the azinphos-methyl
treatment. At 96h the control had the greatest mean proportion of males surviving (0.73)
followed by imidacloprid (0.58), methoxyfenozide (0.56), and esfenvalerate (0.40). At
120h the control had the greatest mean proportion of males surviving (0.63) followed by
methoxyfenozide (0.56), imidacloprid (0.52), and esfenvalerate (0.35).

Survival analysis showed no signiﬁcant differences for the time in which the
insecticides were allowed to dry therefore the least squares means results for treatments
allowed to dry 24h are the same as those dried 1h and so are the toxicity rankings.
Macrocentrus linearis Exposed to Residues on Petri Dishes and Leaves

Survival analysis for female and male M. linearis parasitoids that had been

exposed to insecticides sprayed onto Petri dishes or apple leaves and allowed to dry for

90

lh or 24h (Table 3.9) showed signiﬁcant effects for week (blocking) (x2=29.89, df=4,
P<0.0001), the chemicals used (x2=278.64, df=4, P <0.0001), the presence of a leaf
(x =103.08, df=l, P <0.0001), time interval (x =105.67, df=5, P <0.0001) at which data
was recorded, a chemical and leaf interaction (x =39.84, df=4, P <0.0001), and a
chemical and gender interaction (36:36.04, df=4, P <0.0001) . There were no signiﬁcant
effects of parasitoid gender (xz=l .01, df=1, P=0.3157), the time in which insecticides
were allowed to dry (x =0.00, df=l, P=0.963 7), and a chemical and leaf and gender
interaction (x2=3.25, df=5, P=0.66l3).
Females: residues on Petri dishes dried 1h

The mean proportion of M. linearis females surviving when exposed to
insecticides dried 1h on Petri dishes was calculated over the ﬁve weeks in which the
experiment took place (Table 3.10). At 4h the methoxyfenozide treatment had the
greatest mean proportion of females surviving (1.00) followed by the control (0.90),
spinosad (0.88), imidacloprid (0.80), esfenvalerate (0.42), and no survivors in the
azinphos-methyl treatment. At 24h methoxyfenozide again had the greatest mean
proportion of females surviving (0.95) followed by the control (0.90), spinosad (0.45),
imidacloprid (0.40), and esfenvalerate (0.10). The mean proportion surviving in the
control and methoxyfenozide at 48h was the same as at 24h. The mean proportion of
females surviving at 48h for imidacloprid, spinosad, and esfenvalerate was 0.20, 0.17,
and 0.05 respectively. At 72h the greatest mean proportion of females surviving was the
control (0.90) followed by methoxyfenozide (0.88), imidacloprid (0.05), and no survivors
in esfenvalerate and spinosad treatments. At 96h the mean proportion of females

surviving in the control and imidacloprid treatments were the same as at 72h and the

91

mean proportion of females surviving in the methoxyfenozide treatment decreased to
0.78. At 120h the control had the greatest mean proportion of females surviving (0.70)
followed by methoxyfenozide (0.33) and imidacloprid (0.05).

Pairwise comparisons (using least squares means) of the six treatments for M.
linearis females exposed to insecticide residues dried 1h onto Petri dishes, showed that
there were no signiﬁcant differences between the control and methoxyfenozide
treatments (P=0.2319), and spinosad and imidacloprid (P=0.5773). All other treatments
are signiﬁcantly different from one another (p50.05). Treatments ranked from the least
toxic to the most toxic for M. linearis females when exposed to residues dried 1h on Petri
dishes where control: methoxyfenozide <imidacloprid= spinosad < esfenvalerate
<azinphos-methyl.

Males: residues on Petri dishes dried 1h

The mean proportion of M. linearis males surviving when exposed to insecticides
dried 1h on Petri dishes was calculated as described for females (Table 3.10). At 4h the
control and spinosad treatments had the greatest mean proportion of males surviving
(0.95), followed by methoxyfenozide (0.93), imidacloprid (0.80), esfenvalerate (0.63),
and azinphos-methyl (0.05). At 24h the control had a mean proportion of 0.88 males
surviving; methoxyfenozide had 0.83, esfenvalerate 0.22, spinosad 0.20, imidacloprid
0.10, and no survivors in the azinphos-methyl treatment. At 48h methoxyfenozide,
control, esfenvalerate, and imidacloprid treatments had a mean proportion of 0.78, 0.77,
0.10, and 0.10 males surviving respectively and no males were surviving in the spinosad
treatment. At 72h the control had the greatest mean proportion of males surviving (0.67)

followed by methoxyfenozide (0.52), esfenvalerate (0.10), and imidacloprid (0.05). The

92

mean proportion for the control, methoxyfenozide, and esfenvalerate treatments at 96h
was the same as at 72h and no males were surviving in the imidacloprid treatments. At
120h the control had a mean proportion of 0.55 males surviving, 0.32 males were
surviving in the methoxyfenozide treatments and 0.10 males were surviving in the
esfenvalerate treatments.

Pairwise comparisons (using least squares means) of the six treatments for M.
linearis males exposed to insecticide residues dried 1h onto Petri dishes, showed that
there were no signiﬁcant differences between the control and methoxyfenozide
treatments (P=0.2673), spinosad and imidacloprid (P=0.6860), esfenvalerate and
imidacloprid (P=0.4079), and esfenvalerate and spinosad (P=0.6719). All other
treatments were signiﬁcantly different from one another (P_<_0.05). Treatments ranked
from the least toxic to the most toxic for M. linearis males when exposed to residues
dried 1h on Petri dishes where control: methoxyfenozide < esfenvalerate: imidacloprid:
spinosad<azinphos~methyl.

