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thesis entitled

BIOLOGICAL CONTROL OF THE SOYBEAN APHID,
APHIS GLYCINES MATSUMURA
(HOMOPTERA: APHIDIDAE)

 

presented by

TYLER BRYCE FOX

has been accepted towards fulfillment
of the requirements for.

M. S. degree in Entomology

 

 

 

Major professor

Date 13 December, 2002

 

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Michigan State
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6/01 cyclRC/DatoDuo.p65<p. 15

BIOLOGICAL CONTROL OF THE SOYBEAN APHID, APHIS GLYCINES
MATSUMURA (HOMOPTERA: APHIDIDAE)
By

Tyler Bryce Fox

A THESIS
Submitted to
Michigan State University
in partial fulfillment of the requirements
for the degree of
MASTER OF SCIENCE

Department of Entomology

2002

ABSTRACT

BIOLOGICAL CONTROL OF THE SOYBEAN APHID, APHIS GLYCINES
MATSUMURA (HOMOPTERA: APHIDIDAE)

By

Tyler Bryce Fox

Aphis glycines Matsumura is an invasive pest of soybean [Glycine max (L.) Merrill] first
discovered in the United States in 2000. The impact of predation on A. glycines
establishment and population increase was studied in Ingham County, Michigan during
2001-2002. Direct observation and pitfall traps were utilized to determine the species
composition and abundance of potential predators in soybean fields. Laboratory feeding
assays showed that most of the common foliar-foraging and ground-dwelling predators
present in soybean fields were capable of consuming A. glycines. The impact of
predation on A. glycines establishment in the field was examined using clip cages.
Predation significantly reduced A. glycines 24 h survival in four out of six trials over both
years. In a field study during July-August in 2001- 2002, l m2 predator exclusion or
sham cages were used to assess predation impacts on established A. glycines populations.
Cages were initially infested with A. glycines adults and sampled for approximately four
weeks. The 2001 trial was inconclusive, however, in 2002 foliar-foraging predators
prevented population growth in sham cages and dramatically reduced A. glycines
populations where exclusion cages were opened after two weeks. These studies
demonstrate that predator communities can significantly impact A. glycines establishment
and population density in soybean and should be further investigated as a potential means

of managing A. glycines populations in United States soybean production systems.

Dedicated with love to my wife Mari Igarashi Fox, for always loving, encouraging and
supporting me while I was pursuing this degree, and to Naotsugu Igarashi for becoming a

second father and a best friend.

iii

ACKNOWLEDGEMENTS

I must first thank Doug Landis, for showing me that science is a challenge worth
investigating. I greatly appreciate his dedication to investigate unique interactions within
the insect world, and his willingness to share his wealth knowledge with others. I thank
Chris DiFonzo for always assisting me with my numerous aphid-related questions. I also
thank Suzanne Thiem and Kurt Thelen for their guidance during every stage of my
experiments over the past two years. I also thank Fabian Menalled for his guidance with
another project. Fernando Cardoso of the Statistical Consulting Center also deserves and
enormous amount of thanks for his unquestionable devotion to helping me with statistical

questions throughout these studies.

I am indebted to Chris Sebolt for his field assistance and friendship. I also thank my
fellow lab mates Matt O’Neal, Tammy Wilkinson, and Alejandro Costamagna for their
friendship, understanding, and encouragement at all times. I also thank Sandra Clay,
Alison Gould, Andrea McMillian, Andre Ball, Meghan Burns, Michelle Smith, Christy
Hemming, Kathy McCamant, Allison Lewinski, Ben Nessia, and Kevin Newhouse for
their help with fieldwork. Collectively, these folks probably counted more aphids than

there are stars in the sky.

iv

I also thank the Niles APHIS lab for supplying live aphids for my studies. Early season
research would have been nearly impossible without the use of their colony. This work

funded by a Cooperative Agreement with USDA APHIS PPQ.

I am greatly indebted to my family for their overwhelming support and encouragement. I
am very fortunate to have two loving sets of parents in both the United States (Dan
“Fodge” and Cheryl Fox) and Japan (Naotsugu and Kiyo Igarashi) who showed their love

and devotion at all times.

TABLE OF CONTENTS
LIST OF TABLES
LIST OF FIGURES
KEY TO SYMBOLS AND ABBREVIATIONS

CHAPTER 1 Introduction to soybean production, Aphis glycines Matsumura
biology and the importance of biological control

List of References

CHAPTER 2 The impact of indigenous predators on preventing establishment
of the soybean aphid, Aphis glycines Matsumura

Introduction

Materials and Methods

Results

Discussion

List of References

CHAPTER 3 Evaluating the impact of indigenous and exotic predators of the

soybean aphid, Aphis glycines Matsumura, in laboratory no-choice
feeding assays

Introduction

Materials and Methods

Results

Discussion

List of References

CHAPTER 4 Predator effects on soybean aphid, Aphis glycines
Matsumura, population growth

Introduction

Materials and Methods

vi

viii

xii

xvi

14

20

23

28

34

64

67

69

71

73

8O

82

85

Results
Discussion
List of References

APPENDIX A Effects of soybean varieties on Aphis glycines Matsumura
survival and reproduction

APPENDIX B Record of deposition of voucher specimens

vii

89

97

145

148

154

LIST OF TABLES

Table 1.1. Soybean management strategies in four counties of Michigan.
Rotation percentages show the percentage of farmers that use each rotation
within the three counties. Tillage percentages show the percentage of farmers
within the three counties that use particular tillage practices. Row spacing
percentages show the percent of farmers that use specific row spacing within
each county. All surveys were conducted between April 23 and March 13, 2001

Table 2.1. Species composition, total number and percent of total potential A.
glycines predators in five-minute observations in l m x 30 cm areas of soybean
during trial one (7-8 June 2001), trial two (14-15 June 2001), and trial three (24-
25 June 2001), East Lansing, Michigan

Table 2.2. Species composition, total number, and percent of total potential A.
glycines predators in three-minute observations in l m x 30 cm areas of soybean
during trial one (18-19 June 2002), trial two (24-25 June 2002), and trial three
(2-3 June 2002), East Lansing, Michigan

Table 2.3. Species composition, total number, and percent of total of predators
collected in pitfall traps in refuge and control plots during trial one (7-8 June
2001), trial two (14-15 June 2001), and trial three (24-25 June 2001), East

Lansing, Michigan

Table 2.4. Species composition, total number, and percent of predators
collected in pitfall traps during trial one (18-19 June 2002), trial two (24-25 June
2002), and trial three (2-3 July 2002), East Lansing, Michigan

Table 2.5. Probability of a greater F -statistic based on the proportion of live
adult A. glycines remaining in refuge and control plots under different cage
treatments during 2001, East Lansing, Michigan

Table 2.6. Probability of a greater F -statistic based on the number of A. glycines
nymphs produced per cage in refuge and control plots under different cage
treatments during 2001, East Lansing, Michigan

Table 2.7. Probability of a greater F -statistic based on the total number (adults
+ nymphs) of live A. glycines in refuge and control plots under different cage
treatments during 2001, East Lansing, Michigan

Table 2.8. Probability of a greater F -statistic based on the proportion of live

adult A. glycines remaining under different cage treatments during 2002, East
Lansing, Michigan

viii

13

39

40

41

42

43

45

46

Table 2.9. Probability of a greater F —statistic based on the number of A. glycines
nymphs produced per cage in soybean plots under different cage treatments
during 2002, East Lansing, Michigan

Table 2.10. Probability of a greater F -statistic based on the total number (adults
+ nymphs) of live A. glycines under different cage treatments during 2002, East
Lansing, Michigan

Table 3.1. Number of A. glycines surviving and percent mortality of A. glycines
in 24 h no-choice feeding trials consumed by foliar-foraging predators from 8
June to 10 August 2001, East Lansing, Michigan

Table 3.2. Number of A. glycines surviving and percent mortality of A. glycines
in 24 h no-choice feeding trials consumed by ground-dwelling predators from 8
June to 10 August 2001, East Lansing, Michigan

Table 3.3. Estimated seasonal occurrence of foliar-foraging predators during
2001, East Lansing, Michigan

Table 3.4. Estimated seasonal occurrence of ground-dwelling predators during
2001, East Lansing, Michigan

Table 4.1. Species composition, total, and percent predators observed during 3-
minute non-intrusive and intrusive observations in exclusion and open cages
during 2001. Exclusion cages were sampled once a week from 26 June to 31
July and open cages were sampled from 26 June to 4 September, East Lansing,
Michigan

Table 4.2. Species composition, total, and percent ground dwelling predators
captured per seven days in exclusion cages versus those in the surrounding field
during 2001. Pitfalls were sampled once a week from 26 June to 31 July, 2001,
East Lansing, Michigan

Table 4.3. Probability of a greater F -statistic based on results of temperature
difference (°C interior minus oC exterior) of open, exclusion, and frame cages
during trial one, 2002

Table 4.4. Probability of a greater F -statistic based on results of temperature
difference (°C interior minus °C exterior) of open, exclusion, and frame cages
during trial two, 2002

Table 4.5. Probability of a greater F -statistic based on results of relative

humidity difference (interior minus exterior) of open, exclusion, and frame cages
during trial one, 2002

ix

47

48

76

77

78

79

102

103

104

105

106

Table 4.6. Probability of a greater F -statistic based on results of relative
humidity difference (interior minus exterior) of open, exclusion, and frame cages
during trial two, 2002

Table 4.7. Probability of a greater F -statistic based on results of plant height
(based on measurement of five random plants) in exclusion, open, and frame
cages during trial one, 2002

Table 4.8. Probability of a greater F -statistic based on plant height (based on
measurement of five random plants) in exclusion, open, and frame cages during
trial two, 2002

Table 4.9. Species composition, total, and percent of ground dwelling predators
captured per seven days in exclusion cages (2 pitfall traps/cage) versus those
placed randomly throughout the study area in trial one (28 June to 29 July) and
trial two (12 July to 12 August), 2002, East Lansing, Michigan

Table 4.10. Probabilities of a greater F -statistic based on results of total pitfall
captures of ground-dwelling predators in exclusion cages versus those in the
study area (plot) during trial one, 2002

Table 4.11. Probability of a greater F -statistic based on results of total pitfall
captures of ground-dwelling predators in exclusion cages versus those in the
study area (plot) during trial two, 2002

Table 4.12. Probability of a greater F -statistic based the number of adult A.
glycines in 1 1112 open, exclusion and frame cages during trial one, 2002

Table 4.13. Probability of a greater F -statistic based on the number nymph A.
glycines in l m2 open, exclusion and frame cages during trial one, 2002

Table 4.14. Species composition, total, and percent predators observed during
3-minute non-intrusive and intrusive observations in exclusion, open, and frame
cages prior to cage switch during trial one, (28 June to 12 July), 2002, East
Lansing, Michigan

Table 4.15. Species composition, total, and percent of predators observed
during 3-minute non-intrusive and intrusive observations in exclusionl, open,
and frame cages after cage switch (15 July to 29 July) during trial one, 2002

Table 4.16. Probability of a greater F -statistic based on predators observed
during 3-minute non-intrusive and intrusive observations in exclusion, open, and
frame cages during trial one, 2002

107

108

109

110

111

112

113

114

115

116

117

Table 4.17. Probability of a greater F -statistic based on number adult A.
glycines in l m2 open, exclusion and frame cages during trial two, 2002

Table 4.18. Probability of a greater F -statistic based on results of nymph A.
glycines produced in 1 m2 open, exclusion and frame cages during experiment
two, 2002

Table 4.19. Species composition, total, and percent of total predators observed
during 3 minute non-intrusive and intrusive foliar observations in exclusion,
open, and frame cages prior to cage switch during (12 July to 26 July) tn'al two,
2002, East Lansing, Michigan

Table 4.20. Species composition, total, and percent of total predators observed
during 3-minute non-intrusive and intrusive foliar observations in exclusionl,
open, and frame cages after cage switch (29 July to 12 August) during trial two,
2002. This part of the experiment was conducted from during 2002, after open
and exclusion cages were switched, East Lansing, Michigan

Table 4.21. Probability of a greater F -statistic based on the number of predators
observed during 3-minute non-intrusive and intrusive foliar observations in
exclusion, open, and frame cages during trial two, 2002

Table 1. Mean number (1'. SEM) of adult A. glycines remaining and offspring
produced on six different varieties of soybean at 24 h (day 1), 48 h (day 2), and
72 h (day 3) during trial one

Table 2. Mean number (_-I_- SEM) of adult A. glycines remaining and offspring
produced on six different varieties of soybean at 24 h (day 1), 48 h (day 2), and
72 h (day 3) during trial two

Table 3. Mean number (i SEM) of adult A. glycines remaining and offspring

produced on six different varieties of soybean at 24 h (day 1), 48 h (day 2), and
72 h (day 3) during trial three

xi

118

119

120

121

122

151

152

153

LIST OF FIGURES

Figure 1.1. Distribution of A. glycines in Michigan. Dotted counties indicate the
presence of A. glycines during sampling. Dark colored counties indicate
infestation levels of 100 or more aphids per leaf during sampling. Dr. Chris
DiFonzo, Michigan State University, Personal Communication.

Figure 2.1. Layout of the 2001 field location on the Michigan State University
Entomology Farm, East Lansing, Michigan. The fields were separated into four
blocks, each containing a refuge and control plot. Enlarged plots illustrate where
pitfall traps and foliar sampling areas were located, and where clip cages were
placed.

Figure 2.2. Mean number (i SEM) of predators observed in l m x 30 cm areas
during; A. 5- minutes in trial one (7-8 June 2001), trial two (14-15 June 2001),
and trial three (24-25 June 2001) and; B. 3-minutes during trial one (18-19 June
2002), trial two (24-25 June 2002), and trial three (2-3 July 2002), East Lansing,
Michigan.

Figure 2.3. Mean number (i SEM) of predators per trap per day collected in 32
pitfall traps; A. located in refuge and control plot during trial one (7-8 June 2001),
trial two (14-15 June 2001), and trial three (24-25 June 2001); B. in 30 pitfall traps
in five blocks during trial one (18-19 June 2002), trial two (24-25 June 2002), and
trial three (2-3 July 2002), East Lansing, Michigan.

Figure 2.4. Percentage of live adult A. glycines remaining at 15 and 24 h for the
open, leaky and exclosure treatments in refuge and control plots during; A. trial
one (7-8 June 2001); B. trial two (14-15 June 2001); and C. trial three (24-25 June
2001), East Lansing, Michigan. Different letters above bars within an hour
denotes significant (P g 0.1) differences among open, leaky, and exclosure
treatments (Poisson regression test).

Figure 2.5. Number of live A. glycines nymphs at 15 and 24 h in three cage
treatments during; A. trial one (7-8 June 2001); B. trial two (14-15 June 2001);
and C. trial three (24-25 June 2001), East Lansing, Michigan. Different letters
above bars within an hour denote significant (P 5 0.1) differences in the number
of nymphs present in open, leaky, and exclosure treatments (Poisson regression
(log-linear model) test).

Figure 2.6. Total number of live adult and nymph A. glycines at 15 and 24 h in h
in three cage treatments during 1) trial one (7-8 June 2001), 2) trial two (14-15
June 2001) and 3) trial three (24-25 June 2001), East Lansing, Michigan. Different
letters above bars within an hour denote significant (P 5 0.1) differences among
open, leaky, and exclosure treatments (Poisson regression (log-linear model) test).

xii

12

49

50

51

53

55

57

Figure 2.7. Percentage of live adult A. glycines remaining at 15 and 24 h for the
open, leaky and exclosure treatments in during; A. trial one (18-19 June 2002); B.
trial two (24-25 June 2002); and C. trial three (2-3 July 2002), East Lansing,
Michigan. Different letters above bars within an hour denote significant
differences among open, leaky, and exclosure treatments (Poisson regression test).

Figure 2.8. Number of live nymph A. glycines at 15 and 24 h in three cage
treatments during; A. trial one (18-19 June 2002); B. trial two (24-25 June 2002);
and C. trial three (2-3 July 2002), East Lansing, Michigan. Different letters above
bars within a given hour denote significant (P 5 0.1) differences in the number of
nymphs present in open, leaky, and exclosure treatments (Poisson regression (log-
linear model) test).

Figure 2.9. Total number of live adult and nymph A. glycines at 15 and 24 h in
three cage treatments during; A. trial one (18-19 June 2002); B. trial two (24-25
June 2002) and C. trial three (2-3 July 2002), East Lansing, Michigan. Different
letters above bars within a given hour denote significant (P 5 0.1) differences
among open, leaky, and exclosure treatments (Poisson regression (log-linear
model) test).

Figure 4.1. Design of 1 m2 cages used during 2001-2002. Both cage types
contain the same cage materials to account for potential cage effects. A. open and
B. exclusion.

Figure 4.2. Mean (i SEM) temperature difference (°C interior minus the oC
exterior) of open and exclusion cages during 2001, East Lansing, Michigan.

Figure 4.3. Mean (i SEM) relative humidity difference (interior minus the
exterior) of open and exclusion cages during 2001, East Lansing, Michigan.

Figure 4.4. Mean height (t SEM) in cm of five randomly selected soybean plants
in the open and exclusion treatments during 2001, East Lansing, Michigan.

Figure 4.5. Mean (i SEM) abundance of foliar-foraging predators based on a
combination of 3-minute non-intrusive visual examination followed by hand
examinations of foliage in the Open and exclusion treatments during 2001, East
Lansing, Michigan.

Figure 4.6. Mean (1- SEM) abundance of Harmonia axyridis adults and larvae
based on a combination of 3-minute non-intrusive visual examination followed by
hand examinations of foliage in the open and exclusion treatments during 2001,
East Lansing, Michigan.

xiii

59

61

63

123

124

125

126

127

128

Figure 4.7. Mean (i SEM) abundance of Orius insidiosus adults and nymphs
based on a combination of 3-minute non-intrusive visual examination followed by
hand examinations of foliage in the open and exclusion treatments during 2001,
East Lansing, Michigan.

Figure 4.8. Mean (i SEM) adult A. glycines population per 5 plant tips during
2001 in open and exclusion cages during 2001, East Lansing, Michigan.

Figure 4.9. Mean (i SEM) nymph A. glycines population during 2001 in Open
and exclusion treatments during 2001, East Lansing, Michigan.

Figure 4.10. Mean (1- SEM) abundance Of Harmonia axyridis (Pallas) found on
sticky traps in the exclusion cages versus those found in the entire plot during
2001, East Lansing, Michigan.

Figure 4.11. Mean (i SEM) abundance of Orius insidiosus (Say) found on sticky
traps in the exclusion cages versus those found in the entire plot during 2001, East
Lansing, Michigan.

Figure 4.12. Mean (i SEM) predator/pitfall trap/day of ground beetles in pitfall
traps in exclusion cages versus those in the study area during 2001, East Lansing,
Michigan.

Figure 4.13. Mean (i SEM) temperature difference (°C interior minus the oC
exterior temperature) in open, exclusion, and frame cages during 2002. The arrow

indicates when open and exclusion cages over 1 m2 plots were switched during: A.

Trial one; and B. Trial two. One randomly selected replicate had cages that were
not switched to show the trend if cages were not switched.

Figure 4.14. Mean (i SEM) relative humidity difference (interior minus the
exterior) in open, exclusion, and frame cages during 2002. The arrow indicates
when open and exclusion cages over 1 in2 plots were switched during: A. Trial
one; and B. Trial two. One randomly selected replicate had cages that were not
switched to show the trend if cages were not switched.

Figure 4.15. Mean (i SEM) plant height per five plants in open, exclusion, and
frame cages during 2002. The arrow indicates when open and exclusion cages
over 1 m plots were switched during: A. Trial one; and B. Trial two. One
randomly selected replicate had cages that were not switched to show the trend if
cages were not switched.

xiv

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131

132

133

134

135

136

137

Figure 4.16. Mean (1 SEM) abundance of carabid beetles collected per seven
days in 10 total pitfall traps from exclusion cages (2 traps/ cage) versus 10 total
pitfall traps placed randomly in the study area during 2002: A. Trial one; and B.
Trial two. The arrow indicates when open and exclusion cages over 1 m2 plots
were switched, at which time eight pitfall traps were in exclusion cages and eight
within the plot.

Figure 4.17. Mean (i SEM) adult (A.) and nymph (B.) A. glycines population
(log scale) per ten whole plants in Open, exclusion, and frame cages in trial one
during 2002. The arrow indicates when open and exclusion cages over 1m2 plots
were switched. One randomly selected replicate had cages that were not switched
to show the trend if cages were not switched.

Figure 4.18. Mean (i SEM) adult (A.) and nymph (B.) A. glycines population
(log scale) per ten whole plants in open, exclusion, and frame cages in trial one
during 2002. An arrow indicated when Open and exclusion cages over 1m2 plots
were switched. One randomly selected replicate had cages that were not switched
to show the trend if cages were not switched.

Figure 4.19. Mean (i SEM) abundance of foliar-foraging predators based on a
combination of 3-minute non-intrusive visual examination followed by hand
examinations of foliage in the open, exclusion, and frame treatments during 2002.
The arrow indicates when open and exclusion cages over 1 in2 plots were switched
during: A. Trial one; and B. Trial two. One randomly selected replicate had cages
that were not switched to show the trend if cages were not switched.

Figure 4.20. Mean (1- SEM) abundance of Harmonia axyridis (Pallas) adults
based on a combination of 3-minute non-intrusive visual examination followed by
hand examination of foliage in the open, exclusion, and frame treatments during
2002. The arrow indicates when open and exclusion cages over 1 m2 plots were
switched during: A. Trial one; and B. Trial two. One randomly selected replicate
had cages that were not switched to show the trend if cages were not switched.

Figure 4.21. Mean (i SEM) abundance of Leucopis midge larvae in based on a
combination of 3-minute non-intrusive visual examination followed by hand
examinations of foliage in the open, exclusion, and frame treatments during 2002.
The arrow indicates when open and exclusion cages over 1 m2 plots were switched
during: A. Trial one; and B. Trial two. One randomly selected replicate had cages
that were not switched to show the trend if cages were not switched.

Figure 4.22. Mean (i SEM) abundance of Orius insidiosus (Say) based on a
combination Of 3-minute non-intrusive visual examination followed by a hand
examinations of foliage in the open, exclusion, and frame treatments during 2002.
The arrow indicates when open and exclusion cages over 1 m2 plots were switched
during: A. Trial one; and B. Trial two. One randomly selected replicate had cages
that were not switched to show the trend if cages were not switched.

XV

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139

140

141

142

143

144

AN OVA
0C

cm

df

ha

L:D

ns

RH

SEM

spp.

KEY TO SYMBOLS AND ABBREVIATIONS

analysis of variance
degrees Celsius
centimeters

days

degrees of freedom
F -statistic

hours

hectare

liter

light: dark hours
meters

number of observations

not significant

probability under the assumption that the null hypothesis is true

relative humidity
standard error of the mean
species

t-statistic

xvi

CHAPTER 1

Introduction to soybean production, Aphis glycines Matsumura biology and the

importance of biological control

Introduction

Prior to the summer of 2000, no aphid species was known to regularly colonize
soybean, Glycine max (L.), in the United States (DiFonzo 2000). However, in 2000
Aphis glycines Matsumura, an invasive aphid species from Asia, was discovered infesting
soybean plants in the United States. First observed in Wisconsin in July 2000, the aphid
was initially thought to be the melon aphid, Aphis gossypii (Glover). The positive
identification of A. glycines prompted surveys in surrounding states in the summer of
2000 and 2001. As of 2001, the current distribution of A. glycines included MN, IL, IA,
IN, MI, ND, KY, OH, WI, and NY (University of Minnesota Web Site, North Dakota
State University). In 2002, it had spread to NE, KS, DE, MN, GA, and MS (Ragsdale
Pers. Comm.). In Michigan A. glycines is distributed primarily in the central and
southern portions of the state, with the most severe infestations occurring in the
southwestern counties during 2000 and the southeastern counties during 2001 (DiFonzo
2001, Figure 1.1). Aphis glycines populations in Michigan during 2002 presumably
occurred in most soybean growing regions of the states; however, populations remained
low.

Aphis glycines is a serious pest of soybean in Asia and has the potential to

negatively impact soybean production in Michigan and the entire United States. Aphis

glycines feeding can cause up to a 20.2 cm reduction in growth and a 27.8 percent
reduction in seed yield (Wang et a1. 1996). In 2000, up to a 13 percent yield reduction
occurred in replicated field plots in Wisconsin during the year 2000 (University of
Minnesota Extension Service Web Site). In 2001, A. glycines caused up to 40 percent
yield loss in Michigan (DiFonzo, Pers. Comm). This pest can indirectly harm soybean
plants by vectoring persistent viruses, such as soybean dwarf virus, millet red leaf and
non-persistent viruses such as soybean stunt virus, soybean mosaic virus, bean yellow
mosaic virus, beet mosaic, and mung bean mosaic (Halbert et al. 1986, Van den Berg et
al. 1997, Fletcher and Desborough 2000). Epidemics of soybean mosaic potyvirus in
summer-sown soybean fields in Jiangsu, China are closely related to the timing of A.
glycines immigration (Li and Pu 1991). Virus transmission by aphids has not yet been
observed in United States (DiFonzo Pers. Comm.). In addition, aphids also cause indirect
damage by excreting honeydew onto foliage which promotes the growth of sooty molds
that have the potential to reduce the photosynthetic capacity of the darkened leaves
(Lenné and Trutmann 1994, Hirano et a1. 1996, DiFonzo 2000, Ostlie and Hutchinson
2000).

Due to its recent arrival in the United States, the ideal way to manage A. glycines
in North America is not known. Insecticides have been used as a short-term solution on
other aphid species, but studies show that insecticide treatments often fail to significantly
reduce aphid populations and can disrupt control by predatory insects (Asin and Pons
1999, Wilson et a1. 1999, Jansen 2000). The potential for predators to control this pest in
the United States is also not well understood, though they have shown to be important in

Asia (Van den Berg et a1. 1997, Chang et a1. 1994). Many sources have illustrated that

aphidophagous predators can reduce aphid populations (Grasswitz and Burts 1995, Star)?
1995, Van den Berg et a1. 1997, Obrycki and Kring 1998). However, generalist natural
enemies can also play crucial roles in biological control (Hance 1987; Landis and Van
der Werf 1997; Chang and Kareiva 1999, Symondson et a1. 2002). Moreover, conserving
predatory insects through habitat management may enhance both specialist and generalist
predator activity (Tonhasca 1993, Menalled et al. in review, Carmona and Landis 1999,
Landis et a1. 2000, Lee and Landis 2002, Lee et a1. 2001). Therefore, the potential for
indigenous and exotic predators to aid in the control of this pest with and without

conservation enhancement were examined.

Introduction to Soybean Value and Ecology

Glycine max (L.) is a very important crop in Michigan and other parts of the
United States. As a source of protein, soybean is often more inexpensive on a cost-per-
kilogram basis than animal protein (Hymowitz and Newell 1981). Moreover, soybean
contains 20 to 23 percent oil, a component commonly used in margarine, shortening,
mayonnaise, and dressing. Soybean meal is commonly used as a major source of protein
in animal feeds (Hymowitz and Newell 1981). The production of soybean in Michigan
totaled 74.9 million bushels during the year 2000 harvest and the average yield was 36
bushels per acre (Michigan Agricultural Statistics 2000-2001). According to Michigan
Agricultural Statistics (2000-2001), the price of soybean per bushel received by farmers
in 2000 was $4.75 in Michigan. While this is lower than historical prices, it is still an

attractive alternative to corn ($1.90/bu) and wheat ($2.10/bu).

Soybean Management

Soybean production methods vary from region to region within Michigan.
Typical soybean production practices for several of the aphid infested soybean-producing
regions of the state are presented in Table 1.1. Overall soybean fits into several different
rotations, frequently following corn. Most Michigan producers seem to be following
reduced tillage with a large proportion of the acreage being produced in drilled, narrow
rows (< 76 cm). These production practices have the potential to influence management

Of the A. glycines.

Biology and Life Cycle of Aphis glycines Matsumura

A major challenge in this research is that while extensive literature on A. glycines
exists, a majority of it is in Japanese, Korean, and Chinese language journals, and only a
limited number of manuscripts have been translated to English at this time (Kansas State
University Web Site 2001). The following contains the majority of the literature
currently available in English. Unfortunately, some of the literature is only available
through secondary sources and translated abstracts, putting limitations on knowledge of
previous research.

Like all insects, A. glycines development is affected by temperature. Laboratory
research showed the intrinsic rate of increase of A. glycines was higher at 27° C than at
22° C (Hirano et al. 1996). Hirano et a1. (1996) also found that mean daily fecundity rose
at a more rapid rate, peaked earlier, and declined faster at 27° C than at 22° C. It also has

been stated that the optimum temperatures for A. glycines development in late June to

early July are between 22 and 25° C, with a relative humidity less than 78 percent in
China (Wang et a1. 1962).

In Asia, A. glycines requires soybean and Rhamnus davurica (buckthom) to
complete its life cycle (Blackman and Eastop 2000). Four Rhamnus spp. are currently
distributed in Michigan, R. alnifolia ‘Her’ (Alderleaf buckthom), R. cathartica L.
(Common buckthom), R. utilis Dcne (Chinese buckthom), and R. frangula L. (Glossy
buckthom) (Voss 1998). Another source suggests a fifth species, R. davurica Pallas, is
also present in the state (USDA Natural Resources Conservation Services Plants Data
Base).

The life cycle of A. glycines is complex. In late fall, female oviparae lay eggs on
Rhamnus species, after mating with males. Nymphs hatch in spring and the species
undergoes two generations of Wingless females, followed by a winged generation of
females. These winged females leave Rhamnus in search of soybean, their summer host.
Once on soybean, there are generations of Wingless and winged females, the latter
leaving their natal site in search of new soybean plants when crowding occurs. In fall,
males develop on soybean plants, fly to Rhamnus, and mate with oviparae on Rhamnus.
These mated females then lay eggs on the inner margins of buds on Rhamnus twigs
(Blackman and Eastop 2000).

Guang-xue and Tie-sen (1982) observed hybridization between Aphis glycines
and Aphis gossypii, the melon aphid, under artificial conditions. The authors found that
the hybrid offspring reproduced both parthenogenetic and sexual forms to complete their
life cycle. They hypothesized that this potential for hybridization may result in aphid

lines more resistant to certain chemical insecticides, but this has not been tested.

Aphidophagous Predators

Aphidophagous predators can greatly contribute to the reduction of a wide variety
of aphid species (Grasswitz and Burts 1995, Star)? 1995, Van den Berg et a1. 1997,
Obrycki and Kring 1998). For example, it was found that a complex of natural enemies,
including Chrysopa nigricomis Burmeister, Orius spp., Coccinella transversoguttata
Faldermann, Hippodamia convergens Guerin, and various species of Syrphidae and
Chamaemyiidae all contributed to the reduction of Aphis pomi De Geer in a field study
using apple trees (Grasswitz and Burts 1995). Similarly, Star)? (1995) found that
Coccinella septempunctata L., Adalia bipunctata (L.), and Episyrphus balteatus (De
Geer) were common predators that consumed, and thus aided in control, of the Spiraea
aphid, Aphis spiraephaga Muller in Czechoslovakia.

Furthermore, it is known that in Asia, coccinellid (Harmonia spp.) predators play
an important role in suppressing A. glycines populations in soybean fields in tropical
areas of Southeast Asia (Van den Berg et al. 1997). Other aphidophagous predator
species, such as Nabis spp., Harmonia axyridis (Pallas), Coccinella septempunctata L.,
and Chrysopa spp. aided in its control during the mid to late season in China (Han 1997).
Schneider (1971) reported the predaceous syrphid larva Ischiodon escutellaris (F.) in the
Philippines was another aphidophagous predator that fed on a wide variety of aphids,
including A. glycines. However, low syrphid abundance in comparison to the number of
aphids has not resulted in suppression of aphid populations by syrphids, though they do

contribute aphid reduction (Alfiler and Calilung 1978, Van den Berg et a1. 1997).

In Asia, coccinellid predators (Harmonia spp.) and to a much lesser extent
syrphid predators, depend on aphids as a food source and reduce A. glycines populations,
but their effects are not as significant in temperate versus tropical climates (Van den Berg
1997). At lower temperatures it was found that the reproductive rate of A. glycines
exceeded the predation rate of the coccinellid predators (Van den Berg et a1. 1997). This
allowed A. glycines populations to rapidly develop in temperate regions, particularly
during the early portion of the season (Van den Berg et al. 1997). A similar result has
been documented for Coccinnella spp. attacking pea aphids, Acyrthosiphon pisum
(Harris), British Columbia (Frazer and Gilbert 1976)

Parasitoids of A. glycines have also been identified in Taejon, Korea and reports
suggest that Ephredrus plagiator (Hymenoptera: Braconidae) might be a potential
biological control agent because they are less frequently attacked by hyperparasitoids
(Chang et a1. 1994). Foraging predators searching for aphids accidentally consume some
larvae of parasitoids (Taylor et a1. 1998). Taylor et a1. (1998) found that aphid
parasitoids respond to the presence of predators by reducing residence time and
oviposition in patches containing aphid predators. This interaction is not completely
understood, but it is thought that the parasitoids perceive chemical cues produced by
either the predators or aphids. Even when the introduction of specific parasitoids resulted
in spectacular success of biological control of the pest, the importance of other predators

should not be ignored (Takagi 1999).

Generalist Predators

The role of aphidophagous predators in control of A. glycines in the United States
is not currently known. One of the main benefits of generalist predators is that they may
help to reduce pest populations when specialized predators are not available (Symondson
et al. 2002). One example is that of the Colorado potato beetle, Leptinotarsa
decemlineata (Say), which has few specialized natural enemies. Hilbeck et a1. (1997)
found that generalist predators have the ability to significantly reduce the abundance of
Colorado potato beetle eggs during their three-year field study. Similarly, it was found
that immigration of generalist lycosid spiders and carabids into a garden area exerted
sufficient biological control of the striped cucumber beetle, Acalymma vittata F., the
spotted cucumber beetle, Diabrotica undecimpunctata howardi Barber, and the squash
bug, Anasa tristis De Geer, to increase the fruit production of squash (Snyder and Wise
1999). Furthermore, three carabid species, Asaphidion flavipes (L.), Agonum dorsale
(Pont.) and Pterostichus melanarius (111.) all reduced populations of Aphisfabae Scopoli,
a pest of sugar beet, in caged experiments. Further, it has been shown that a complex of
ground-dwelling predators, such as carabids, staphylinids, and spider, all contributed to
the reduction of the bird cherry-oat aphid, Rhopalosiphum padi (L.), populations (Ostman
et a1. 2001).