Females: residues on Petri dishes dried 24h

The mean proportion of M. linearis females surviving when exposed to
insecticides dried 24h on Petri dishes was calculated over the ﬁve weeks in which the
experiment took place (Table 3.11). At 4h the control, methoxyfenozide, and
imidacloprid treatments had the greatest mean proportion of females surviving (1.00)
followed by the spinosad (0.90), esfenvalerate (0.35), and no survivors in the azinphos-
methyl treatment. At 24h the control had the greatest mean proportion of females
surviving (1.00) followed by the methoxyfenozide (0.95), imidacloprid and spinosad

(0.50), and esfenvalerate (0.15). The mean proportion surviving in the control and

93

methoxyfenozide at 48h was 0.95 and 0.80 respectively. The mean proportion of females
surviving at 48h for imidacloprid and spinosad was 0.15 and 0.10 respectively and no
females were surviving in the esfenvalerate treatment. At 72h the greatest mean
proportion of females surviving was in the methoxyfenozide treatment (0.70) followed by
the control (0.67), spinosad (0.10), imidacloprid (0.05). At 96h the mean proportion of
females surviving in the control was 0.57 decreasing to 0.52 surviving at 120h. The mean
proportion of females surviving in the methoxyfenozide treatment at 96h and 120h was
0.55. No females were surviving at 96h in the esfenvalerate and imidacloprid treatments.

Survival analysis showed no signiﬁcant differences for the time in which the
insecticides were allowed to dry therefore the least squares means results for treatments
allowed to dry 24h are the same as those dried 1h and so are the toxicity rankings.
Males: residues on Petri dishes dried 24h

The mean proportion of M. linearis males surviving when exposed to insecticides
dried 24h on Petri dishes was calculated as described for females (Table 3.11). At 4h the
control and spinosad had a mean proportion of 1.00 males surviving, 0.95 were surviving
in the methoxyfenozide treatment, 0.80 in imidacloprid, 0.75 in esfenvalerate, and 0.05
azinphos-methyl. At 24h the control and methoxyfenozide had the greatest mean
proportion of males surviving (0.75) followed by esfenvalerate (0.45), spinosad (0.35),
imidacloprid (0.30), and no surviving males in the azinphos-methyl treatment. At 48h
methoxyfenozide had the greatest mean proportion of males surviving (0.62) followed by
the control (0.58), esfenvalerate (0.15), imidacloprid (0.05), and no surviving males in the
spinosad treatment. At 72h methoxyfenozide had the greatest mean proportion of males

surviving (0.57) followed by the control (0.53), esfenvalerate (0.05), and no surviving

94

males in the imidacloprid treatment. At 96h the control had a mean proportion of 0.42
males surviving and 0.45 were surviving in the methoxyfenozide treatment and no
surviving males in the esfenvalerate treatment. At 120h the control and Intrepid had a
mean proportion surviving of 0.35 and 0.45 respectively.

Survival analysis showed no signiﬁcant differences for the time in which the
insecticides were allowed to dry therefore the least squares means results for treatments
allowed to dry 24h are the same as those dried 1h and so are the toxicity rankings.
Females: residues on apple leaves dried 1h

The mean proportion of M. linearis females surviving when exposed to
insecticides dried lh on apple leaves was calculated over the ﬁve weeks in which the
experiment took place (Table 3.12). At 4h the control and methoxyfenozide had a mean
proportion of 1.00 females surviving and imidacloprid and spinosad both had 0.88
surviving, while esfenvalerate and azinphos-methyl had 0.52 and 0.45 surviving
respectively. At 24h the control treatment had the greatest mean proportion of females
surviving (1.00) followed by methoxyfenozide (0.95), imidacloprid (0.73), spinosad
(0.65), esfenvalerate (0.42), and no females surviving in the azinphos-methyl treatment.
At 48h the control had a mean proportion of 1.00 females surviving while
methoxyfenozide had 0.75, imidacloprid 0.57, spinosad 0.43, and esfenvalerate 0.42. At
72h the control had the greatest mean proportion of females surviving (0.90) followed by
methoxyfenozide (0.60), imidacloprid (0.50), esfenvalerate (0.37), and spinosad (0.22).
At 96h the control had a mean proportion of 0.90 females surviving, methoxyfenozide

and imidacloprid had 0.50, esfenvalerate had 0.32, and spinosad had 0.10. At 120h the

95

control had a mean proportion of 0.90 females surviving; Intrepid had 0.45, esfenvalerate
0.32, imidacloprid 0.30, and spinosad 0.05.

Pairwise comparisons (using least squares means) of the six treatments for M.
linearis females exposed to insecticide residues dried 1h onto apple leaves, showed that
there were no signiﬁcant differences between the methoxyfenozide and imidacloprid
treatments (P=0.2246), and esfenvalerate and spinosad (P=0.4905). All other treatments
are signiﬁcantly different from one another (P_<_0.05). Treatments ranked from the least
toxic to the most toxic for M. linearis females when exposed to residues dried 1h on
apple leaves where control<methoxyfenozide= imidacloprid < esfenvalerate =
spinosad<azinphos~methyl.

Males: residues on apple leaves dried 1h

The mean proportion of M. linearis males surviving when exposed to insecticides
dried 1h on apple leaves was calculated as described for females (Table 3.12). At 4h the
control and methoxyfenozide had a mean proportion of 1.00 males surviving and
esfenvalerate and imidacloprid both had 0.90 surviving, while spinosad and azinphos-
methyl had 0.82 and 0.45 surviving respectively. At 24h the control and methoxyfenozide
treatment had the greatest mean proportion of males (1.00) surviving followed by
imidacloprid (0.80), esfenvalerate (0.75), spinosad (0.48), and no males surviving in the
azinphos-methyl treatment. The control and methoxyfenozide treatments had a 0.87 mean
proportion surviving at 48h while imidacloprid had 0.63, esfenvalerate 0.60, and spinosad
0.33 males surviving. At 72h the control had the greatest mean proportion of males
surviving (0.87) followed by methoxyfenozide (0.77), esfenvalerate (0.60), imidacloprid

(0.47), and spinosad (0.15). At 96h the control had a mean proportion of 0.87 males

96

surviving; methoxyfenozide had 0.65, esfenvalerate 0.55, imidacloprid 0.32, and
spinosad 0.05. At 120h the control had a mean proportion of 0.73 males surviving;
methoxyfenozide had 0.60, esfenvalerate 0.55, imidacloprid 0.20, and spinosad 0.05.