While generalist predators may not be as effective as specialists, they can make
up for this by being present earlier in the season (Chang and Kareiva 1999). Early in the
growing season, pest density is low but populations build up and may reach outbreak
status late in the season (Takagi 1999). Thus, the early season might be an important

time for generalists to reduce pest density before they have an opportunity to initiate large

colonies. For example, Landis and Van der Werf (1997) found many species of carabids
in sugar beet fields in the Netherlands, along with spiders and a dominant generalist
predator, Cantharis lateralis (Coleoptera: Cantharidae) early in the season. They found
that early season predation by generalists played a key role in suppressing the spread of
aphid-vectored viruses and allowed for season-long reduction of aphid populations.
Early season predation by generalist predators may also be important because these
predators are capable of locating alternate food sources when the pest population is low

(Chang and Kareiva 1999, Symondson et a1. 2002).

Effects of Pesticides on Aphid Predators

The negative effects of insecticides on beneficial insects are well documented
(Wilkinson et al. 1979, Bellows and Morse 1993, Epstein et al. 2000). In Belgium, use of
insecticides using fluvalinate and esfenvalerate to control cereal aphids in wheat was
detrimental to coccinellids and pirimicarb was found to be harmful to syrphid larvae
(Jansen 2000). Jansen (2000) also reported that cyfluthrin, deltamethrin and phosalone
reduced catches of both syrphid and coccinellids in wheat fields. Similarly, higher
numbers of melon aphids, A. gossypii, occurred in cotton treated with thiodicarb than in
unsprayed cotton due to its negative effect on aphidophagous predators (Wilson et al.
1999). Similarly, it was found that at planting treatments of carbofuran negatively
affected populations of carabid beetles and that maize aphid, Rhopalosiphum padi (L.),
populations became higher in carbofuran treated plots compared to control plots. In
conventional and no-tillage situations, chloropyrifos, DPX-43898, fonofos, and terbufos,

all granular insecticides, negatively affected carabid beetles (Reed et a1. 1992). Certain

herbicides may also negatively affect predators. Brust (1990) found that glyphosate and

paraquat acted as repellents to certain species of carabid beetles.

Importance of Conservation Biological Control

The aim of conservation biological control is to enhance the overall survival
impact of natural enemies (Debach and Rosen 1991). This can be accomplished by
manipulating the environment to reduce harmful factors and to increase favorable
conditions (Landis et a1. 2000). Reducing direct mortality, providing supplementary
resources, controlling secondary enemies, and manipulating host plant attributes are the

main approaches to natural enemy conservation (Debach and Rosen 1991).

Importance of Habitat Management

Habitat management is considered a subset of conservation biological control
(Pickett and Bugg 1998, Landis et a1. 2000). A number of studies show the significance
of habitat management in increasing predator abundance. For example, in the United
Kindom, species richness of generalist predators (spiders, carabids, and heteropterans)
was greater in non-cropped headlands on the outer six meters of arable fields (Hassall et
al. 1992). Canola flowers in an adjacent crop area to wheat crops were an important food
source for adult syrphid flies, which flew to the wheat crop to oviposit (Bowie et a1.
1999). Furthermore, carabid beetles in upland rice fields were significantly more
abundant in plots that contain piles or strips of weeds and staphylinid beetles were more
abundant in mulched plots (Afun et a1. 1999). Undisturbed semi-natural habitats and

extensively managed field margins were found to be important overwintering sites for

10

predatory arthropods, including staphylinids, carabids, and spiders (Pfiffner and Luka
2000).

Management practices of the crops themselves can also have an influence on
predators. In Michigan, researchers have been working to increase generalist predators in
Michigan corn, soybean and wheat rotations (Carmona and Landis 1999; Landis et al.
2000; Lee and Landis 2002; Lee et al. 2001). They have found that grassy refuge strips
with cover crops and reduced tillage can increase the number of species and the overall
abundance of generalist predators in crop fields adjacent to the refuge habitats, by
providing overwintering sites, alternate food sources and cover from crop management

practices.

Objectives

The purpose Of these studies was to evaluate the impacts of indigenous and exotic
predators on A. glycines with and without habitat management. The specific objectives
were to:
1. To determine the importance of early-season predation on A. glycines by exotic and
indigenous predators.
2. To determine which exotic and indigenous foliar and ground-dwelling predators are
capable of consuming A. glycines.
3. To determine the ability of exotic and indigenous predators to reduce establishing

aphid colonies during mid to late season.

11

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

III?

 

Distribution as of Distribution as of
October 2000 October 2001
Figure 1.1. Distribution of A. glycines in Michigan. Dotted counties indicate the
presence of A. glycines during sampling. Dark colored counties indicate
infestation levels of 100 or more aphids per leaf during sampling. Dr. Chris

DiFonzo, Michigan State University, Personal Communication.

Table 1.1. Soybean management strategies in four counties of Michigan. Rotation

percentages show the percentage of farmers that use each rotation within the three

counties. Tillage percentages show the percentage of farmers within the three counties

that use particular tillage practices. Row spacing percentages show the percent of

farmers that use specific row spacing within each county. All surveys were conducted

between April 23 and March 13, 2001

 

 

 

County: Saginaw (M. Gratiot (D. Rossman Monroe (N. Berrien (M.
Seamon Pers. Pers. Comm.) Birkey Pers. Staton Pers.
Comm.) Comm.) Comm.)
Rotations C-S 30 % C-S 40 % C-S 35 % C-S 60%
C-S-W 10% C-S-W 20 % C-S-W 50 % C-S-W 6-10%
S-SB-S-C 30% 8-8 < 10 % 8-8 40% S-S 34-30%
S-W-SB-C 15% SB-C-DB-W-S 20 % C-S-Vegetable
S-W-S-W 10 % 15 %
Tillage No till 50% No till 35 % No till 50 % No till 40%
(Preceding Fall chisel plow 40 % Fall chisel plow including Minimum tillage Fall chisel
soybeans) Moldboard plow 10% field cultivation in spring 50% plow 60%
60 %
Moldboard plow and all
Others 5%
Row 7 1/2” 50% (70% 7 V2” 60 % (use no till) 7 V2” 50 % (No 7 V2” 70% (No
spacing conventional tillage, 15" 5 % till) till) 30” 30%
30 % no till) 30” 35 % (drilled) 15”, 20” and 30” (chisel/disc
20 or 22” 10% (90% equals the combo, though
conventional, 10% no remainder a few also
till) incorporate no
28 or 30" 40% (40% tillage)
conventional, 60% no
till)
Key:
S=soybean
W=wheat
DB: dry beans
C: corn

SB: sugar beets

13

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18

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19

CHAPTER 2
The impact of indigenous predators on preventing establishment of the soybean

aphid, Aphis glycines Matsumura

Introduction

The soybean aphid, Aphis glycines Matsumura, is an exotic pest from Asia that
was discovered in the United States in 2000. In Asia, A. glycines feeding can cause up to
a 20 cm reduction in growth and a 27.8 percent reduction in seed yields (Wang et al.
1996). In 2000, A. glycines caused up to a 13 percent yield reduction in replicated field
plots in Wisconsin (University of Minnesota Extension Service Web Site). In 2001, it
was found that A. glycines caused up to a 40 percent sprayed versus unsprayed yield loss
in Michigan (Difonzo, Pers. Comm). This pest can also indirectly harm soybeans by
vectoring persistent viruses, such as soybean dwarf virus and non-persistent viruses, such
as soybean stunt virus, soybean mosaic virus, and bean yellow mosaic virus (Van den
Berg et al. 1997). Epidemics of soybean mosaic potyvirus in summer-sown soybean
fields in Jiangsu, China were found to be closely associated to the timing of A. glycines
immigration (Li and Pu 1991). In addition, aphids also cause indirect damage by
excreting honeydew onto foliage, which promotes the growth of sooty molds that reduce
the photosynthetic capacity of the leaves (Lenné and Trutmann 1994, Hirano et al. 1996).

Aphidophagous predators can greatly contribute to the reduction of a wide variety
of aphid species (Grasswitz and Burts 1995, Stary 1995, Van den Berg et al. 1997,

Obrycki and Kring 1998). For example, a complex of natural enemies, including

20

Chrysopa nigricornis Burmeister, Orius spp., Coccinella transversoguttata Faldermann,
Hippodamia convergens Guerin, and several species of Syrphidae and Chamaemyiidae
all contributed to reductions in Aphis pomi De Geer in a field study on apple (Grasswitz
and Burts 1995). Similarly, Stary (1995) found that Coccinella septempunctata L.,
Adalia bipunctata (L.), and Episyrphus balteatus (De Geer) were common predators that
all consumed and thus aided in control of the spiraea aphid, Aphis spiraephaga Muller in
Czechoslovakia.

Furthermore, it is known that in Asia that coccinellid (Harmonia spp.) predators
play an important role in suppressing A. glycines populations in soybeans (Van den Berg
et al. 1997). Other predator species, such as Nabis spp., Harmonia axyridis (Pallas),
Coccinella septempunctata L., and Chrysopa spp. have been shown to aid in A. glycines
control during the mid to late season in China (Han 1997).

Schneider (1971) reported the predaceous syrphid larva Ischiodon escutellaris (F .)
in the Philippines was another aphidophagous predator that fed on a wide variety of
aphids, including A. glycines. However, low syrphid abundance in comparison to the
number of aphids has not caused suppression of aphid populations by syrphids alone,
although they do contribute aphid reduction (Alfiler and Calilung 1978, Van den Berg et
al. 1997).

In Asia, coccinellid predators (Harmonia spp.) and to a much lesser extent
syrphid predators are associated with A. glycines populations (Van den Berg et al. 1997).
Aphidophagous predators clearly depended on aphids as a food source and reduced A.
glycines populations in tropical areas of Southeast Asia, but the effects were not as

pronounced in temperate climates. At lower temperatures it was found that the

21

reproductive rate of A. glycines exceeded the predation rate of the coccinellid predators
(Van den Berg et al. 1997). This allowed A. glycines populations to develop rapidly in
temperate regions, particularly during the early portion of the season (Van den Berg et al.
1997). A similar result has been documented for Coccinnella spp. attacking pea aphids,
Acyrthosiphon pisum (Harris) in British Columbia (Frazer and Gilbert 1976).

Much consideration has been given to the importance that more generalist
predators may play in biological control (Hance 1987, Hilbeck et al. 1997, Landis and
Van der Werf 1997, Snyder and Wise 1999, Chang and Kareiva 1999, Symondson et al.
2002). For example, it has been shown that ground beetles (Carabidae) species are
capable of reducing populations of Aphis fabae Scopoli, a pest of sugar beet (Hance
1987). It has also been demonstrated that many species of carabid beetles in sugar beet
fields in the Netherlands, along with spiders and a dominant cantharid generalist predator,
Cantharis lateralis (Coleoptera: Cantharidae) aided in A. fabae aphid control early in the
season (Landis and Van der Werf 1997). Further, it has been shown that a complex of
ground-dwelling predators, such as carabids, staphylinids, and spider, all contributed to
the reduction of the bird cherry-oat aphid, Rhopalosiphum padi (L.), populations (Ostman
et al. 2001). While generalist predators are not as effective per capita as specialized
predators, they can often compensate by being present earlier in the season (Chang and
Kareiva 1999), when pest densities are low and specialist predators scarce (Takagi 1999).
It is now known that A. glycines establishment in Michigan occurs in rrrid-June, prior to
the arrival of specialized natural enemies. Thus, it is the more generalist predators that
will likely make an impact when A. glycines establishment occurs. However, the role of

predation to control A. glycines in the United States is not currently known.

22

The positive aspects of conservation biological control have been well
documented in the literature for both specialist and generalist predators (Bowie et al.
1999, Carmona and Landis 1999, Landis et al. 2000, Debach and Rosen 2001, Lee and
Landis 2002; Lee et al. 2001). Manipulating the environment through habitat
management to favor natural enemies can reduce direct mortality, provide supplementary
resources, and help to control secondary enemies by manipulating host plant attributes
(Debach and Rosen 2001). One potentially important role of habitat management is to
increase the abundance of generalist predators early in the season.

The objectives of these studies during 2001 was to: 1) determine the abundance
and species composition of potential A. glycines predators in plots bordering natural
enemy refuge habitats versus control plots; 2) to study the impacts of predators on A.
glycines establishment in these soybean plots. The objective in 2002 was to: 3) examine
the impact predation on A. glycines establishment in soybean fields without refuge

habitats.

Materials and Methods

Studies during 2001 were conducted at the Michigan State University
Entomology Farm, Ingham County, MI. The site consisted of 30 x 30 m plots arranged
in a randomized complete block design with four replications containing “refuge” and
control plots established in 1994 (Figure 2.1). Refuge plots contained a central 3.2 m
refuge strip consisting of a combination of orchard grass (Dactylis glomerata L.), white
clover (Trifolium repens L.), and several flowering perennial plants (Carmona and Landis

1999). The control plots had no refuge and were planted to soybean. One half of each

23

plot was randomly selected and used for either predation studies or predator sampling
during June of 2001. Predation of A. glycines was studied in the two rows approximately
8 m from the refuge or control strip (Figure 2.1). Sampling for predators occurred at 4
and 8 m from the refuge, and consisted of pitfall traps in rows and a predator observation
area at 8 m from the refuge or control strip (Figure 2.1). The outer 6 m of the field was
not used to minimize edge effects. The crop area was managed using reduced primary
tillage (chisel plow, disc) followed by secondary tillage (field cultivation). The herbicide
metolachlor (Dual 11) was applied at a rate of 2 l/ha. Potash was applied at a rate of 168
kg/ha to meet soil test requirements. Soybeans (Mycogen 5251RR) were planted on 5
May 2001 in 38 cm rows at a rate of 70,822 seeds/ha.

In 2002, studies were conducted in June at Michigan State University Crop and
Soil Sciences Research Farm, Ingham County, Michigan. The study field measured
approximately 36 m x 117 m and was split into five 12 m x 24 m blocks. The outer 6 m
of the field was not used to minimize edge effect. Each block was divided in half, with
each 12 m x 12 m area randomly designated for either predator sampling or predation
studies. Pitfall traps were placed in two rows 4 m apart, with a distance of 3 m between
pitfall traps. A l m x 30 cm predator observation area was randomly placed within each
12 m x 12 m sampling area throughout the experiment. The crop area was managed
using reduced tillage (fall chisel plow, secondary tillage with cultivator). Planting took
place on 5 May, 2002 in 38 cm rows. The cultivar used was Mycogen 5251RR at a
population density of 68,825 seeds/ha. Alpine liquid fertilizer (6-24-6 Fortified) was
applied on 5 May at a rate of 38 l/ha.

Insects.

24

In both 2001 and 2002, infested soybean plants containing Aphis glycines
Matsumura were obtained from a laboratory colony maintained by the USDA-APHIS-
PPQ facility located in Niles, Michigan, where they were reared on Asgrow #3303
cultivar soybeans at 26 °C and 60 percent RH with a photoperiod of 16:8 (L:D). Once at
Michigan State university, they were placed in grow chambers at 25°C, 70 % RH, and
16:8 (L:D) photoperiod until used.

Predator Abundance and Sampling.

In both 2001 and 2002, ground dwelling predator abundance and composition was
assessed using six 8.5 cm wide by 13 cm deep pitfall traps placed in two rows in each
half of the plots with rims at the substrate level. The six pitfall traps were placed at a
distance of 4 m and 8 m from the refuge or control strip, and at a distance of 3.7 m away
from the previous trap. Pitfall samples were collected each 48 h during trials. In
addition, there was one 1 m x 30 cm area in each sampling plot where ground and foliar
predator density and species composition were recorded during 5 min. visual
observations. Foliar predator observations were recorded when aphids were sampled at
15 and 24 h. The methodology was similar during 2002, except pitfall traps were placed
in two rows in each block half and the l m x 30 cm predator observation area was
randomly placed over a pitfall trap in each block.

Aphid Survival and Reproduction.