Pairwise comparisons (using least squares means) of the six treatments for M.
linearis males exposed to insecticide residues dried 1h onto apple leaves, showed that
there were no signiﬁcant differences between the control and methoxyfenozide
treatments (P=0.59l6), esfenvalerate and methoxyfenozide (P=0.5295), esfenvalerate and
control (P=0.2506), and esfenvalerate and imidacloprid (P=0.1035). All other treatments
are signiﬁcantly different from one another (P3005). Treatments ranked from the least
toxic to the most toxic for M. linearis males when exposed to residues dried lh on apple
leaves where control=methoxyfenozide=esfenvalerate=imidacloprid<spinosad<azinphos-
methyl.
Females: residues on apple leaves dried 24h

The mean proportion of M. linearis females surviving when exposed to
insecticides dried 24h on apple leaves was calculated over the ﬁve weeks in which the
experiment took place (Table 3.13). At 4h the imidacloprid treatment had the greatest
mean proportion of females surviving (1.00) followed by the control (0.95), spinosad
(0.90), methoxyfenozide (0.83), esfenvalerate (0.57), and azinphos-methyl (0.55). At 24h
imidacloprid the control and methoxyfenozide had the same mean proportion of females
surviving as at 4h. The treatments esfenvalerate and spinosad had a mean proportion of
0.30 and 0.65 females surviving respectively at 24b and no females surviving in the
azinphos-methyl treatment. At 48h the control and imidacloprid treatments had the

greatest mean proportion of females surviving (0.95), followed by methoxyfenozide

97

(0.83), spinosad (0.35), and esfenvalerate (0.30). At 72h the control, methoxyfenozide,
imidacloprid, esfenvalerate, and spinosad had a mean proportion of 0.90, 0.83, 0.80, 0.30,
and 0.25 females surviving respectively. At 96h the control had the greatest mean
proportion of females surviving (0.85) followed by methoxyfenozide (0.77), imidacloprid
(0.70), esfenvalerate (0.30), and spinosad (0.05). At 120h the control had the greatest
mean proportion of females surviving (0.85) followed by methoxyfenozide (0.62),
imidacloprid (0.40), esfenvalerate (0.30), and spinosad (0.05).

Survival analysis showed no signiﬁcant differences for the time in which the
insecticides were allowed to dry therefore the least squares means results for treatments
allowed to dry 24h are the same as those dried 1h and so are the toxicity rankings.
Males: residues on apple leaves dried 24h

The mean proportion of M. linearis males surviving when exposed to insecticides
dried 24h on apple leaves was calculated as described for females (Table 3.13). At 4h the
control and methoxyfenozide had all males surviving with a mean proportion of 1.00.
Spinosad, esfenvalerate, imidacloprid, and azinphos-methyl had a mean proportion of
0.93, 0.85, 0.75, and 0.50 males surviving respectively at 4h. At 24h the control had the
greatest mean proportion of males surviving (0.85) followed by methoxyfenozide and
imidacloprid (0.75), esfenvalerate (0.60), spinosad (0.57), and no survivors in the
azinphos-methyl treatment. At 48h the control had the greatest mean proportion of males
surviving (0.75) followed by methoxyfenozide (0.70), esfenvalerate and imidacloprid
(0.60), and spinosad (0.07). At 72h the control had the greatest mean proportion of males
surviving (0.65) followed by methoxyfenozide (0.60), esfenvalerate and imidacloprid

(0.50), and spinosad (0.07). At 96h the control had the greatest mean proportion of males

98

surviving (0.65) followed by methoxyfenozide (0.60), imidacloprid (0.50), esfenvalerate
(0.45), and spinosad (0.07). At 120h the control had the greatest mean proportion of
males surviving (0.60) followed by methoxyfenozide (0.55), esfenvalerate (0.45),
imidacloprid (0.40), and spinosad (0.07).

Survival analysis showed no signiﬁcant differences for the time in which the
insecticides were allowed to dry therefore the least squares means results for treatments
allowed to dry 24h are the same as those dried lb and so are the toxicity rankings.
Discussion

A signiﬁcant blocking effect (by week) occurred for both B. dimidiator
experiments (Table 3.2 and 3.4) and for the M. linearis experiment (Table 3.9). A
blocking effect was present in the Survival analysis due to individual parasitoids that
would survive to 120h for certain insecticides in different weeks where other individuals
exposed to the same insecticide would die before that time. A signiﬁcant chemical effect
(Tables 3.2, 3.4, 3.9) occurred because of the substantial differences in the toxicity of the
insecticides. Fewer B. dimidiator and M. linearis would survive past 4h when exposed to
azinphos-methyl while many individual parasitoids would survive to 120h for other
insecticides such as methoxyfenozide. For B. dimidiator exposed to residues on leaves or
Petri dishes, there were signiﬁcant effects of gender (Table 3.2 and 3.4) where females
appeared to survive longer than males (Table 3.3, 3.5, 3.6, 3.7, and 3.8). In the B.
dimidiator experiment where insecticides were sprayed on Petri dishes or apple leaves
and in the M. linearis experiment the 24h drying time period was added to determine if
the age of the residues would increase the survival of the parasitoids. No differences

between a lh drying time and a 24h drying time occurred, however, the insecticides were

99

not exposed to the same type of environment as in an orchard where rain, sun and other
elements would degrade the toxicity of the insecticides over time. All experiments had a
signiﬁcant effect of the time interval in which the mortality of the parasitoids was
assessed because as time progresses and parasitoids age there is a certain degree of
natural mortality. The complementary log-log function of survival analysis also
recognizes that parasitoids could have died at any point in time between when data was
actually recorded.

For the B. dimidiator and M. linearis experiments where apple leaves were
sprayed there was a signiﬁcant leaf effect and a signiﬁcant chemical leaf interaction
(Table 3.4 and 3.9) where the presence of a leaf appeared to increase the length of
survival for most insecticides, and especially for certain insecticides, such as with
imidacloprid when compared to those with no leaf. One possible explanation for the
differences in the presence or absence of leaves could be that parasitoids in arenas with
leaves had more space to escape from the insecticide because only the upper leaf surface
had been treated so the parasitoids could rest on the insecticide free meshed ring or on the
top Petri dish that was also insecticide free, while parasitoids that were in Petri dish
arenas had less insecticide free space to escape to because both the top and bottom Petri
dishes contained insecticide. The arenas with leaves are closer to what would actually
occur in the orchard where parasitoids are able to avoid insecticide residues. It is possible
that parasitoids could be gaining some type of nutrient or water from the leaves that
enhance their survival. In addition, leaves were also used to see if the Systemic properties
of imidacloprid (Provado) (Wise et al. 2002) could result in an increase in survival of

parasitoids when exposed to residues of this insecticide sprayed onto leaves. I did ﬁnd

100

that parasitoids exposed to imidacloprid sprayed on leaves had greater survival compared
to those exposed to imidacloprid sprayed onto Petri dishes.

The insect growth regulator, methoxyfenozide (Intrepid) appears to be safe for B.
dimidiator males and females when sprayed on Petri dishes or leaves. Survival of
parasitoids exposed to this insecticide were similar to parasitoids in the control treatments
where parasitoids in both treatments were able to survive to 120h and were not found to
be signiﬁcantly different from one another (Table 3.3, 3.5, 3.6, 3.7, and 3.8). Intrepid also
appears to be safe for M. linearis males and females when sprayed on Petri dishes or
leaves, where survival of parasitoids exposed to this insecticide is similar to parasitoids in
the control and were found not to be signiﬁcantly different from one another (Table 3.10,
3.11, 3.12, and 3.13). Methoxyfenozide was also found to be non-toxic to the parasitoid
Colpoclypeusﬂorus (Walker) in direct contact insecticide bioassay experiments (Brunner
et al. 2001).

Azinphos-methyl (Guthion) was highly toxic to both male and female B.
dimidiator and M. linearis when sprayed on leaves and Petri dishes (Table 3.3, 3.5, 3.6,
3.7, 3.8, 3.10, 3.11, 3.12, 3.13). Azinphos-methyl was also found to be highly toxic to
parasitoids in contact and residual insecticide bioassays (Jones et al. 1995, Brunner et al.
2001) and to spiders when sprayed in orchards (Bajwa and Aliniazee 2001). In this
experiment azinphos-methyl was so toxic to M. linearis that the insecticide could not be
used in the survival analysis because it did not ﬁt the assumptions of the model.

Spinosad (SpinTor) appears to be moderately too highly toxic for male and female
B. dimidiator and M. linearis when sprayed on leaves and Petri dishes (Table 3.3, 3.5,

3.6, 3.7, 3.8, 3.10, 3.11, 3.12, and 3.13). Spinosad has been found to be toxic to

101

parasitoids (Suh et al. 2000, Consoli et al. 2001, Mason et al. 2002) and predators
(Cisneros et al. 2002) though it is touted as a “selective insecticide.” Imidacloprid and
esfenvalerate also appear to be moderately toxic to both B. dimidiator and M. linearis
males and females when sprayed onto Petri dishes and leaves (Table 3.3, 3.5, 3.6, 3.7,
3.8, 3.10, 3.11, 3.12, and 3.13). The proportion of parasitoids surviving after exposure to
imidacloprid also appears to have increased when this insecticide was sprayed onto
leaves. Brunner et al. (2001) found that esfenvalerate (Asana) was toxic to parasitoids C.
ﬂorus and Trichogramma platneri N agarkatti, but could possibly be used at low rates at
times of parasitoid inactivity without negative impact on parasitoid populations.
Imidacloprid (Provado) was found to be toxic to C. ﬂorus and T. plameri in contact
insecticide experiments (Brunner et al. 2001). Imidacloprid (Provado) has translaminar
properties and is taken up by the leaves that it is sprayed on however there have been
studies where imidacloprid has sublethal effects on parasitoids who feed on the nectar of
plants sprayed with imidacloprid. Stapel et al.(2000) found that the longevity and
fecundity of the parasitoid Microplitis croceipes Cresson, was negatively effected after
parasitoids fed on nectar from cotton plants that had been sprayed with imidacloprid.
Conclusion

The insecticide methoxyfenozide appears to be safe for both B. dimidiator and M.
linearis. The insecticide azinphos-methyl was highly toxic and should probably not be
included in an apple pest management program that integrates biological control for
OBLR into its management strategy. The insecticides imidacloprid, esfenvalerate, and
spinosad appear to be moderately to highly toxic to these parasitoids depending method

of application in this study (sprayed onto a leaf or onto a Petri dish) and could probably

102

be used without interfering with biological control agents if applied with appropriate
timing in regards to the presence of parasitoids. Further studies should be done with
imidacloprid, esfenvalerate, and spinosad in an orchard setting in order to determine if
ﬁeld conditions make these insecticides less harmful to biological control agents than
under laboratory conditions. Further study could also be done with these three
insecticides applied at the lowest recommended ﬁeld rates in the laboratory setting. The
timing of adult parasitoid presence in the orchard should also be determined so that the
moderately toxic insecticides can be used when parasitoids are least susceptible. Further
tests should be conducted to determine if imidacloprid could adversely affect B.
dimidiator and M. linearis through ﬂoral resources. The effects of the age of the residue
should also be tested further, to determine how long residues are toxic in the ﬁeld.
Further studies should be conducted that look at the indirect effects, such as decreased
fecundity, lost ability to parasitized or locate hosts, that these insecticides may have on

parasitoids.

103

 

 

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118

Reference

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Brunner, J .F., J .E. Dunley, M.D. Doerr, and E. H. Beers. 2001. Effect of pesticides on
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Gut, L., J. Wise, J. Miller, R. Isaacs, and P. McGhee. 1999. MSHS Trust Funded
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Hill. T.
(Lepith
Ichnucr

Ho. HI
Michig
thesis.

Ho“ in
63.

Jones.1
Bemisi
Entom.

Kromb
Hymel
\"olum

Li. S.\'
O'Hur;
Tortric

Li. SN
Obllqm1
J. ECOr

 

Madsel
Similk.

SpinOS;
EnlOm

OhlEn.
State“
Agn'q

Reisgi
Econ.

StaDc]
inSeCU

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Bemisia tabaci (Hom., Aleyrodidae) to leaf residues of selected cotton insecticides.
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Krombein, K.V., P.D. Hurd Jr., D.R. Smith, and B.D. Burks. 1979. Catalog of
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Li, S.Y., S.M. Fitzpatrick, J .T. Troubridge, M.J. Sharkey, J .R. Barron, and J .E.
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Madsen, HE, J .M. Vakenti, and AP. Gaunce. 1984. Distribution and ﬂight activity of
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Mason, P.G., M.A. Erlandson, R.H. Elliott, and 3.]. Harris. 2002. Potential impact of
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Econ. Entomol. 71: 804-809.