Early season A. glycines survival and reproduction was studied by confining A.
glycines adults on soybeans in clip cages allowing variable access to predators. Larger A.
glycines with a visible cauda were considered adults. Three treatments (Open, exclosure,

and leaky) of 1 cm (interior) circumference clip cages constructed of 1.8 cm (outside)

25

diameter Cresline® PVC pipe were used in three trials during 2001; 7-8 June (plants in
V2), 14-15 June (plants in V3), and 24-25 June (plants inV5), and three trials during
2002; 18-19 June (plants in V3), 24-25 June (plants in V5), and 2-3 July (plants in V6).
The aim was to do this study before, during, and immediately after natural A. glycines
infestation. Fine-mesh brass screen (96 threads per in.) on cages allowed air exchange
but kept aphids enclosed. Natural A. glycines were first observed on 12 June 2001 at an
initial density of 7.8, and on 14 June 2002 at a lower initial density of 1.2 aphids per m2.
In 2001, three adult female A. glycines were placed in each clip cage for trial one and
then four per cage during the second and third trials. For all treatments, aphids were
initially transferred into clip cages using a fine camel hair brush and then clipped on the
underside surface of soybean leaves. Four replicates of each cage treatment were placed
on soybean leaves in each refuge or control plot that were each replicated in four blocks.
Cages were placed on the uppermost trifoliate of selected plants at 8:00 AM. In 2002,
five adult A. glycines were placed in six of each cage treatment replicated in five blocks.
A. glycines were given a 6 h acclimation period to settle before differential cage
treatments were applied. At this point, the cages were completely removed from open
treatments and the leaky cages had a 3 mm corks removed from the side. This allowed A.
glycines to exit but prevented entry by predators larger than 3 mm. During 2001, cages
were placed 4 m away from control or refuge strips and were placed on the uppermost
leaves of plants large enough to support clip cages. In 2002, cages were randomly placed
on plants with leaves large enough to support the clip cages. In both years, at 8:00 AM

(15 h) and 4:00 PM (24 h) the following day, cages were momentarily opened and data

26

on the proportion of live adult A. glycines remaining and the number of nymphs produced
in each cage were recorded.

In 2001, an additional test was conducted as checks on cage performance. The
first consisted of leaky and exclosure cages clipped onto wooden pot stakes in the field.
Comparison of A. glycines numbers in these treatments allowed us to evaluate the
propensity for A. glycines to escape or emigrate when confined on a non-food source.
These internal controls were used as a check on the methods and were not statistically
analyzed.

In general A. glycines confined to soybean leaves in clip cages in the field settled
and began to feed within several hours. Aphis glycines in exclosure treatments were
totally confined and could not leave the cages, while those in leaky cages could leave if
they desired. Differences in numbers of A. glycines remaining in exclosure versus leaky
cages thus represents those aphids that emigrated from the cage. Aphis glycines in open
cages may be removed by predators or emigration, so a comparison of A. glycines
remaining in open versus leaky cages reveals the impact of predation.

Data Analysis.

Data from 2001 from predator observation areas were analyzed as the mean
number of predators per 5 min. per 1 m x 30 cm in refuge versus control plots. Data from
2001 pitfall traps were analyzed as the mean number of predators/trap/day in refuge
versus control plots. A type III F -test for overall treatment effect determined statistical
significance of treatment effect of pitfall and direct predator observation data. Data from
2002 predator observations were summarized as the mean number of predators per 3 min.

per 1 m x 30 cm in the five blocks. Data from 2002 pitfalls were summarized as the

27

mean number of predators/trap/day. Neither foliar or pitfall data was statistically
analyzed during 2002 because no treatment was applied. During 2001 and 2002, data on
the proportion of live adult aphids and the number of nymphs produced were analyzed by
logistic and Poisson regression, respectively, using the GLIMMIX Macro link of SAS
statistical program (SAS Institute 2000). When a significant treatment*hour interaction
existed, data was further sliced to reveal individual significant comparisons within the LS
MEANS. When analyzing nymph data, a significant effect of the number of A. glycines
at the beginning of trial was sometimes encountered. This indicates that the number of
adults entering the trial at the beginning differed between treatments. This can be
explained by the fact that not all Of the adult A. glycines settled on plants when cages
were removed. The number of adult A. glycines at the beginning of the trial was
therefore applied as a covariate to equalize treatments. A P value of 0.1 was accepted as
significant in this study for several reasons. First, trials were designed to be conducted in
24 h to minimize potential loss of data due to rainfall, or temperature extremes.

However, this leaves little time for predation to occur. Thus, the risk of rejecting the Ho
of predation effect is already quite substantial. Second, as the first test of its kind on A.
glycines in North America, there was no preliminary data with which to predict the power
of the tests used. Thus, less restrictive criteria were considered appropriate. Graphs in
this study were based on actual means and standard errors and not the estimated means

and confidence intervals from the Poisson Regression.

Results

Refuge Habitat Effects 2001.

28

Proximity to refuge habitats did not significantly (F = 2.00, df = l, 18, P: 0.20; F =
0.10, df= 1, 18, P: 0.90; F = 0.34, df= l, 18, P: 0.60) affect the number of predators
Observed in the 1 m x 30 cm plots during any of the three trials. Pitfall trap catches were
significantly (F = 2.90, df=: 1, 18, P: 0.04) higher in control versus refuge plots during
trial one; however, this effect did not persist into trials two or three (F = 0.08, df= l, 18,
P: 0.93; F: 0.40, df= 1, 18, P: 0.54). Similarly, there was no significant refuge effect
on predation of A. glycines adults or nymphs during any trial during 2001 (Table 2.5,
Table 2.6). Though there was a significant interaction between refuge*treatment*hour
during trial three for adults, slicing of the analysis showed that this interaction was
between an individual cage at 15 and 24 h and was not associated with refuge. Therefore,
refuge and control plot data was pooled for subsequent analysis.

Predator Density 2001-2002.

In 2001, predator density in predators Observations (1 m x 30 cm per 5 min.) was
greatest in trial one, lowest in two, and intermediate in trial three (Figure 2.2), with
ground dwelling predators predominant in all but trial three (Table 2.1). In trial one, the
carabid beetle, Elaphropus anceps (Le Conte) was the most abundant predator,
accounting for 70.7 percent of the total number of predators observed. During trial two,
E. anceps was still the most abundant predator, accounting for 55.6 percent of predators
observed, with foliar-foraging predators making their first appearance. Coccinella
septempunctata (L.) adults accounted for 27.8 percent of the predators and was the
second most abundant predator. In contrast, during trial three, foliar-foraging predators
were overall more abundant. Harmonia axyridis (Pallas) larvae, 39.5 percent, H. axyridis

adults, 18.6 percent, and Orius insidiosus (Say), 14 percent, made up a large portion of

29

the observed predators, but the carabid beetle E. anceps, 16.3 percent, were still
abundant

Predator density in 2002 was much lower than in 2001, peaking at 0.8 predators
per 1 m x 30 cm per 3 min. in trial two (Figure 2.2). During trial one, the two most
abundant predators were spiders and C. septempunctata, both of which accounted for 40
percent of the predators observed during this trial. During trial two, spiders were again
one of the more abundant predators, accounting for 87.5 percent of the predators
observed. In trial three, though, the diversity of foliar-foraging predators increased.
Hippodamia convergens Guerin, Nabis spp., and 0. insidiosus adults all accounted for 20
percent of the predators observed, while spiders once again were the most abundant and
made up 40 percent of the observed predators, though the abundance of predators during
this year was quite low in all three trials (Table 2.2).
Pitfall Captures 2001-2002.

Pitfall captures in 2001 were greatest in trial one and lowest in trial three (Figure
2.3). Almost all of the ground-dwelling predators captured were carabid beetles. In trial
one, E. anceps predominated in refuge and control plots and accounting for 51.1 percent
of the total catches. In trial two, however, Scarites quadriceps Chd., 35.2 percent, was
the most abundant. During trial three, Scarites subterraneus F., 33.3 percent, was the
most abundant (Table 2.3).

In 2002, total trap captures (Figure 2.3) were very similar to 2001, and the species
collected differed (Table 2.4). Notably, E. anceps was missing from 2002 collections and

in all three trials. Clavina impressefrons Le Conte was the most abundant predator

30

comprising 22 percent of the catches in trial one, 29.7 percent in trial two, and 50 percent
in trial three (Table 2.4).

While much remains to be learned about the consumption of aphids by ground
dwelling predators, E. anceps and C. impressefrons have been shown to be capable of
consuming A. glycines in laboratory feeding assays (Chapter 3). It is possible that these
predators foraged on plants at night, but this was not observed because of the beetles’
nocturnal activity. Thus, the effectiveness of carabid feeding on establishing aphid
colonies needs to be further investigated. However, in the case of foliar-foraging
predators such as C. septempunctata, H. axyridis, H. convergens, and Nabis spp., they
readily feed on A. glycines in feeding assays (Chapter 3) and were each observed to
consume A. glycines in the field (Fox Pers. Obs).

Predation on A. glycines.
Test of cage efficacy:

Confinement of A. glycines in leaky and exclosure clip cages on a wooden surface
(i.e. no food or water resources) showed that they readily disperse from leaky cages under
unfavorable conditions. In one trial, 100 percent of the A. glycines left the leaky cage by
15 h, while in a second, 89.3 percent left by 15 h and 98.2 percent by 24 h. The survival
in the exclosure cages at 24 h was very low (0-7 percent). This test indicates that A.
glycines are unable to escape the exclosure cages on a flat surface of wood versus a leaf
surface but can readily emigrate from leaky cages.

Clip cage trials:
Figures 2.4 and 2.7 reveal the overall trends in adult A. glycines survival under the

differing cage treatments. As expected, the number of A. glycines remaining in all cage

31

types was greater at 15 versus 24 h. At 15 h, the greatest percentage of A. glycines
remained in the exclosure treatments with a mean of 84.7 :1; 2.3 percent across all trials
(n=6). The mean number remaining in the leaky cages was 77.8 i 4.7 percent (n=6),
with 69.2 :1; 3.9 percent (n=6) remaining in the open treatment. At 24 h, the greatest
percentage of A. glycines remained in the enclosure treatments with a mean of 73.5 i 2.0
percent (n=6). The number remaining in the leaky cages was intermediate at 62.6 i 3.5
percent (n=6), with only 49.5 i 5.5 percent (n=6). In both years, more aphids survived to
24 h in the first trial with fewer remaining in the second and third trials.

2001 Adult Survival.

Analysis of predator exclosure treatments revealed a significant treatment effect
in trials one and two (Figure 2.4). There was a significant treatment*hour interaction in
trials one and three, due to differential numbers remaining in open versus exclusion
treatments at 15 or 24 h. There was also a highly significant hour effect, with fewer adult
A. glycines remaining at 24 h than at 15 h in all trials. In trial one, significantly fewer A.
glycines remained in open versus exclosure cages and open versus leaky cages at 15 h
(Table 2.5, Figure 2.4). In trial two, significantly fewer A. glycines remained in open
versus exclosure cages and leaky versus exclosure cages at 15 h. At 24 b there were
significantly fewer adult A. glycines in open versus exclosure cages, and leaky versus
exclosure cages in trial two. In trial three no significant effects occurred.

2001 Nymph Production.

In 2001, the greatest number of A. glycines nymphs per cage were generally

produced in the exclosure treatments (Table 2.6, Figure 2.5). In trial one there was no

significant treatment effect during any trial (Table 2.6, Figure 2.5). All three trials

32

showed a significant hour effect, with more nymphs present at 24 versus 15 h. In trial
two, there was a significant treatment*hour interaction, but further slicing of the data did
not reveal further significance based on pair wise comparisons.

2001 Total Aphid Numbers.

A comparison of the total A. glycines number (adults + nymphs) remaining in the
different treatments per cage is shown in Figure 2.6 and Table 2.7. There was a
significant effect of treatment in trials one and two, and there was also a significant
treatment*hour interaction in trial two. In all three trials there was a significant hour
effect, with fewer adults remaining and more nymphs being produced. In trial one, fewer
total A. glycines were found in open versus leaky treatments at 15 h fewer A. glycines in
Open versus both leaky and exclosure treatments at 24 h. In trial two there were
significantly fewer aphids in open versus leaky and exclosure cages at 24 h. In trial three,
there was no significant treatment effect.

2002 Adult Survival.

In 2002, there was evidence for predation on adult A. glycines (Table 2.8, Figure
2.7). There was a significant treatment effect in trials two and three. There was a highly
significant hour effect in all three trials. In trial one there was no significant treatment
effect (Table 8, Figure 2.7). During trial two, significantly fewer A. glycines were found
in open versus exclosure cages and leaky versus exclosure cages at 15 h. At 24 h,
significantly fewer A. glycines remained in open versus exclosure and open versus leaky
cages at 24 h. During trial three there were significantly fewer A. glycines in open and
leaky cages versus exclosure at 15 h. At 24 h, open cages contained fewer A. glycines

than leaky or exclosure cages.

33

2002 Nymph Production.

In 2002 the greatest number of nymphs were generally produced in leaky or
exclosure treatments, but differences were not consistent (Table 2.9, Figure 2.8). There
was no significant treatment effect in trial one or three, but there was a significant
treatment effect in trial two. In addition, there was a significant hour effect in trials one
and two (Table 2.9). In trial two there were significantly more nymphs in exclosure
versus Open or leaky cages at 15 h and 24h. There was no significant treatment effect in
trial three, though there was a significant treatment*hour interaction, but this interaction
did not reveal significant pair wise comparisons.

2002 Total Aphids.

In 2002, total A. glycines numbers per cage (adults + nymphs) was again higher in
leaky and exclusion cages versus open cages (Table 2.10, Fig. 2.9). In trials one and two,
there was a significant treatment effect. A significant treatment*hour interaction was
found in trials two and three. In trial one this interaction showed a significant treatment
effect at 24 h, but this was not the case in trial two, where the interaction revealed no
further significance. In all trials there was a significant hour interaction. In trial one,
there were significantly more A. glycines in leaky and versus exclosure treatments at 15
h, and leaky versus open treatments at 24 h. In trial two, there were significantly more A.
glycines in exclosure versus open, and exclosure versus leaky cages at 24 h. In trial

three, there was no significant treatment effect.

Discussion

34

Overall refuge plots did not alter the abundance or species composition of foliar-
foraging or ground-dwelling predators and impact predation. One possible reason for
finding no significant impact is that the plot size was small compared to the mobility of
the dominant predators. The importance of habitat manipulation cannot be discounted,
and results may have been different if the plot size was larger. This part of the study
should be repeated in a larger area.

Examining adult, nymph and total A. glycines remaining in 2001 revealed several
trends. First, the number remaining to 15 h was generally rather high. Although a trend
of reduced numbers remaining in the more exposed treatments (leaky and open) was
observed, it was seldom significant. More pronounced differences are seen at 24 h where
a consistent trend for reduced numbers of aphids remaining in open treatments was
observed. The strongest evidence of predation occurs when the numbers in open
treatments were significantly less than exclosure treatments and when there was a
significant difference between the open and leaky cages. When significantly more A.
glycines remained in leaky versus open cages, there was evidence that A. glycines were
also being lost to predation in addition to those that may have emigrated.

The case for predation is weakened but not excluded in cases where there was no
significant difference between open and leaky cages. During 2001, there were
significantly fewer A. glycines in open versus exclosure treatments at 15 h but not 24 h.
While trends for lower numbers of remaining nymphs did exist, there was no significant
treatment effect during any trial. Evidence based on the total number of A. glycines
remaining suggests predation was likely responsible this reduction during trial one of

2001, where there were significantly fewer A. glycines present in open versus leaky and

35

exclusion cages at 24 h. There is also evidence for predation during trial two because
there were significantly fewer aphids present in open versus leaky cages and open versus
exclusion cages at 24 h.

Data from 2002 yields overall stronger evidence for predation, with significant
reductions in the number of adult A. glycines remaining in two out of three trials at 24 h.
In trial two there was evidence for predation because there were significantly fewer A.
glycines remaining in Open versus leaky cages and open versus exclusion cages at 24 h.
A similar trend existed in trial three, where significantly fewer A. glycines remained in
open versus leaky and exclosure cages at 24 h. There did not seem to be significant
predation on nymphs during 2002. The reason for this is not known. Perhaps due to their
small size, nymphs may be more difficult for predators to locate. In the case of the total
number of A. glycines, there was no statistical evidence for predation.

In summary, there was strong evidence for predation on adult A. glycines in one
out of six trials at 15 h and two out of six trials at 24 h. There was no evidence for
predation of nymphs in any trial. Furthermore, there was strong evidence for predation
based on the total number of live A. glycines in two out of six trials at 24 h. Thus, as a
result of these trials, the Ho that predators do not impact A. glycines establishment is
rejected. In contrast, these studies establish that predation can be a significant factor
influencing establishment of A. glycines populations in soybean.

Our studies also shed light on which predators are responsible for reductions in A.
glycines establishment. Significant predation occurring at the 15 h mark may in part be
attributed to the activity of nocturnal predators. While many carabid beetles were present

in the plots and our no-choice tests show that most of the carabid species could consume

36

A. glycines (Chapter 3), results show this predation to be limited. This is in contrast to
Hance (1987), who attributed reductions in aphid populations to predatory carabids and
Ostman et al. (2001), who also found carabid beetles and other ground-dwelling predators
to successfully reduce low density aphid populations. Other investigators have noted an
interaction between foliar predators that disturb aphids and cause them to drop and
predation by ground-dwelling predators (Losey and Denno 1998). A preliminary study
indicated that A. glycines do not drop in response to disturbance. Thus, this was an
important factor in our result. Since A. glycines does not readily drop from plants,
ground-dwelling predators would have to climb plants to encounter most A. glycines.
However, this study is in agreement with the findings of Chang and Kareiva (1999), and
Takagi (1999), who suggest that generalist predators may be most effective by reducing
initial pest populations before they reach outbreak levels. Even a low level of nocturnal
feeding may thus reduce initial numbers so that diurnal predators foraging on soybean
leaves would be better able to reduce populations.