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17: 243-249.

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Trichogramma exiguum (Trichogrammatidae: Hymenoptera) preimaginal development
and adult survival. J. Econ. Entomol. 93: 577-583.

Sun, X., BA. Barrett, and DJ. Biddinger. 2000. Fecundity and fertility reductions on
adult leafrollers ecposed to surfaces treated with the ecdysteroid agonists tebufenozide

and methoxyfenozide. Entomol. Exp. Appl. 94: 75-83.

Thompson, G.D., R. Dutton, and T.C. Sparks. 2000. Spinosad - a case study: an example
from a natural products discovery programme. Pest Manag. Sci. 56: 696-702.

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121

 

Phen
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Chapter 4

Phenology of Adult Bassus dimidiator (Nees.) and Macrocentrus linearis (Nees.)
(Hymenoptera: Braconidae), in commercially managed Michigan apple orchards.

Abstract

A final study was conducted to determine the activity periods of adult B.
dimidiator and M. linearis in Michigan apple orchards. Yellow bucket traps and sentinel
larvae were placed in two commercially managed apple orchards located in Kent, and
Van Buren Counties, Michigan and in the Trevor Nichols Research Center orchard in
Allegan County, Michigan. Parasitoid occurrence in the orchards was also compared to
OBLR adult ﬂight data obtained from pheromone trap catches. Out of a total of 2,790
OBLR sentinel larvae, thirteen parasitoids were recovered, two M. linearis and 11 Enytus
sp. No B. dimidiator were recovered from the sentinel larvae. All parasitoids recovered
emerged from sentinel larvae that had been placed in the orchard located in Allegan
County. A total of 2,318 Hymenoptera and 2,987 Diptera were captured in the yellow
bucket traps including three B. dimidiator. Macrocentrus linearis was not captured in
bucket traps. All the B. dimidiator captured were from buckets placed in the Van Buren
County orchard. Macrocentrus linearis was present in the orchards shortly after peak
OBLR adult ﬂight that occurred in mid June after codling moth and leafroller sprays are
applied in the orchard. Bassus dimidiator was present in the orchards during peak OBLR
ﬂight at the time when codling moth and leafroller sprays are being applied.
Recommendations can be made so that insecticides could be applied at times when these

parasitoids are not active in Michigan apple orchards.

122

 

Introduction

A survey of the parasitoids attacking the obliquebanded leafroller (OBLR),
Choristoneura rosaceana (Harris), an important pest in Michigan apple production, was
conducted during 1999 and 2000 (Chapter 2). The survey resulted in the discovery of two
important Braconid parasitoids, Bassus dimidiator (Nees.) and Macrocentrus linearis
(Nees.) (Hymenoptera). Bassus dimidiator was the most abundant hymenopteran
parasitoid comprising up to 96% of the parasitoid complex attacking OBLR while M.
linearis made up to 12% of the parasitoid complex attacking OBLR (Chapter 2). The
parasitoid survey conducted in Michigan apple orchards during 1999 and 2000 suggests
that biological control could be a key component in an integrated pest management (IPM)
program for OBLR in Michigan apple orchards.

The discovery of B. dimidiator developing on C. rosaceana constitutes a new host
record for this parasitoid. Previously B. dimidiator had only been reported to attack the
eye-spotted bud moth, Spilonota ocellana (Denis and Schiffermuller) (Krombein et al.
1979). The complete biology of B. dimidiator, a solitary endoparasitoid, has been
described by Dondale (1954) under the name Agathis laticinctus (Cresson). In contrast,
M. linearis is a known parasitoid of OBLR (Krombein et al. 1979). The biology of M.
linearis, a polyembryonic endoparasitoid, is similar to that of Macrocentrus nigridorsis
Viereck described by Li et al. (1999).

Organophosphate insecticides (OPs) have been the major form of control for
OBLR for more than 40 years (Gut et al. 1999). However, the occurrence of up to 21-
fold resistance to CPS by OBLR in Michigan apple orchards constitutes a major threat to

this production system (Gut et al. 1998). Along with OBLR resistance, increasing

123

 

restrictions on broad-spectrum insecticide use in agriculture resulting from the
Environmental Protection Agency’s Food Quality Protection Act (1996) has prompted
the search for more sustainable and environmentally friendly forms of insect control.
Reductions in the use of broad-spectrum insecticides and the development of pheromone
mating disruption programs and more selective insecticides has left the door open for
successful use of biological control agents as a major mortality factor for OBLR.

The selectivity of some of the newer insecticides however, is questionable and
should be tested on natural enemies in the laboratory and in the orchard prior to wide
scale commercial use. The direct effect of ﬁve insecticides currently used in Michigan
apple orchards for control of OBLR was tested on the adult parasitoids B. dimidiator and
M. linearis (Chapter 3). The insecticides ranged from traditional broad spectrum
insecticides such as azinphos-methyl, to the newer more selective insecticides such as the
insect growth regulator (IGR), methoxyfenozide. Azinphos-methyl was found to be
highly toxic for both B. dimidiator and M. linearis, while methoxyfenozide appeared to
be safe for both parasitoids (Chapter 3). The other insecticides tested (esfenvalerate,
imidac10prid, and spinosad) were found to be highly to moderately toxic to the
parasitoids depending on if the insecticide was sprayed onto Petri dishes or leaves
(Chapter 3). Information on toxicity allows growers to avoid the use of broad-spectrum
insecticides when M. linearis and B. dimidiator adults are present in the orchard.

The exact time in which B. dimidiator and M. linearis are present and attacking
OBLR in Michigan apple orchards has not been determined. The abundance, diversity,
and time in which parasitoids are present in an environment has been successfully

delineated by others using yellow pan traps (Finnamore 1994, Purcell and Messing 1996)

124

 

 

 

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and sentinel larvae (Marino and Landis 1996, Costamagna 2002). Yellow pan traps are
shallow bowls or pans containing a mixture of water and soap, painted yellow to mimic
the reﬂectance of leaves, which attract insects to their hosts. Sentinel larvae are larvae
placed into an environment by the researcher for a predetermined amount of time that are
later removed to determine if the larvae have been parasitized.