During the later spring trials, more specialized (aphidophagous) predators became
predominant and were responsible for aphid reduction. During the second and third trials
in both years aphids were reduced the most at 24 h. During these studies predators were
observed consuming A. glycines on eight separate occasions feeding on aphids in the
open treatment. This included observations of predation by early instar H. axyridis
larvae, and 0. insidiosus nymphs (Fox unpub. data). Considering the very low density Of
A. glycines in the field at this time, these observations of early season predation on A.

glycines should not be underestimated and are consistent with the known ability of

37

aphidophagous predators to search for and find prey at low densities (Grasswitz and
Burts 1995, Stary 1995, Van den Berg et al. 1997, Obrycki and Kring 1998).

Overall, this research points to the importance of early season predators in
reducing the establishment of A. glycines in soybean. A complex of predators including
both generalist and more specialized natural enemies contributed to these effects.
Establishment success was reduced to a greater degree later in the spring. This may
indicate a potentially important interaction between crop planting date, A. glycines arrival
and conservation of predators in the field. Further research should concentrate on means
to improve the reliability of predators in reducing early season A. glycines survival and

establishment.

38

 

 

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48

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sampling area

Figure 2.1. Layout of the 2001 field location on the Michigan State University
Entomology Farm, East Lansing, Michigan. The fields were separated into four blocks,
each containing a refuge and control plot. Enlarged plots illustrate where pitfall traps and

foliar sampling areas were located, and where clip cages were placed.

49

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

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Trial One Trial Two Trial Three

Figure 2.2. Mean number (i SEM) of predators observed in l m x 30 cm areas during;
A. 5- minutes in trial one (7-8 June 2001), trial two (14-15 June 2001), and trial three
(24-25 June 2001) and; B. 3-minutes during trial one (18-19 June 2002), trial two (24-25

June 2002), and trial three (2-3 July 2002), East Lansing, Michigan.

50

 

 

 

 

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Trial One Trial Two Trial Three

Figure 2.3. Mean number (i SEM) of predators per trap per day collected in 32 pitfall
traps; A. located in refuge and control plot during trial one (7-8 June 2001), trial two (14-
15 June 2001), and trial three (24-25 June 2001); B. in 30 pitfall traps in five blocks
during trial one (18-19 June 2002), trial two (24-25 June 2002), and trial three (2-3 July

2002), East Lansing, Michigan.

51

Figure 2.4. Percentage of live adult A. glycines remaining at 15 and 24 h for the open,
leaky and exclosure treatments in refuge and control plots during; A. trial one (7-8 June
2001); B. trial two (14-15 June 2001); and C. trial three (24-25 June 2001), East Lansing,
Michigan. Different letters above bars within. an hour denotes significant (P _<_ 0.1)

differences among open, leaky, and exclosure treatments (Poisson regression test).

52

 

 

 

 

 

 

 

 

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l
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53

Figure 2.5. Number of live A. glycines nymphs at 15 and 24 h in three cage treatments
during; A. trial one (7-8 June 2001); B. trial two (14-15 June 2001); and C. trial three

(24-25 June 2001), East Lansing, Michigan. Different letters above bars within an hour
denote significant (P g 0.1) differences in the number of nymphs present in open, leaky,

and exclosure treatments (Poisson regression (log-linear model) test).

54

 

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55

Figure 2.6. Total number of live adult and nymph A. glycines at 15 and 24 h in h in three
cage treatments during 1) trial one (7-8 June 2001), 2) trial two (14—15 June 2001) and 3)
trial three (24-25 June 2001), East Lansing, Michigan. Different letters above bars within
an hour denote significant (P g 0.1) differences. among open, leaky, and exclosure

treatments (Poisson regression (log-linear model) test).

56

1 I Adults

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57

Figure 2.7. Percentage of live adult A. glycines remaining at 15 and 24 h for the open,
leaky and exclosure treatments in during; A. trial one (18-19 June 2002); B. trial two (24-
25 June 2002); and C. trial three (2-3 July 2002), East Lansing, Michigan. Different
letters above bars within an hour denote significant differences among open, leaky, and

exclosure treatments (Poisson regression test).

58

 

 

 

 

 

 

 

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ll 11

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Open

59

Figure 2.8. Number of live nymph A. glycines at 15 and 24 h in three cage treatments
during; A. trial one (1819 June 2002); B. trial two (24-25 June 2002); and C. trial three
(2-3 July 2002), East Lansing, Michigan. Different letters above bars within a given hour
denote significant (P g 0.1) differences in the number of nymphs present in open, leaky,

and exclosure treatments (Poisson regression (log-linear model) test).

60

menu
31 the:
;\ an hour

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Number of A. glycines nymphs at 15 and 24 h

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

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61

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Figure 2.9. Total number of live adult and nymph A. glycines at 15 and 24 h in three cage
treatments during; A. trial one (1819 June 2002); B. trial two (24-25 June 2002) and C. trial
three (2-3 July 2002), East Lansing, Michigan. Different letters above bars within a given hour
denote significant (P g 0.1) differences amongiopen, leaky, and exclosure treatments (Poisson

regression (log-linear model) test).

62

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63

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exotic immigrant aphid in central Europe. Entomophaga. 40(1): 29-34.

Takagi, M. 1999. Perspective of practical biological control and population theories.
Researches on population ecology. 41: 121-126.

University of Minnesota Extension Service Web Site:
http://www.sovbeans.umn.edu/crop prod/insects/aphid/aphid.htm

Van Den Berg, H., D. Ankasah, A. Muhammad, R. Rusli, H.A. Widayanto, H.B. Wirasto,
and I. Yully. 1997. Evaluating the role of predation in population fluctuations of the
soybean aphid, Aphis glycines in farmers’ fields in Indonesia. Journal of Applied
Ecology. 34, 971

Wang, S. Y., X. Z. Boa, Y. J. Sun, R. L. Chen, and B. P. Zhai. 1996. Study on the
effects of the population dynamics of soybean aphid (Aphis glycines) on both growth and
yield of soyabean. Soybean Science. 15(3): 243-247.

66

CHAPTER 3
Evaluating the impact of indigenous and exotic predators of the soybean aphid, A.

glycines, in laboratory no-choice feeding assays

Introduction

The soybean aphid, Aphis glycines Matsumura, is an exotic pest from Asia that
was discovered in the United States in 2000. In Asia A. glycines feeding can cause up to
a 20 cm reduction in growth and a 27.8 percent reduction in seed yields (Wang et al.
1996). In 2000, it was found that up to a 13 percent yield reduction occurred in
replicated field plots in Wisconsin (University of Minnesota Extension Service Web
Site). In 2001, this aphid caused a 40 percent yield loss in (Difonzo, Pers. Comm). This
pest may also indirectly harm soybeans by vectoring persistent viruses, such as soybean
dwarf virus and non-persistent viruses, such as soybean stunt virus, soybean mosaic
virus, bean yellow mosaic virus (Van den Berg et al. 1997). Epidemics of soybean
mosaic potyvirus in summer-sown soybean fields in Jiangsu, China were found to be
closely related to the timing of A. glycines immigration (Li and Pu 1991). In addition,
aphids also cause indirect damage by excreting honeydew onto foliage, which promotes
the growth of sooty molds that reduce the photosynthetic capacity of the leaves (Lenné
and Trutmann 1994, Hirano et al. 1996).

Foliar-foraging predators can contribute to the control of a wide variety of aphid
species (Grasswitz and Burts 1995, Stary 1995, Obrycki and Kring 1998). For example,

it was found that a complex of natural enemies, including Chrysopa nigricomis

67

Burmeister, Orius spp., Coccinella transversoguttata Faldermann, Hippodamia
convergens Guerin, and various species of Syrphidae and Chamaemyiidae all contributed
to the reduction of Aphis pomi De Geer in a field study using apple trees (Grasswitz and
Burts 1995). Similarly, Stary (1995) found that Coccinella septempunctata L., Adalia
bipunctata (L.), and Episyrphus balteatus (De Geer) were common predators that aided
in control of the spiraea aphid, Aphis spiraephaga Muller in Czechoslovakia.

There is currently no published data on the ability of folia-foraging predators to
consume A. glycines in United States. In Asia it is known that coccinellid (Harmonia
spp.) predators play an important role in suppressing A. glycines populations in soybean
fields in the tropical Southeast at higher temperatures (Van den Berg et al. 1997).
Another study suggested that Nabis spp., Harmonia axyridis (Pallas), Coccinella
septempunctata L., and Chrysopa spp. aid in A. glycines control during the mid to late
growing season in China (Han 1997). At this time it is not known if these species will
consume A. glycines in the Michigan, or which other common predators in soybean fields
will aid in its control.

Ground-dwelling predators may also play an important role in aphid biological
control (Hance 1987, Landis and Van der Werf 1997, Snyder and Wise 1999, Chang and
Kareiva 1999, Symondson et al. 2002). For example, it has been shown that ground
beetles (Carabidae) species can of reduce populations of Aphis fabae Scopoli, a pest of
sugar beet (Hance 1987). It was also demonstrated that many species of carabid beetles
in sugar beet fields in the Netherlands, along with spiders and a dominant cantharid

generalist predator, Cantharis lateralis aided in aphid control early in the season (Landis

68

 

and Van der Werf 1997). No data exists to assess the ability of ground-dwelling
predators to consume A. glycines in North America.

Petri dish or small cage laboratory studies provided an avenue for quickly
assessing predation on numerous pest species by a wide variety of potential predators
(Bilde and Toft 1997, Sebolt 2000, Schmaedick and Shelton 2000). Landis and Van der
Werf (1997) used Petri dish assays to determine potential predators of A. fabae, and their
possible preference for nymph or adult aphids. Therefore, the objective of this study was
to examine the capability of common predators in Michigan soybean fields to consume A.
glycines adults in laboratory no-choice feeding assays using techniques similar to Landis
and Van der Werf (1997). Using a no—choice test, it was determined which species can
feed on A. glycines adults and nymphs, and if these predators have a preference for aduls
or nymph A. glycines. Attention was focused on these predators as potential predators of

A. glycines in the field.

Materials and Methods
Insects.

A colony of A. glycines was obtained from the USDA-APHIS—PPQ facility, Niles,
Michigan and reared on greenhouse grown soybeans (Mycogen 5251RR) in growth
chambers at 250 C, 70 % RH, and 16:8 (L:D) photoperiod. Plants were changed on a
weekly basis, and adults were transferred from old to new plants with a fine camel hair
brush.

Predator Collection.
Foliar-foraging and ground-dwelling predators used for feeding assays were

collected from soybean fields located at the Michigan State University Entomology

69

Research Farm, Ingham County, Michigan. From 7 June to 9 August 2001 foliar-
foraging predators were collected with sweep nets from soybean foliage. Ground-
dwelling predators were collected in dry pitfall traps placed in soybean fields. Pitfall
traps were opened for 62 h each week, and checked every 24 h.

Feeding Assay.

Predators were returned to the laboratory, held at approximately 24¢ 20 C and
placed into individual Petri dishes (90 mm diam. with a 4 mm screened hole in the lid for
ventilation) lined with moistened filter paper for a 24 h acclimation/starvation period. A
2 cm wet cotton wick in each dish moistened with distilled water provided moisture.
Predator availability varied between species and over time; the number tested varied from
a minimum of five to a maximum of 60 individuals. All feeding assays were conducted
from 8 June to 10 August 2001. After 24 h of acclimatization for predators, ten adult
aphids were placed onto a soybean leaf and then transferred to each experimental dish
containing a predator. Larger aphids with a visible cauda were considered adults in thsi
study. During each trial, five to ten control dishes without predators were also
established to evaluate survival in the absence of predation. Aphis glycines and predators
were left in experimental and control dishes for 24 h after which predators were removed
and the number of remaining (out of ten) A. glycines were counted. At this time nymph
aphids that were produced were also counted.

Analysis.
At the end of the season, adult and nymph aphid numbers in experimental and control
dishes were pooled and compared for each predator species tested (SAS Institute 2000).

Since only several of a given species were often collected on a given date, and survival of

70

 

aphids in control dishes did not differ significantly by date, individual predator dishes and
their controls were pooled throughout the season, which yielded a stronger statistical
analysis. A pooled t-test with equal variance was used on the number of aphids
remaining in dishes to evaluate feeding on A. glycines for all predator species.
Experimental and control dishes were not paired for analysis, since control dishes were
compared to all experimental dishes. We calculated percent mortality (= predation rate)
for both adults and nymphs that were produced during the trial. Nymphal mortality was
defined as an expected reduction in both control and experimental dishes. Expected
reduction was calculated by averaging the number of nymphs produced in experimental
dishes divided by the average beginning and final adult aphid number in experimental
dishes. When the same procedure was done in control dishes, nymphal mortality could
be determined by dividing expected reduction in predator dishes by that in control dishes.
After this, nymphal mortality was contrasted to adult mortality, allowing the
measurement of preference. A mortality ratio greater than one indicates preference for

nymphs over adults.

Results

All foliar predators consumed significant (P g 0.05) numbers of A. glycines adults
when compared to survival in the control (Table 3.1). The mean numbers of A. glycines
surviving were consistently low for almost all coccinellid species, including Coccinella
septempunctata (L.), Harmonia axyridis (Pallas), and Hippodamia convergens Guerin,
but C. septempunctata larvae consumed the most, with an average of 1.1 i 0.3 A. glycines

surviving at the end of the 24 h period. Other foliar predators that consumed 70 percent

71

or more of the A. glycines presented, included Chrysopa spp. larvae, and Nabis spp.
adults and nymphs. Several foliar-foraging predators consumed less than 50 percent of
the A. glycines presented, including Coleomegilla maculata De Geer adults, which
allowed the most A. glycines to survive (6.4 i 0.7) at 24 h. Chrysopa spp. adults, Orius
insidiosus adults and nymphs each consumed fewer A. glycines.

Foliar—foraging predators also consumed a significant (P g 0.05) number of A.
glycines nymphs in all but one case when compared to survival in the control (Table 3.1).
The only exception was Orius insidiosus adults, which left 6.6 i 0.9 nymph aphids in the
dish, and was not significantly different from the control. While Orius insidiosus
nymphs and Chrysopa spp. adults also left over five nymph A. glycines in the dish,
though their feeding was significant in both cases. All other predators left no more than
three remaining A. glycines in the dish at 24 hours.

Four of the species tested had a preference for nymph over adult aphids.
Coccinella septempunctata larvae, and H. axyridis adults and nymphs had a slight
preference, while C. maculata had a strong preference, for nymphs. The remaining
predators had mortality ratios less than one and preferred adults over nymphs, though
several species (C. septempunctata adults, H. convergens, and Nabis spp.) were
borderline and therefore it can be assumed that their preference was minimal.

Most ground-dwelling predators also always significantly reduced adult aphid
survival in contrast to the control (Table 3.2). Poecilus chalcites, Poecilus lucumblandus,
and Pterostichus melanarius were significant predators (P g 0.05). Forficula auricularia

each consumed more than 50 percent of the A. glycines presented (P g 0.05). Two

72

predators, Clavina impressefrons and Philonthus thoracicus, did not show significant
feeding on adult A. glycines.

Ground-dwelling predator feeding on nymphal A. glycines was also significant in
most cases. Both P. chalcites and P. lucublandus left the fewest remaining nymphs, 1.5
i 0.5 and 2.2 i 0.5, respectively. Clavina impressefrons, Harpalus herbivagus, and
Philonthus throracicus did not show significant feeding on nymph A. glycines.

The mortality ratio for ground-dwelling predators differed from that of foliar-
foraging predators. All predators with the exception of one, F. auricularia, had a
preference for nymphs over adults. This predator had a borderline mortality ratio of 0.9.
The mortality ratio was greatest, indicating stronger preference, for smaller predators,
including Elaphropus anceps, Harpalus herbigus, and Philonthus thoracicus, despite the

fact that feeding was not significant for the latter two species.

Discussion

While all foliar species tested showed significant feeding on adult A. glycines,
some species (C. septempunctata, H. axyridis, H. convergens, Chrysopa spp. larvae, and
Nabis spp.) appeared to feed more readily on A. glycines than other species (Chrysopa
spp. adults, C. maculata, and 0. insidiosus) tested. In many cases C. septempunctata and
H. axyridis began immediately feeding on A. glycines and consumed most of the A.
glycines in the dish within the first few hours of the study. In this case the apparent
preference for nymphs is artifact of the equation used to calculate nymphal mortality
slightly overestimates the number of nymphs available for predation. The predators

tested have a differing seasonal occurrence, with Orius insidiosus, Harmonia axyridis,

73

and Coccinella septempunctata appearing in early June, when aphid establishment occurs
(Table 3.3, Chapter 4). Although 0. insidiosus adults and nymphs left more adult and
nymph A. glycines than other predators tested, their abundance in the field may make up
for their small size and relatively low feeding capacity. These predators appearing
around the time of A. glycines establishment likely will help to control it before colonies
become large. Those appearing later may help to reduce the rise of A. glycines colonies
that survive initial reduction from other predators.

As for ground-dwelling predators, most of which are nocturnal, immediate
feeding was rarely observed. Most predators hid under the soybean leaf in the dish when
they were introduced. However, F. auricularia began immediately consuming A.
glycines when it was introduced into dishes. During the course of the trial most predators
consumed significant numbers of adult and nymph A. glycines. The reason for a
preference of nymphs in most cases cannot easily be explained. One would think that
voracious predators such as larger carabid beetles would prefer larger prey. The fact that
Elaphropus anceps had a preference for nymph A. glycines is not surprising, since this
predator is approximately the size of adult A. glycines. Many of these ground-dwelling
predators are present from June to August, and may encounter A. glycines during their
nocturnal foraging (Table 3.4), so their importance as aphid predators should not be
discounted. However, their importance as A. glycines predators needs to be assessed
further. Further studies are needed to determine if ground-dwelling predators actively
climb plants to feed on aphids, or consume aphids that may fall from plants when

disturbed.

74

Any successful biological control program for A. glycines in part depends on
existing predators present in soybean fields to both prevent aphid establishment and
reduce populations of established colonies. As such, the results of this study contribute to
implementation of a successful biological control program for the soybean aphid. These
studies indicate that both foliar and ground-dwelling predators readily consume both
adult and nymph A. glycines in no—choice tests. The role of these predators in future

predation needs to be further assessed.

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Literature Cited

Bilde, T., and S. Toft. 1997. Limited predation capacity by generalist arthropod
predators on the cereal aphid, Rhopalosiphum padi. Entomological Research in Organic
Agriculture. 15: 143-150.

Chang, GO, and P. Kareiva. 1999. The case for indigenous generalists in biological
control, pp. 103-115. In B. A. Hawkins and H. V. Cornell, ed. Theoretical approaches to
biological control. Cambridge University Press, UK.

Grasswitz, T.R., and E. Burts. 1995. Effect of native natural enemies and augmentative
releases of Chrysoperla rufilabris Burmeister and Aphidoletes aphidimyza (Rondani) on
the population dynamics of the green apple aphid, Aphid pomi De Geer. International
Journal of Pest Management. 41(3): 176-183.

Han, X. 1997. Population dynamics of soybean aphid Aphis glycines and its natural
enemies in fields. Hubei Agricultural Sciences. 2: 22-24.

Hance, T. 1987. Predation impact of carabids at different population densities on Aphis
fabae development in sugar beet. Pedobiologia. 30: 251-262.

Hirano, K., K. Honda, and S. Miyai. 1996. Effects of temperature on deve10pment,
longevity and reproduction of the soybean aphid, Aphis glycines (Homoptera:
Aphididae). Applied Entomology and Zoology. 31(1): 178-180.

Landis, D.A., and W. Van der Werf. 1997. Early-season aphid predation impacts
establishment and spread of sugar beet yellows virus in the Netherlands. Entomophaga.
42: 499-516.

Lenné, J.M., and P. Trutmann. 1994. Diseases of tropical pasture plants. CAB
International, Wallingford, UK. P. 69.

Li, W.M., and Z.Q. Pu. 1991. Population dynamics of aphids and epidemics of soybean
mosaic virus in summer sown soybean fields. Acta Phytophylactica Sinica. 18(3): 123-
126.

Obrycki, J .J ., and T.J. Kring. 1998. Predaceous coccinellidae in biological control.
Annual Review of Entomolgy. 43: 295-321.

80

 

SAS Institute. 2000. SAS/STAT user’s guide, release 8.1 led. SAS Institute, Cary, NC.

Sebolt, D. C. 2000. Predator effects on Galerucella calmariensis L. (Coleoptera:
Chrysomelidae), classical biological control agent of Lythrum salicaria L. (Myrtales:
Lythraceae). MS. Thesis, Michigan State University.

Snyder, W.E., and DH. Wise. 1999. Predation interference and the establishment of
generalist predator populations for biocontrol. Biological Control. 15: 283-292.

Syndmondson, W.O.C., K.D. Sunderland, and M.H. Greenstone. 2002. Can generalist
predators be effective biocontrol agents? Annual Review of Entomology. 47: 561-594.

Schmaedick, M. A., and A. M. Shelton. 2000. Arthropod predators in cabbage
(Cruciferae) and their potential as naturally occurring biological control agents for Pieris
rapae (Lepidopera: Pieridae). The Canadian Entomologist. 132: 655-675.

Stary, P. 1995. Natural enemy spectrum of Aphis spiraephaga (Hom: Aphididae), an
exotic immigrant aphid in central Europe. Entomophaga. 40(1): 29-34.

University of Minnesota Extension Service Web Site:
http://wwwsoybeansumn.edu/crop prod/insects/@hid/aphidhtm

Van den Berg, H., D. Ankasah, A. Muhammad, R. Rusli, H.A. Widayanto, H.B. Wirasto,
and I. Yully. 1997. Evaluating the role of predation in population fluctuations of the
soybean aphid Aphis glycines in farmers’ fields in Indonesia. Journal of Applied
Ecology. 34: 971-984.

Wang, S.Y., X.Z. Boa, Y.J. Sun, R.L. Chen, and BF. Zhai. 1996. Study on the effects of
the population dynamics of soybean aphid (Aphis glycines) on both growth and yield of
soyabean. Soybean Science. 15(3): 243-247.

81

CHAPTER 4

Predator effects on soybean aphid, Aphis glycines Matsumura, population growth

Introduction

The soybean aphid, Aphis glycines Matsumura, is an exotic pest from Asia that
was discovered in the United States in 2000. In Asia A. glycines feeding on soybean can
cause up to a 20 cm reduction in growth and a 27.8 percent reduction in seed yield (Wang
et a1. 1996). In 2000, A. glycines caused up to a 13 percent yield reduction occurred in
replicated field plots in Wisconsin during the year 2000 (University of Minnesota
Extension Service Web Site). In 2001, it was found that A. glycines caused up to a 40
percent yield loss in Michigan (Difonzo, Pers. Comm). Aphis glycines pest can also
indirectly harm soybeans by vectoring persistent viruses, including soybean dwarf virus
and non-persistent viruses, such as soybean stunt virus, soybean mosaic virus, and bean
yellow mosaic virus (Van den Berg et al. 1997). Epidemics of soybean mosaic potyvirus
in summer-sown soybean fields in Jiangsu, China were found to be closely associated to
the timing of A. glycines immigration (Li and Pu 1991). In addition, aphids also cause
indirect damage by excreting honeydew onto foliage, which promotes the growth of
sooty molds that reduce the photosynthetic capacity of the leaves (Lenné and Trutmann
1994, Hirano et al. 1996).

Foliar-foraging predators contribute to the reduction of a wide variety of aphid
species (Grasswitz and Burts 1995, Stary 1995, Van den Berg et al. 1997, Obrycki and

Kring 1998). For example, it was found that a complex of natural enemies, including

82

Chrysopa nigricornis Burmeister, Orius spp., Coccinella transversoguttata Faldermann,
Hippodamia convergens Guerin, and several species of Syrphidae and Chamaemyiidae
all contributed to the reduction of Aphis pomi De Geer in a field study using apple trees
(Grasswitz and Burts 1995). Similarly, Stary (1995) found that Coccinella
septempunctata L., Adalia bipunctata (L.), and Episyrphus balteatus (De Geer) were
common predators that all consumed and thus aided in control of the spiraea aphid, Aphis
spiraephaga Miiller in Czechoslovakia. Chen and Hopper (1997) found in Europe that
Russian wheat aphid, Diuaphis noxia (Mordvilko), populations were reduced at critical
times by several species of coccinellid and syrphid predators.

In Asia, coccinellid predators (Harmonia spp.) play an important role in
suppressing A. glycines populations in soybean fields (Van den Berg et al. 1997). Other
aphidophagous predators, such as Nabis spp., Harmonia axyridis (Pallas), Coccinella
septempunctata L., and Chrysopa spp. aided in its control during the mid to late season in
China (Han 1997). Schneider (1971) reported the predaceous syrphid larva Ischioa’on
escutellaris (F .) was another aphidophagous predator that fed on a wide variety of aphids,
including A. glycines in the Philippines. However, low syrphid abundance in comparison
to the number of aphids has not resulted in suppression of aphid populations by syrphids
alone, although they do contribute aphid reduction (Alfiler and Calilung 1978, Van den
Berg et al. 1997).

Folia—foraging predators clearly depend on aphids as a food source and reduce
aphid populations in tropical areas, but the effects were not as pronounced in temperate
climates. At lower temperatures it was found that the reproductive rate of A. glycines

exceeded the predation rate of the coccinellid predators (Van den Berg et a1. 1997). This

83

allowed A. glycines populations to rapidly develop in temperate regions, particularly
during the early portion of the growing season (Van den Berg et al. 1997). A similar
result has been documented for Coccinnella spp. attacking pea aphids, Acyrthosiphon
pisum (Harris), in British Columbia (Frazer and Gilbert 1976).

In the United States, generalist predators may be the most common natural
enemies of A. glycines. Much consideration has been given to the importance that
generalist predators may play in biological control (Hance 1987, Hilbeck et al. 1997,
Landis and Van der Werf 1997, Snyder and Wise 1999, Chang and Kareiva 1999,
Symondson et al. 2002). For example, it has been shown that ground beetles (Carabidae)
species are capable of reducing populations of Aphisfabae Scopoli, a pest of sugar beet
(Hance 1987). It has also been demonstrated that many species of carabid beetles in
sugar beet fields in the Netherlands, along with spiders and a cantharid, Cantharis
lateralis (Coleoptera: Cantharidae) aided in A. fabae aphid control early in the season
(Landis and Van der Werf 1997). Further, it has been shown that a complex of ground-
dwelling predators, such as carabids, staphylinids, and spiders, all contributed to the
reduction of bird cherry-oat aphid, Rhopalosiphum padi (L.), populations (Ostman et al.
2001). While generalist predators are not as effective per capita as specialized predators,
they can often compensate by being present earlier in the season (Chang and Kareiva
1999), when pest densities are low and specialist predators scarce (Takagi 1999).
However, the role of predation in control of A. glycines in the United States is not
currently known.

The objectives of these studies were to: 1) determine the abundance and species

COmposition of potential A. glycines predators in Michigan soybean fields following

84

aphid establishment (2001) and prior to A. glycines establishment (2002), and 2) study

the impacts of predators on A. glycines with and without predator exclusion.

Materials and Methods
Field Site.

Experiments took place at the Michigan State University Entomology Farm,
Ingham County, Michigan. During 2001, a 134 m x 99 m field was planted to soybean
variety Mycogen (5251RR) in 38 cm rows. All plots were located at least 9 m from any
field borders to minimize edge effects. The crop area was managed using reduced
primary tillage (chisel plow, disc) followed by secondary tillage (field cultivation) after
metolachlor (Dual 11) was applied at a rate of 2 l/ha to control weeds. Potash was applied
at a rate of 168 kg/ha to meet soil test requirements. Soybeans were planted on 5 May
2001 at a rate of 70,823 seeds/ha.

During 2002, a 99 m x 94 m field was planted to soybean Pioneer (93882) in 38
cm rows. Experiments were conducted in this larger field with no plot closer than 9 m
from any edge to minimize edge effect. The field was planted on 20 May 2002 at a rate
of 70,900 seeds/ ha. The crop area was again managed using reduced primary tillage
(chisel plow, disc) followed by secondary tillage (field cultivation). A tank mix of the
herbicides, of lactofen (Cobra) (1 l/ha), bentazon (Basagran) (2 l/ha), sethoxydim + dash
(Poast Plus) (2 l/ha), and crop oil concentrate (21/ha) was applied on 5 June 2002.

2001 Predator Exclusion Trial.
In 2001, A. glycines population growth was contrasted in treatments consisting of

cages designed to exclude all predators versus open (sham) cages that allowed predator

85

access (Figure 4.1). The experiment was laid out as a completely randomized design
with five replications and one cage of each cage type placed per 9 m x 9 m area. Cage
frames were constructed of 1.3 cm outside diameter Cresline PVC pipe. Frames for
exclusion cages were 1 m2 (top view) with legs 0.90 m long, with 20 cm to be placed in
the soil and 0.70 m to extend above the soil line (Figure 4.1). The top of the frame was
covered with l m2 white no-see-um fine mesh netting that draped 27 em down the side of
cages. The bottom of the frame was surrounded by a thin 3 mil plastic sheet that
extended 10 cm below the ground and upward 27 cm to meet the bottom of the screen.
Where they met, the screen and the plastic were joined with a 2 cm strip of Velcro that
allowed cages to be opened for sampling. Frames for open cages were also 1 m2 (top
view) but legs were 1 m long, with 0.10 m below the soil surface. This allowed for a 18
cm gap between the plastic and the soil line to allowed predators to enter and a 10 cm gap
between the plastic and the screen for foliar-foraging predators to enter. Both exclusion
and open cages contained the same amount of screen and plastic materials above the soil
level to control for potential cage effects. The exclusion cage was designed to exclude all
predators and was completely sealed. Two 8.5 cm by 13 cm pitfall traps with rims at the
soil level were placed in exclusion cages to remove ground-dwelling predators and two
standard 14 cm x 23 cm yellow sticky traps were placed in each cage to remove foliar-
foraging predators. Twenty sticky traps and twenty pitfall traps (one in each treatment
plot) were placed in the field to allow comparisons to be made between predator
composition and abundance in exclusion treatments versus those in the entire plot area.

Pitfall and sticky traps were changed weekly.

86

Sampling was initiated on 26, June 2001, after natural A. glycines infestation took
place, and was completed on 31 July 2001. Sampling was continued in the open cage
treatment until 4 September 2001. At weekly intervals, the temperature inside and
outside of cages were determined using a mercury thermometer held inside cages for 1
minute and then outside cages for 1 minute. A hygrometer was similarly used to collect
relative humidity data. Foliar observations in the form of a 3-minute non-intrusive visual
examination of soybeans in each cage was followed by a hand examination of foliage
were conducted to determine predator abundance and species composition. After this,
five soybean tips per cage (consisting of the uppermost node) were collected to assess A.
glycines populations. Tips were placed in plastic bags and returned to the laboratory for
counting. Then plant height was determined by measuring from the soil to the top of the
canOpy for five random plants in each cage.

2002 Predator Exclusion Trial.

In 2002, three cage treatments were used, open and exclusion, as described above
and a frame alone treatment, to control for the possible effects that plastic and screen
netting may have on conditions in cages. This treatment had the same dimensions as the
open treatment but lacked plastic and screen netting. The plot layout was a completely
randomized block design, with one cage per 6 m x 6 m area. There were five replications
with three cages in each replication, for a total of 15 cages. Two trials of this experiment
were conducted during 2002, and each trial was split into two parts (before and after cage
switch), with five sample dates for each part. The first trial was initiated on 26 June,
prior to natural A. glycines infestation in this field, when an average of 110 _+_ 10 adult A.

glycines were introduced to random plants in each cage by transferring them from

87

infested soybean sprigs to plants within cages using a thin camel hair brush. Large A.
glycines with a visible cauda were considered adults. The first trial was sampled from 28
June t012 July. On 12 July, four replicates were randomly selected then open and
exclusion cages were switched in these replications. The frame cages were never moved.
The trial was then conducted for another five sample dates from 15 July to 29 July. The
unchanged open and exclusion cages served as a control to determine A. glycines
population trajectories. These cages were sampled from 15 July to 29 July. A second
experiment was initiated on 10 July, when we artificially infested plants in each cage
with 131 i 11 adult A. glycines using the same methodology described above. This
second trial of this experiment ran from 12 July to 26 July. At this time, open and
exclusion cages were once again switched. Data was collected again from 29 July to 12
August. To accommodate increased soybean height, when cages were switched,
exclusion cages were raised approximately 10 cm. This left enough plastic to provide a
barrier to prevent entry by predators.

In both trials, data was collected every Monday and Friday. Temperature and
relative humidity data was collected as in 2001 and three-minute visual examinations
were taken using the same methodology described above. Then 10 randomly selected
whole plants were counted inside each replicate in the field to assess the adult and nymph
A. glycines population. Five plants were selected and measured in each cage and their
stage recorded on each sample date. Exclusion cages each had two 8.5 cm by 13 cm
pitfall traps with rims at the substrate level. These traps were placed in opposite comers
of the cage to reduce populations of ground-dwelling predators. Therefore, there were

ten total pitfall traps in the exclusion cages in each plot. There were also ten pitfall traps

88

placed randomly within each 6 m x 6 m plot to compare the abundance of predators in
cages and in surrounding crop. Pitfall traps were filled with 50 percent ethylene glycol
and samples were collected every seven days.
Analysis.

Data from 2001 was considered preliminary and not statistically analyzed. In
2002 a type III F -test for overall treatment effect determined the statistical significance of
treatment effects on temperature, humidity, and plant variables in open, exclusion, and
frame cages by an analysis of variance (ANOVA). Adult and nymph A. glycines,
predator, and pitfall trap counts were analyzed with a type III F -test for overall treatment
effect with the Poisson regression for counts, using the GLIMMIX Macro link of SAS
statistical program (SAS Institute 2000). From this analysis, treatment, date, and
treatment*date interaction will be reported. A significant treatment effect indicates that
means between treatments differed (P g 0.05), and a significant date effect indicates that
means were higher or lower than other dates. A significant treatment*date interaction
occurs when the effect of treatment on the date that it is being observed and vice-versa,
i.e. the effect of date will be different for each treatment. When this occurred, data was
sliced to reveal differences on particular dates. When treatment and date were both
significant, individual pair wise comparisons from LS MEANS from SAS output were
used to determine significance between individual treatments on that date. When there
was no interaction, treatment was reported as an overall treatment effect, because it was

then significant regardless of the date.