The objective of this study was to determine the time at which the adult
parasitoids B. dimidiator and M. linearis are present in apple orchards in Michigan using
two methods of sampling. The results of this study could then be combined with the
information obtained from the insecticide bioassays and suggestions could be made to
growers about the timing of insecticide applications that could minimize or avoid
mortality of B. dimidiator and M. linearis in commercially managed orchards.

Methods

Two sampling methods (yellow bucket traps and sentinel larvae) were used
together in the same orchard block in order to determine when the adult parasitoids, B.
dimidiator and M. linearis, were present and parasitizing OBLR in Michigan apple
orchards.

This study was conducted in two commercially managed apple orchards, and in a
research orchard from late April to late July. Two of the orchards were located in the
major apple producing regions of the state Kent County (Fruit Ridge), and Van Buren
County (Southwest) (Figure 1). The third orchard was located at the Michigan State
University Trevor Nichols Research Center (TNRC) in Allegan County, Michigan
(Figure 4.1). Three blocks per orchard were chosen that were approximately 1.62

hectares in size, however, blocks varied in apple variety and tree size. Sampling did not

125

occur within 9m of block edges so that edge effects could be avoided. Trees and rows
within the sample area were then counted and a random number table was used to
determine which rows and trees would be assigned to sentinel larvae or bucket traps.

In each block a total of ten sentinel larvae stations were placed onto apple tree
branches. Stations consisted of a 2 L plastic pop bottle that had the bottom cut off and
had a square cut out of the front half the length of the bottle so that a 32 02 cup could ﬁt
into it (Figure 4.2). Pop bottles were ﬁxed to the trees with plastic cable ties placed
around stable branches. Only ﬁve stations per block were used each week. The ﬁrst ﬁve
pop bottles were placed in randomly selected trees, and the other ﬁve bottles were placed
in trees directly across the row (Figure 4.3). Trees containing sentinel larvae could then
be alternated from week to week.

Apple shoots approximately 0.30m to 0.61m in length were cut each week from
an abandoned apple orchard located in Allegan County, Michigan. A total of 450 shoots
were cut and bundled into individual bouquets of 10 shoots each bound together with
electrical tape. After three weeks into the study we switched to a total of 225 shoots cut
each week and bundled into individual bouquets of ﬁve shoots each. Bouquets were each

placed into 3202. plastic cups containing water and Floralife® Crystal ClearTM (Floralife

Inc., Walterboro) fresh ﬂower food in order to extend the life of the bouquets. Melted
parafﬁn wax was poured over the water in each cup to hold the bouquets in place and
reduce evaporative water loss. In mid- summer we switched from parafﬁn wax to

Paraﬁlm M® (American National Can, Chicago) as high temperatures made the wax

unstable.

126

 

OBLR egg masses were obtained from the TNRC laboratory colony, where the
egg masses were laid onto pieces of wax paper. A single OBLR egg mass at black head
or newly hatched stage was clipped to the bouquets with a small binder clip. Cups with
bouquets were then placed into the sentinel larvae stations in the apple orchards where
they remained for three days. Bouquets were disassembled in the orchard and leaves and
stems were placed into Ziploc bags and put into a cooler with ice packs for transportation
to the laboratory. OBLR larvae recovered from the bouquets were placed onto a modiﬁed
pinto bean diet (Shorey and Hale 1965). The diet was contained in 402 plastic soufﬂé
cups with lid and approximately ﬁve larvae were placed into each cup. Larvae were
reared on the laboratory bench at room temperature. Larvae were monitored weekly for
mortality, pupation, adult OBLR emergence, and parasitism. Bouquets were replaced in
the orchards the following week and placed into the station opposite from where the
previous bouquet was placed. Parasitoids were identiﬁed from specimens collected in a
previous survey of parasitoids attacking OBLR in Michigan apple orchards (Chapter 2).

Yellow bucket traps were constructed from half gallon plastic buckets painted
yellow. Each bucket had four holes drilled into the sides covered with screen that were
located half an inch from the bucket bottom to allow excess water to drain after rain.
Buckets were ﬁlled just below the holes with a water and soap (Ivory liquid dish soap)
mixture (four drops of soap/3.79L of H20). Buckets remained ﬁxed to trees with plastic
cable ties. Yellow bucket traps were placed on either side of one of the sentinel larvae
stations (Figure 4.3) resulting in a total of ten-bucket traps per block. Bucket traps were

checked twice per week. The contents of the bucket were emptied into a tea strainer and

127

 

rinsed with water. Insects were placed onto a piece of paper towel and placed into a
Ziploc bag for transport to the laboratory, and placed in the freezer for later examination.

Insects caught in the yellow bucket traps were sorted by order. For simplicity,
insects in the orders Hymenoptera and Diptera were kept and counted while others were
discarded. Hymenoptera were further divided into ants, bees, and wasps. Only B.
dimidiator and M. linearis were identiﬁed to species.

Adult OBLR were monitored at the same time the sentinel larvae and yellow
bucket traps were used. Moth captures in pheromone traps from each of the three
orchards were provided by L. Stelinski, Tree Fruit Entomology Laboratory, Michigan
State University, East Lansing, Michigan, and M. Haas, Trevor Nichols Research Center,
Fennville, Michigan. With this additional data, OBLR adult ﬂight and timing of leafroller
insecticide applications could be compared to adult B. dimidiator and M. linearis
occurrence in the orchards.

Results

A total of 2,790 OBLR sentinel larvae were recovered from the three apple
orchards, of which 1,089 larvae died, and 1,688 emerged as adults (Table 4.1). The total
percent mortality of the OBLR larvae recovered was 39.03%, and a total of 13 parasitoids
emerged from the sentinel larvae (0.76% parasitism) (Table 4.1). The greatest number of
larvae recovered, 1,087, came from the orchard located in Kent County, Michigan, which
also had the highest percent mortality (44.16%) (Table 4.1). No parasitoids emerged from
larvae collected from the Kent county orchard (Table 4.1). The second highest number of
sentinel larvae, 880, was recovered from the orchard located in Allegan County (Table

4.1). All 13 parasitoids that had emerged from sentinel larvae also came from the Allegan

128

county orchard (2.21% parasitism) (Table 4.1). Of the 13 OBLR that had parasitoids
emerge from them 11 were parasitized by Enytus sp. (Ichnuemonidae) and two were
parasitized by M. linearis. The fewest number of sentinel larvae, 823, were recovered
from the orchard located in Van Buren County, but these larvae had the second highest
percent mortality (38.07%) (Table 4.1). The parasitoid B. dimidiator had not parasitized
any of the sentinel OBLR larvae recovered from the three orchards.

A total of 2,318 Hymenoptera and 2,987 Diptera were captured in the yellow
bucket traps placed in the three apple orchards (Table 4.2). The greatest number of
Hymenoptera, 931, was captured in the Kent County orchard followed by the Allegan
County orchard with 814, and the Van Buren orchard with 573 (Table 4.2). The
Hymenoptera captured in the yellow bucket traps were sorted into bees, wasps, and ants.
A total of 342 bees were captured in traps located in the Allegan County orchard, while
80 and 47 bees were captured in the Kent and Van Buren orchards respectively (Table
4.2). A total of 371 wasps were collected from the Allegan orchard while 192 and 331
wasps were collected at the Kent and Van Buren orchards respectively (Table 4.2). No M.
linearis were found in the bucket traps. A total of three B. dimidiator however, were
found in bucket traps from the Van Buren orchard. No B. dimidiator were captured in
bucket traps at the other two orchards (Table 4.2). A total of 659 ants were captured at
the Kent county orchard, 195 were captured in buckets at the Van Buren orchard, and 101
were captured at the Allegan County orchard (Table 4.2). The greatest number of Diptera,
a total of 1,233, was captured in bucket traps in the Van Buren orchard (Table 4.2). A
total of 1,098 Diptera was captured in the Allegan county orchard and 656 were captures

in the Kent county orchard (Table 4.2).

129

 

Data from the OBLR pheromone traps were not used for the Kent County orchard
because no B. dimidiator or M. linearis were collected using either the yellow bucket
traps or sentinel larvae methods of sampling. OBLR moth catches in pheromone traps
were only collected for the two blocks where sentinel larvae and bucket traps were being
used in the Allegan County orchard. The combined OBLR catches for the two blocks are
presented in Figure 4.4. OBLR catches were also combined for the three blocks where
sentinel larvae and bucket traps were being used in the Van Buren orchard (Figure 4.5).
Peak adult OBLR ﬂight for both the Allegan County and Van Buren orchards occurred
around mid June (Figures 4.4 - 4.5). The Enytus sp. (Ichneumonidae) that were collected
from sentinel larvae located in the Allegan County orchard were present in the orchard
before peak adult OBLR ﬂight from late May into early June during the time when
coddling moth, Cydia pomonella (Linnaeus), insecticides are being applied in the
orchards (Figure 4.4). The M. linearis (Braconidae) that were collected from the sentinel
larvae that had been placed in the Allegan County orchard were present after peak adult
OBLR ﬂight from late June to the ﬁrst of July after codling moth and leafroller
insecticides are applied in the orchards (Figure 4.4). The B. dimidiator (Braconidae) that
were captured in the yellow bucket traps that had been placed in the Van Buren County
orchard were present during peak adult OBLR ﬂight during mid June at the same time
codling moth and leafroller insecticides are being applied (Figure 4.5).

Discussion and Conclusion

A large number of sentinel larvae were successfully recovered however, a large

percentage of the larvae did not develop into adult moths. The level of mortality that had

occurred in the sentinel larvae could possibly be due to injury to the larvae as they were

130

being transferred from the apple branches to the diet. Insecticides that were applied when
larvae were present in the orchard could have also killed many larvae. Other possible
explanations for sentinel larvae mortality could be disease, and in some cases the diet
became moldy. Though a reasonable number of OBLR larvae were recovered from the
orchards, few parasitoids emerged from these larvae. Some possible reasons that could
account for the low level of parasitism could be due to the searching habits of the
parasitoids, where larger larvae are more apparent than early instar larvae. However,
Dondale (1954) observed that B. dimidiator parasitized early instar (actual instar not
speciﬁed) eye-spotted bud moth, Spilonota ocellana (Denis and Schiffermuller) in
orchards.

A preliminary study that we conducted showed that B. dimidiator does parasitize
ﬁrst instar OBLR (n=14), however the OBLR were on artiﬁcial diet in plain sight of the
parasitoid in a small, enclosed 4 oz. diet cup. Though B. dimidiator appears to be able to
parasitize early instar OBLR in the laboratory it is possible that the parasitoid is unable to
locate these larvae in the ﬁeld where they are maybe concealed in leaf and ﬂower bud
terminals. The number of sentinel larvae placed into the ﬁeld also may not have been
numerous enough or spread widely enough throughout the orchard to enable parasitoids
to easily locate them. Sentinel larvae were also left in the ﬁeld for three days had they
been left for a longer period of time there may possibly have been a higher incidence of
parasitism.

The Enytus sp. (Ichneumonidae) that were recovered from the sentinel larvae
were also found to have emerged from the OBLR that were collected during the 1999 and

2000 parasitoids survey that was previously conducted in Michigan apple orchards

131

(Chapter 2). The Enytus sp. recovered in the survey were not a consistently abundant
parasitoid but made up to 23% of the total parasitoid complex attacking OBLR, while M.
linearis which was also recovered in the sentinel larvae made up to 12% of the parasitoid
complex attacking OBLR but was more consistently abundant (Chapter 2). A possible
reason that these two parasitoids were recovered from the sentinel larvae when B.
dimidiator was not could again be due to searching behavior of the parasitoid. There is
also the possibility that the cues required for B. dimidiator to locate its host were not
present or strong enough, where larger larvae would produce a grater amount of feeding
damage.