Results

89

2001 Predator Exclusion Trial.

Neither cage type appeared to influence temperature as the mean difference
between interior and exterior temperatures varied by -2 i 0.70 C in exclusion cages and -
0.6 i 04" C in open cages (Figure 4.2). Relative humidity also varied little with the
exception of 17 June, after a rainfall, where the humidity inside the exclusion cage was
approximately nine percent higher than the outside humidity (Figure 4.3). Plant growth
did not vary in any cage due to A. glycines or cages effects, as plant heights were similar
in all treatments on all sample dates (Figure 4.4).

Prior to the implementation of cage treatments in 2001, A. glycines and predators
were well established in plots. While removal of all predators from the exclusion cages
was attempted, this proved to be impossible (Figure 4.5). Further, the exclusion cages
were unsuccessful in preventing re-entry of some predator species. In particular,
Harmonia axyridis (Pallas) larvae and Orius insidiosus (Say) nymphs and adults were
found in nearly equal numbers in both open and exclusion cages, and made up a large
portion of the predators observed (Table 4.1, Figure 4.6, Figure 4.7). It was evident that
coccinellid egg masses were missed in the visual searches as concentrations of young
larvae were frequently found in subsequent searches in the exclusion treatment.

Had exclusion cages effectively reduced predator numbers, the expectation was
that A. glycines numbers inside exclusion cages would rise in relation to those in open
cages. In contrast, A. glycines adult and nymph populations in both open and exclusion
plots fell in the first two weeks of the experiment, and remained similar in open and
exclusion treatments until mid-late July (Figure 4.8, Figure 4.9). The reduction in A.

glycines adult and nymph numbers occurred at the time H. axyridis populations reached

90

their peak abundance on 3 July (Figure 4.6). In general, H. axyridis populations in both
open and exclusion cages appeared to track populations of A. glycines with peaks in H.
axyridis following aphid peaks by approximately one week (Figure 4.6, Figure 4.8,
Figure 4.9). From 24-31 July adult A. glycines numbers declined in the exclusion plots
but rose dramatically in the open plots. A second peak in H. axyridis numbers
subsequently followed this.

In contrast, populations of 0. insidiosus were low in late June and early July,
peaking on July 17‘h (Figure 4.7). There were no differences in the number of 0.
insidiosus inside the exclusion or open cages. Orius insidiosus was largely absent for the
first peak in A. glycines and reached it peak densities in plots shortly after a low point in
A. glycines populations. Orius insidiosus was unable to prevent resurgence in A. glycines
populations in the open plots but the higher numbers of 0. insidiosus in exclusion plots
are associated with a decline in adult A. glycines numbers (Figure 4.8) but not nymphs
Figure 4.9).

The placement of sticky traps in the exclusion cages did not greatly influence
predator numbers. While large numbers of H. axyridis were present in the field, few
were caught on sticky traps in exclusion cages or field areas (Figure 4.10). Orius
insidiosus populations also did not appear to have been reduced by the traps in cages, as
numbers remained steady over the trial (Figure 4.11). The mean number of ground-
dwelling predators generally decreased over time in exclusion plots, while mean number
of ground predators in the entire plot increased slightly (Figure 4.12). Carabid abundance
and species richness was lower in exclusion cages versus the surrounding study area,

indicting that exclusion cages were effective at reducing these predators (Table 4.2).

91

2002 Predator Exclusion Trials.

Temperatures inside and outside of cage treatments differed very little throughout
both trials in 2002 (Figure 4.13). Statistically significant effects, were few, and when
they did occur, they were caused by the exclusion cages differing from the open and
frame cages (Table 4.3, Table 4.4). This is likely a result of the fact that temperature in
exclusion cages was typically slightly higher, because the screen and plastic caused
ventilation to be minimal.

With one exception, relative humidity also did not vary greatly between
treatments in trial one, with the humidity difference typically slightly higher in exclusion
cages (Figure 4.14). Significant differences were only found after the switch when open
and exclusion cages had higher relative humidity than frame cages (Table 4.5). In trial
two, the humidity difference appears to be greatest in exclusion cages (Figure 4.14).
Exclusion cages generally had higher relative humidity than open or frame cages during
both parts of the trial (Table 4.6).

Plant growth was not significantly affected in either trial, and neither cage type
nor A. glycines caused plant heights to differ (Table 4.7, Table 4.8, Figure 4.15). During
trial one, plants were in V5 stage on the first sample date (28 June), and R1 on the last
sample date before cages were switched (12 July). After cages were switched, plants
were in R1 stage on the first sample (15 July) date and R2 on the last 29 July. During
trial two, plants were in R1 stage on the first sample date (15 June), and R2 on the last
sample date before cages were switched (26 July). After cages were switched, plants
were in R2 stage on the first sample date (29 July) and R4 on the last sample date (9

August).

92

Abundance and species composition of ground-dwelling predators was
consistently low in both trials and therefore their potential A. glycines feeding was likely
minimal (Table 4.9, Figure 4.16). In both trials the species richness was lower in
exclusion cages than in the field as a whole. In trial one, captures were significantly
higher on all sample dates in the crop area (Table 4.10). In trial two, captures were low
(Table 4.9, Figure 4.16) and not significantly different in cages and the field (Table 4.11),
because abundance was similar in exclusion cages and in the crop area (Table 4.9, Figure
4.11). Even though there was not statistical significance, the captures were extremely
low in this part of the experiment (Table 4.11).

Aphid and Predator Response Trial One.

After cage establishment, adult A. glycines populations in trial one increased
steadily, reaching approximately 100 aphids per ten plants (Figure 4.17). In contrast, in
open and frame cages populations remained below 10 aphids per ten plants in both cages.
Similar trends occurred for nymphal A. glycines (Figure 4.17). Statistically, exclusion
cages contained greater numbers of adult and nymphal A. glycines than open and frame
cages on most dates prior to cages being switched (Table 4.12, Table 4.13). Prior to
cages being switched, the abundance of predators was lowest in the exclusion cages,
although 0. insidiosus adults and Chrysoperla spp. were found at a very low density
(Table 4.14, Figure 4.19). Orius insidiosus adults were abundant and made up 61.7 and
55.2 percent of the observed predators in open and frame cages, respectively (Table
4.14). More predators were observed in the open and frame cages, where the species
composition was greater and consisted of a combination of foliar predators, including H.

axyridis at a low density (Figure 4.20).

93

The un-switched replicates demonstrated what occurs with A. glycines adult and
nymph populations when cage treatments were left in place (Figure 4.17). The A.
glycines population increased dramatically in exclusion cages, peaking at 1,534 adult and
2,492 nymph A. glycines per ten plants on 26 July. When cages were switched, high
populations of A. glycines were exposed to predator colonization and the low populations
in former open treatments were protected from predation. In the newly opened cages, the
adult and nymphal A. glycines populations remained constant for approximately one
week and then decreased from 103 adult A. glycines per ten plants on 15 July, to 11 per
ten plants on 26 July, and from 159 A. glycines nymph per ten plants to 40 per ten plants
on the same dates (Figure 4.17). For both adult and nymph A. glycines, there were
statistically more A. glycines in exclusion versus open or frame treatments on most days
prior to the switch (Table 4.13, Figure 4.17). This trend was significantly reversed by the
end of the test on 26 July.

When predators were excluded from formerly open cages, there was an almost
immediate increase in both adult and nymph A. glycines populations, indicating that
predators had been playing a role in keeping these A. glycines populations low (Figure
4.17). There were significant differences in A. glycines adults and nymphs when
comparing the now open versus exclusion treatments. As the A. glycines population
decreased in the open treatments, it increased in the exclusion treatments (Table 4.12,
Table 4.13).

On 19 July, there was a similar predator community in most treatments, but an
enormous increase in predator abundance in the former exclusion, now newly opened

treatments, where predator abundance jumped from below 20 predators per 3 min. to over

94

 

60 predators per 3 min. (Figure 4.19). The most abundant predators in this part of the
trial were H. axyridis adults, Leucopis spp. midge larvae, and 0. insidiosus (Say) adults,
which made up 22.9, 30.6, and 14 percent of the total predator counts (Table 4.15). For
H. axyridis and Leucopz's midges, there was a striking increase on 19 July, when the
initial decrease of A. glycines began (Figure 4.20, Figure 4.21). The population of H.
axyridis remained high as the A. glycines population decreased, but the Leucopis spp.
larvae increase was ephemeral. The 0. insidiosus population also increased on this date,
but appears to have also increased equally in exclusion and frame cages (Figure 4.22).
There were significantly more predators in the now open treatment versus the other
treatments on 19 July (Table 4.16).
Aphid and Predator Response Trial Two.

In trial two, results were qualitatively similar to trial one for the first half of the
trial. The statistically significant differences were detected on many dates (Table 4.17,
Table 4.18). The main difference was that adult and nymph A. glycines populations were
uniformly lower. Exclusion cages had higher adult and nymphal populations than open
or frame cages on most dates. Adult A. glycines population peaked at about 30 A.
glycines per ten plants, and the nymph populations peaked at about 70 A. glycines per ten
plants. Predator counts appeared to be slightly higher in open cages than in the other
treatments (Figure 4.19). During this part of the trial, the predator community was
similar to that of trial one (Table 4.19). The most abundant predator in all cages were 0.
insidiosus adults, which made up 69.9, 5 8.5, and 61.5 percent of predators observed in
exclusion, open, and frame cages. There were few statistical differences between

treatments, and the only difference occurred on 19 July (Table 4.21). While the

95

exclusion cages prevented entry by most predators, 0. insidiosus was more difficult to
remove in this experiment because as the plant canopy became more dense, visibility and
efficiency of removing predators decreased. The number of 0. insidiosus was similar in
all cages (Table 4.19, Figure 4.22). Harmonia axyridis was the second most abundant in
open and frame cages, though its population remained low (Table 4.21, Figure 4.20)
compared to trial one (Figure 4.20).

In contrast to trial one, aphid numbers did not decrease in the now open cages in
the second half of the trial (Fig. 4.18). In addition, the un—manipulated control cage, the
adult and nymph A. glycines populations never increased beyond those in the new
exclusion cage. The reason was not explained by difficulty excluding predators, since
very few predators were encountered in this cage (Table 4.20). Adult and nymph A.
glycines populations continued to increase in open, frame and exclusion cages, with the
population open cages being higher until the last sample date, when open and exclusion
cages became similar in all cages (Figure 4.18). In both open and exclusion cages, open
cages differed from the other treatments on most dates (Table 4.17, Table 4.18). Again,
predator abundance increased in open cages, but the increase was not as obvious as in
experiment one (Figure 4.19). The same three species were again the most abundant in
open cages (H. axyridis, Leucopis midge larvae, and 0. insidiosus), and again these
predators became most abundant approximately one sample date after cages were
switched (Table 4.19, Figure 4.20, Figure 4.21, Figure 4.22). This time, though,
Leucopis midges were not prevalent, and 0. insidiosus was more abundant in open cages.

These predator differences between exclusion and the other cages were significant on

96

most dates (Table 4.21). Even with significantly more predators in the now open cages,

adult and nymph A. glycines numbers did not decrease rapidly.

Discussion

Exclusion treatments were not effective at reducing the abundance of foliar-
foraging predators in 2001. Even though any predators seen in the exclusion cages were
killed or physically removed each time they were found during foliar observations this
apparently had only a temporary effect on predator abundance. Implementing this study
after A. glycines colonization and predator appearance made predator removal very
difficult. From the observations of 1st instar coccinellid larvae on plants in exclusion
cages, it was clear that coccinellid egg masses were missed. In addition, 0. insidiosus
nymphs were essentially impossible to remove, as they tended to colonize the folded tips
of newly emerging soybean leaves. These two predators made up the majority of those
found in exclusion cages. More difficult to explain is the appearance of adult
coccinellids and various other predators in exclusion cages. Even though every attempt
was made to seal the cage after sampling, it is likely that some found crevices to enter the
cages at the seams where the Velcro joined the plastic and screen parts of the cage. In
spite of the failure to create treatment differences in predator numbers, this test did reveal
the potential importance of H. axyridis and 0. insidiosus as predators of A. glycines. The
likely cause for A. glycines reduction from 26 June to 10 July was predation, since 0.
insidiosus and H. axyridis clearly responded to A. glycines populations. However, the
failure of cages to create differences in predator populations limits the understanding of

their role in A. glycines population dynamics. In 2001, temperature, relative humidity,

97

and plant height did not differ greatly among cage treatments, and were not likely
associated with the observed trends in A. glycines populations.

As in 2001, in 2002 temperature, relative humidity, and plant height did not differ
greatly among treatments. While average temperature differentials were slightly higher
inside versus outside of exclusion cages in contrast to open or frame treatments, it is
unlikely that this contributed to increased A. glycines populations inside the cages. The
optimum temperature for A. glycines development is reported to be between 22 and 25° C
in late June to early July (Wang et al. 1962). During both of our trials, the average
temperature inside exclusion cages was above 300 C by which exceeds the optimum
temperature for aphid development. Thus, it might be expected that A. glycines
population growth may have been slightly slowed in the exclusion cages in relation to
open or frame treatments.

In addition to excluding predators, exclusion cage treatments could also
unnaturally confine A. glycines on the plants. It is known that production of alate aphids
increases under crowding and plant stress conditions (Dixon 1985). Thus, emigration
may be an alternative explanation for a decrease in aphid abundance after the cages are
switched. Several lines of evidence argue against this. First, alate A. glycines were rarely
observed in exclusion cages during aphid counts and predator observations. No alates
were observed in trial one until 10 July, at this point a total of three alates were found.
Alates only became abundant in the exclusion control on 22 July, when adult aphid
populations were averaging over 1,000 per plant. In trial two there was only one

observation of alates in exclusion cages on 26 July. Coupled with observations of a large

98

increase in predator abundance following cage switch emigration is unlikely to be the
sole explanation for A. glycines reductions in the former exclusion treatments.

In contrast to 2001, in 2002, most predators were successfully reduced in
exclusion cages and tests provided strong evidence that predators were effective at
keeping A. glycines densities low. Actively foraging predators, particularly C.
septempunctata, H. axyridis, and 0. insidiosus, continually removed A. glycines in open
and frame treatments keeping populations low in comparison to exclusion treatments.
Having these treatments side by side eliminates the possibility that environmental
conditions were the cause of limited A. glycines populations. In contrast, where predators
had free access to plants they prevented an aphid outbreak while adjacent plots with
predator exclusions reached thousands of aphids per ten plants. Collectively, predators
showed the ability to keep initial A. glycines populations low (both trials) and quickly
decrease high A. glycines populations when cages were switched (trial one only). This
study also bolsters the findings of Van den Berg et al. (1997), where Harmonia spp.
contributed to the reduction of A. glycines populations.

Overall, the findings also agree with Grasswitz and Burtz (1995) and Chen and
Hopper (1997), who found that aphid densities were controlled by a community of foliar-
foraging predators. During these trials, H. axyridis and 0. insidiosus were consistently
the most abundant predators. Leucopis midge larvae were only abundant during one
sample date. It is possible that they have an ephemeral period of abundance, or that they
provided a secondary food source for H. axyridis and 0. insidiosus. It is unlikely that 0.
insidiosus alone can successfully suppress A. glycines populations, since pOpulations

were similar in all cage treatments after cages were switched in trial one. Despite this

99

similarity in 0. insidiosus populations, there was an increase in exclusion cage aphids
within one week. However, it is possible that 0. insidiosus and H. axyridis may interact
in a positive way to increase A. glycines control.

The overall increase in A. glycines populations in the absence of predators and the
reduction of A. glycines populations when predators were allowed access was greater in
the first trial when plants were smaller and at an earlier phenological stage. Van den
Berg et al. (1997) showed that A. glycines intrinsic rate of increase decreased as soybeans
age. It may be that in the first trial of 2002, A. glycines populations were able to respond
to the lack of predators due to more suitable host plant quality. In turn, predators may
have had an easier time foraging for A. glycines on these smaller plants with less foliage.
When plants are smaller and the canopy less dense, prey have fewer places to hide and
predators have less foliage to search. The opposite may be true when plants mature, as in
trial two, where plants were both taller and had thicker foliage. A study by Garcia and
O’Neil (2000) bolsters this argument, because they found that predation by the
coccinellid C ryptomaemus montrouzieri Mulsant on the citrus mealybug, Planococcus
citri Risso, decreased as Coleus plants increased in size. They suggested that plant
characteristics were the most likely reason for this decrease in predator efficiency found
in their study.

These studies indicate an important role for existing predators in A. glycines
control in Michigan. With apparently strong A. glycines suppression by existing
predators already in place, introduction of additional biological control agents should be
done with caution. It is likely that existing predator communities would interact with

introduced parasitoids (Colfer and Rosenheim 2001) and may slow or prevent their

100

 

establishment. In contrast, combinations of natural enemies may be found that provide
more complete of more reliable aphid suppression. Consideration of these potential

interactions prior to the release of additional natural enemies is recommended.

101

 

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Table 4.2. Species composition, total, and percent ground dwelling predators captured

per seven days in exclusion cages versus those in the surrounding field during 2001.