The time (late May to early June) at which the Enytus Sp. parasitized the sentinel
OBLR larvae placed in the orchard coincided with the naturally occurring OBLR larvae
that are in the later instars before peak adult OBLR ﬂight. OBLR larvae are already in
their 2-3rd instar when they emerge form their overwintering hibemaculum (Howitt
1993). There is the possibility that Enytus sp. could have an alternate host present in the
orchard at the time when OBLR reaches its later instars and pupates. An additional
possibility is that Enytus sp. is capable of parasitizing a range if instars. The M. linearis
that were recovered from the sentinel OBLR were parasitizing these larvae at the same
time (late June to early July, 2-3 weeks after peak adult ﬂight) naturally occurring OBLR
would be primarily in early to mid instar stages and egg hatch nearly complete.

The yellow bucket traps were successful in capturing a large number of beneﬁcial
and non-beneﬁcial insects, although only three B. dimidiator and no M. linearis were
captured. The B. dimidiator that were captured in the orchard occurred at the same time

as peak adult OBLR ﬂight. Bassus dimidiator was observed to have emerged from an

132

overwintering OBLR larva (n=l) so it is possible that B. dimidiator overwinters in the 2-
3rd instar OBLR and emerges before OBLR pupate and thus is present at the time when
OBLR egg masses hatch. Had there been more yellow bucket traps placed throughout the
orchard, more B. dimidiator may have been captured.

Though the sample sizes of the parasitoids recovered from the sentinel larvae and
yellow bucket traps were too small to make ﬁrm conclusions the parasitoids that were
recovered suggests that parasitoids are present in the orchard at times when major spray
applications occur. Further studies should be done in order to determine if the times when
parasitoid presence was detected are when these parasitoids are most abundant. Also it
would be advantageous to determine how long parasitoids are present in the orchards.
Once the timing of parasitoid presence is more thoroughly established then
recommendations could be made to growers as to when to avoid insecticide applications,

and thus decrease mortality of B. dimidiator and M. linearis in the orchard.

133

 

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References

Costamagna, A. 2002. Inﬂuence of agricultural landscape complexity on patterns of
parastioid abundance and diversity. M.S. thesis, Michigan State University, Michigan.

Dondale, CD. 1954. Biology of Agathis laticinctus (Cress.) (Hymenoptera: Braconidae),
a parasitoid of the eye-spotted bud moth, in Novia Scotia. Can. Entomol. 86: 40—44.

Finnamore, A.T. 1994. Hymenoptera of the Wagner natural area, a boreal spring fen in
central Alberta. Mem. Ent. Soc. Can. 169: 181-220.

Gut, L., J. Wise, R. Isaacs, and P. McGhee. 1998. MSHS Trust Funded Research
Obliquebanded leafroller control tactics and management strategies: 1998 update. 128th
Annual Report of the Secretary of the State Hort. Soc. of Michigan.

Gut, L., J. Wise, J. Miller, R. Isaacs, and P. McGhee. 1999. MSHS Trust Funded
Research New insect controls and pest management strategies. 129th Annual Report of
the Secretary of the State Hort. Soc. of Michigan.

Howitt, AH. 1993. Common tree fruit pests. Michigan State University Extension, NCR
63.

Krombein, K.V., P.D. Hurd Jr., D.R. Smith, and B.D. Burks. 1979. Catalog of
Hymenoptera in America north of Mexico. Smithsonian Institute Press Washington DC.
Volume 1.

Li, S.Y., S.M. Fitzpatrick, J .T. Troubridge, M.J. Sharkey, J .R. Barron, and J .E.
O’Hara.l999. Parasitoids reared from the obliquebanded leafroller (Lepidoptera:
Tortricidae) infesting raspberries. Can. Entomol. 131: 399-404.

Purcell, M.F., and RH. Messing. 1996. Ripeness effects of three vegetable crops on
abundance of augmentatively released Psyttaliaﬂetcheri (Hym.: Braconidae): Improved

sampling and release methods. Entomophaga. 41: 105-115.

Marino, RC, and DA. Landis. 1996. Effect pf landscape structure on parasitoid diversity
and parasitism in agroecosystems. Eco. Appl. 6: 276-284.

141

 

Appendix 1
Record of Deposition of Voucher Specimens'
The specimens listed on the following sheet(s) have been deposited in the named museum(s) as
samples of those species or other taxa. which were used in this research. Voucher recognition
labels bearing the Voucher No. have been attached or included in ﬂuid-preserved specimens.
Voucher No.: 2002-08

Title of thesis or dissertation (or other research projects):

Biological Control of Obliquebanded Leafroller, Chon'stoneura msaceana (Harris) (Lepidoptera:
Tortricidae), in Michigan Apple Orchards.

Museum(s) where deposited and abbreviations for table on following sheets:

Entomology Museum, Michigan State University (MSU)

Other Museums:

USDA-APHIS Niles Plant Protection Center, Niles, Michigan

K. Ahlstrom: NCDA & CS Plant Protection Section, Raleigh, North Carolina
J. O’Hara: ECORC, Systematic Entomology Section, Ontario, Canada

M.J. Sharkey: University of Kentucky, Lexington, Kentucky

M.E. Schauff: Systematic Entomology Laboratory, Washington DC, Maryland

Investigators Name(s) (typed)

 

Tammy K. Wilkinson

 

Date 1 1-19—02

*Reference: Yoshimoto, C. M. 1978. Voucher Specimens for Entomology in North America.
Bull. Entomol. Soc. Amer. 24: 141-42.

Deposit as follows:
Original: Include as Appendix 1 in ribbon copy of thesis or dissertation.

Copies: Include as Appendix 1 in copies of thesis or dissertation.
Museum(s) ﬁles.
Research project ﬁles.

This form is available from and the Voucher No. is assigned by the Curator, Michigan State
University Entomology Museum.

142

 

 

Appendix 1.1

Voucher Specimen Data

 

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143

Appendix 1.1

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Appendix 1.1

Voucher Specimen Data

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Appendix 1.1

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Appendix 1.1

Voucher Specimen Data
Page 5 of 7 Pages

 

 

 

 

 

 

 

 

 

 

 

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Appendix 1.1

Voucher Specimen Data

 

Page 6 of 7 Pages

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Appendix 1.1
Page 7 of 7 Pages

Voucher Specimen Data

 

 

 

 

 

 

 

 

 

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