Pitfalls were sampled once a week from 26 June to 31 July, 2001, East Lansing,

 

Michigan
E
Order Coleoptera Exclusion Entire Plot
Family Species Total % Total %
Carabidae Agonum cupripenne Say 2 6.3 2 0.3
Agonum placidum (Say) - - 136 22.4
Amara aenea (De G.) 2 6.3 35 5.8
Amara apricaria (Payk.) - - 1 0.2
Amara rubrica Haldman - - 8 1.3
Anisodactylus rusticus (Say) - - l 0.2
Anisodactylus santaecrusis (F.) 9 28.1 96 15.8
Bembidion quadrimaculatum Say 1 3.1 30 4.9
Bembidion rapidum (Le C.) - - 2 0.3
Bradycellus rupestris (Say) - - l 0.2
Chlaenius pusillus Say - - 3 0.5
Chlaenius tricolor Dej. - - 2 0.3
Clavina bipustulata (F.) l 3.1 4 0.7
Clavina impressefrons Le C. - - 15 2.5
Colliutis pensylvanicus - - 1 0.2
Cyclotrachelus sodalis (Le C.) 1 3.1 11 1.8
Elaphropus anceps (Le C.) 4 12.5 63 10.4
Harpalus affinis (Schrank) - - 3 0.5
Harpalus pensylvanicus (De G.) - — 5 0.8
Poecilus chalcites (Say) - - 23 3.8
Poecilus lucublandus (Say) - - 11 1.8
PIerostichus commutable (Motsch.) - - 1 0.2
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> 1 m
A A
Fine mesh netting
0.9 m f: A A A {5
Plastic barrier
B.
0.7 m
i
Pitfall

Figure 4.1. Design of 1 m2 cages used during 2001—2002. Both cage types contained the

same cage materials to account for potential cage effects. A. open and B. exclusion.

123

LID-Open '
+____ Efiflysion 5

p—
_4A

0 I I.

Mean (i SEM) temperature (°C) difference
(interior minus exterior)

-2 ,7 -. 7 i , _
_ —' _ "" '_ 00 C0 50 DD Q-
: 3 D 3 3
‘-' “r —.. -* —.. 2 2 2 2 a
m O F V "‘ I I I I é.
— —‘ N m [\ V '— co
— N N

Figure 4.2. Mean 0: SEM) temperature difference (°C interior minus the oC exterior) of

open and exclusion cages during 2001, East Lansing, Michigan.

124

l
'0'0pen I i
rflclusig j i

 

 

Mean (_+_ SEM) relative humidity difference
( Interlor trunus exterior)

 

l
I

 

3-Jul ‘
lO-Jul ‘
l7-Jul
24—Jul
3l-Jul
7-Aug
14-Aug ’
21-Aug “
28-Aug ’
4-Sep 7_o

Figure 4.3. Mean (i SEM) relative humidity difference (interior minus the exterior) of

open and exclusion cages during 2001, East Lansing, Michigan.

125

 

  
 

80‘

75 ,. A-U-Open i
70 ‘

1 1
1+Exclusion 1

 

 

 

 

 

3

5

a 65 .

W 60 1

$—

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E 30

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t:

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o. 1

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s ,0 .

2 5 1
O ,i? v Li

3-Aug l
10-Aug ‘
l7-Aug ”

6-Jul
l3-Jul A
20-Jul "
27-Jul

29—Jun '

Figure 4.4. Mean height Ct SEM) in cm of five randomly selected soybean plants in the

open and exclusion treatments during 200l, East Lansing, Michigan.

126

 

 

<15
.0
O T— LLL _
a g-D-Open 1
E 20 ‘ 1+Exclusion i
"=3 1
1
5 1
.E 1
2 15 '
m
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: _ '—' '—' '_' '_ 00 00 00 50 o-
2 .2 .2 s; 2. 2. .2 = = = = g
. «a :5 I; e —: <.< <5 3‘ ‘F -
2?; — ~ N m l\ v — oo ‘1'
v— (\I N

Figure 4.5. Mean (i SEM) abundance of foliar-foraging predators based on a
combination of 3-minute non-intrusive visual examination followed by hand

examinations of foliage in the open and exclusion treatments during 2001, East Lansing,

Michigan.

127

 

N
M
1
1
1
1
1
1

I

 

 

 

 

 

 

 

M

i-I

a 1-o-‘6—“‘

.2 20~ .- I pen. 1

:3 1+_Exclusnon1

k U)

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s: "‘ "‘ "" "‘ 60 DD 00 DO 00
:I 3 3 3 3 :1 :I :I :I :I
-= 2 .7: 3 2 < < < < <.<
33 - N N «'5 o' :x' ~¢' _.

_q — N M

Figure 4.6. Mean (3; SEM) abundance of Harmonia axyridis adults and larvae based on
a combination of 3-minute non-intrusive visual examination followed by hand
examinations of foliage in the open and exclusion treatments during 2001, East Lansing,

Michigan.

128

—
U1
1
1
1
1
1

m
g 1
g -Cl-Open ; 1
% l-O-Exclusion 1 ‘
m -__h - __.
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_=, 2. .5: a a a = = = = g
. «a :5 1; a J— ‘F ‘F ‘F 5‘ 1
(<3. —. .— N m l‘ v — 00 v
-' N N

Figure 4.7. Mean (i SEM) abundance of Orius insidiosus adults and nymphs based on a
combination of 3 minute non-intrusive visual examination followed by hand
examinations of foliage in the open and exclusion treatments during 2001, East Lansing,

Michigan.

129

 

 

 

 

 

Figure 4.8. Mean (i SEM) adult A. glycines population per 5 plant tips during 2001 in

open and exclusion cages during 2001, East Lansing, Michigan.

130

1.0-Open

tn 1 . .

E " 1* Exclusnon

m - __ .

E

Q I-

3.» 10

co

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6 m C l\ V '-' I I I I
N .— —— N m h E (T. :3

4-Sep 1- ___

40 ‘ ..

 

 

 

 

l
l

 

 

 

 

Mean number (i SEM) of nymph A. glycines/ 5
plant tips

‘i
I
g '5 3 '5 '3 3 :9
v-; '7‘ '7 '7 '7‘ _I‘ <
b M O t‘ V "‘ I
N v—q —— N m [\

l4—Aug ‘ I

::0- Exclusion ‘
I
on on a.
:I :I o
< <2 ”.1
.1. 05 v
N N

Figure 4.9. Mean (i SEM) nymph A. glycines population during 2001 in open and

exclusion treatments during 2001, East Lansing, Michigan.

131

 

12:-Exclusion cage‘
fx— Entire plot 1

.O
\l
u:

 

 

 

 

Mean no. (-_+-_ SEM) of H. axyridis found per two
sticky traps per seven days

0.5 -
T

.I. T 1-

o.25 11 l 1
1 T., J

1 .L 1

|

0 1% a +—- a .0 v

3 E E E .25

“1 :5 Sf. x' «7"»

Figure 4.10. Mean (i SEM) abundance of Harmonia axyridis (Pallas) found on sticky

traps in the exclusion cages versus those found in the entire plot during 2001, East

Lansing, Michigan.

132

1;Exclusion cage 1 l 1
1-5- Entire plot

b.)

 

 

Mean no. (i SEM) of 0. insidiosus found per
two sticky traps per seven days
N

J.
l T
1':
L A
'1- l I
l I I
0 k1 A1 ' if —* I 7 h Tqi _ ___—‘i” 7 T“ I
'5 '5' '3 E '5
'7 '7’ '7‘ '7’ '7‘
m o l\ v ~—
-— —I N m

Figure 4.11. Mean (i SEM) abundance of Orius insidiosus (Say) found on sticky traps

in the exclusion cages versus those found in the entire plot during 2001, East Lansing,

Michigan.

133

1 1

 

 

 

'o

2

8 ———*Ak — .

::: -'X- Exterior pitfalls

o . .

0 +Exclu510n cage pitfalls l

i3 ‘9. ‘ r ' r

a g

a)

.o r:

“O °>’ T

g 3 1 T

2 33 ll

:1" °- 1 ;

o g 11:

"‘ b u T

2 5 fi

54, o.

3 J

‘ TT 1

2 0 7‘ V .' A # 7 A 7 air A _ __ ._,, _¥3
":5 ":3 '5 ":3
'7 7 7 '7

Figure 4.12. Mean (i SEM) predator/pitfall trap/day of ground beetles in pitfall traps in

exclusion cages versus those in the study area during 2001, East Lansing, Michigan.

134

 

 

 

Mean (i SEM) temperature (° C) difference
(interior mmus exterIor)

-4 r. , W, , -._-_.,, ,.
+Exclusion then Open
-6 —'D—Open then Exclusion
——A—— Frame
-8 . .
— -O- -Exclusron control
_10 ,j — -E.I- -Open control
-12 . ”Effie“ mg
g '5' '5 ‘3' '5 '5 ‘2' '3'
—. —.~ ’1' 7 '7 7 7 "r
50 N \o o v 00 m \o
N u— —- I-! N N

 

 

Mean (i SEM) temperature (°C) difference
(interior minus extenor)
L

28-Jul l
l-Aug l

lZ-Jul
l6-Jul 7
20-Jul
24-Jul f

Figure 4.13. Mean (i SEM) temperature difference (°C interior minus the °C
exterior) in open, exclusion, and frame cages during 2002. The arrow indicates when
open and exclusion cages over 1 m2 plots were switched during: A. Trial one; and B.
Trial two. One randomly selected replicate had cages that were not switched to show

the trend if cages were not switched.

135

 

30 'A.* i 7 7 ¢ f A a.

25 i 'r
l ~-;Exclt:sionmen Open ’ l

20 l—D—Open then Exclusion 1

i —-A-——Frame

1 - -O - Exclusion control

 
 
   

15

 

10 - :- Open control

  

(interior minus exterior) per

 

Mean (i SEM) relative humidity difference

5 z
0 ‘
-5 l
db V
-10 = * fl .
g 3 3 ‘5 ‘5 3 '5 3
-—. '7’ '7 '7 '7‘ "R '7' H
0;, N o o v co m <5
N u— v—I —‘ N N

N N a»
O U! 0
w
|
|
4 J

_
U!

M
1

O

 

I
M
i

 

 

Mean (i SEM) relative humidity difference
(interior minus exterior) per
<3 ES

24-Jul
28-Jul
l-Aug
S-Aug
9-Aug

3 '5
'7 7
N \0
~ _

Figure 4.14. Mean (i SEM) relative humidity difference (interior minus the exterior)

ZO-Jul

in open, exclusion, and frame cages during 2002. The arrow indicates when open and
exclusion cages over 1 m2 plots were switched during: A. Trial one; and B. Trial two.
One randomly selected replicate had cages that were not switched to show the trend if

cages were not switched.

136

' A.
110 ' ' ” i
3 —o—Exclosure then Open ;
100 ' —c)—Open then Exclusion
% 1 ' -‘ '— Franc ‘
80 — + - Exclusion control

— -CI- — Open control

  

Mean plant height per 5 plants
5’

 

m.
50-
40 L
30‘ :
zol . ~ e I ~9
5 E E E E E E E.
_a l a I o l i o
33 N ‘0 2 3 E 8 :9.
120 - ~~ ——
3110 :
5100‘
cu.
.n 90
h .
a 80 ,4
E .
.20 70
_g 60
‘5' 50-
"5.. 40.
5
E 30*
20 ~ ,, —~ ~ , f — — ~- ——
'5 '5 '5 '5 “:5 on °° °°
2. 3; a 3 :2 5.3 5.5 3.5
.— --I N N N —- V3 0‘

Figure 4.15. Mean (i SEM) plant height per five plants in open, exclusion, and
frame cages during 2002. The arrow indicates when open and exclusion cages over 1
m2 plots were switched during: A. Trial one; and B. Trial two. One randomly selected

replicate had cages that were not switched to show the trend if cages were not

switched.

137

l 7 if. _, ,i 7" ..—, fig.

A. !

*Extegorpitfalls V
‘-0—Exclusion cage pitfalls

 

trap/ day

 

 

Mean (i SEM) predator/ pitfall

 

0 A ifi 7—7——— ~ . -
'5 '5 '3 '5 3 '3

7 *9 7 r: '7 7

V} 0‘ C" l\ —i m

"" —‘ N N

 

trap/ day

 

 

 

 

 

 

Mean (i SEM) predator/ pitfall

 

l
I

 

0 hj—i‘a—+~W~7~——-~——~ T
:3 :3 3 D
O\ M (\ '-' I I
v-I N N M V 00

Figure 4.16. The mean (i SEM) abundance of carabid beetles collected per seven
days in 10 total pitfall traps from exclusion cages (2 traps/ cage) versus 10 total pitfall
traps placed randomly in the study area during 2002: A. Trial one; and B. Trial two.
The arrow indicates when open and exclusion cages over 1 m2 plots were switched, at

which time eight pitfall traps were in exclusion cages and eight within the plot.

138

10000 . 77,, 7* v i , J 7, i 7 i ' i‘
_A. 7
‘TS— Exclusion'thenTOpen
1000 } —O—Open then Exclusion : z ’
——A—- Frame . I
“ — 9- Exclusion control / X
100 ,: 0'. 'Qgeniontrol , l

 

Mean number (i SEM) of adult A.
elvcmes/ 10 plants

 

0.1 r — . ,,, -. a _- - _ .,

2-Jul
6-Jul
lO-Jul
l4-Jul
l8-Jul

28-Jun
22-Jul
26-Jul

 

10000 . H, -,

‘ .55

1000 -- , I

§

O

 

Mean number (i SEM) of nymph A.
alvcmes/ 10 plants

 

 

 

0.1

a

2-Jul
6-Jul
10-Jul *
l4-Jul
18-Jul l
22-Jul
26-Jul .

28-Jun '

Figure 4.17. Mean (i SEM) adult (A.) and nymph (B.) A. glycines population (log
scale) per ten whole plants in open, exclusion, and frame cages in trial one during
2002. The arrow indicates when open and exclusion cages over 1 m2 plots were
switched. One randomly selected replicate had cages that were not switched to show

the trend if cages were not switched.

139

 

 

10000 : ,_ ____,i , —— r ,i, - , .7, ,

 

   

 

  

 

 

vi ,A.

g 1000 . —O—Exclusion then Open

‘05 .2 l —D—Open then Exclusion

E g 1 — A—- Frame

m g 100 l - -O— ‘Exclosion control

(2' : — 6- Open control

V 8 ’ii'

i... E 10

3 a

S a

s: 1 +

c: I

a

a)

2 0.1 . i - - ~ — if _ ~—
'5 '5 '5 '3 ‘5 g0 g0 g0
-—. -s -s t-i H
(4. a :5 s ob <5 ‘F at
w— --I N N N F— W 0‘

10000 -» —— - — -— — -— — — — ——
B.
1000 *

 

 

 

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'3‘ '5 '5 '5 '5 g0 g0 g0
3'} 12 3 2'3 22 ‘F fi< ‘F
— '— N N N — W 0‘

Figure 4.18. Mean (1- SEM) adult (A.) and nymph (B.) A. glycines population (log
scale) per ten whole plants in open, exclusion, and frame cages in trial one during
2002. An arrow indicated when open and exclusion cages over 1m2 plots were
switched. One randomly selected replicate had cages that were not switched to show

the trend if cages were not switched.

140

 

120 T , it _, 7—7 — , — fl ’

 

 

    

 

 

 

.5 A.
:9: _ i ..

“o 100 7 +Exclusron then Open

g —D—Open then Exclusion ‘

'E ' +Frame .
2 80 s _ l
m . ' ° 0 ' - Exclusron control ‘
g 7:7‘Efg'9pen control

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m

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N ._ ._. —- N N
S 120 ~ , . 7w f *A' _q. k" ’** “7
'—= B. ‘
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m i
g l
A m 60 l
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h I
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a ... ” '
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—.. -.~ -.~ -.» -.~

In 0\ M 1‘ "‘ it it it

— --' N N M V w N

Figure 4.19. Mean (i SEM) abundance of foliar-foraging predators based on a
combination of 3-rninute non-intrusive visual examination followed by hand
examinations of foliage in the open, exclusion, and frame treatments during 2002.
The arrow indicates when open and exclusion cages over 1 m2 plots were switched
during: A. Trial one; and B. Trial two. One randomly selected replicate had cages

that were not switched to show the trend if cages were not switched.

141

OJ
C
|
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I
i
|

\

 

 

 

 

2 iA. .
+| 25 —0—Exclusion then Open
V i
{J . —D—Open then Exclusion l
as ,8 s I
E o 20 . ; +Frame ;
f; g : 1 --+--Exclusion control

0
g ‘o— 15 ’ --EI--Open control
a "g __ 4* " i
E "‘- 1

c:
3'" 10 .
o. 2
73 m
k 3—
3 8. 5 -
t'
c
33 0 i: _ __ _ __ __ __ __
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0;, m c o v 00 m o
N ._ —- c— N N

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2 u
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a g 20 . 1
.53 a i
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a? 2 s-
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g

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S o.

O _ _ V7 . ,,

t 2 2 :=. 2 2‘ 2? a? a
g: . . . . . < < <
('3 V3 0‘ m l‘ "" I I I
2

Figure 4.20. Mean (i SEM) abundance of Harmonia axyridis (Pallas) adults based
on a combination of 3-minute non-intrusive visual examination followed by hand
examination of foliage in the open, exclusion, and frame treatments during 2002. The
arrow indicates when open and exclusion cages over 1 m2 plots were switched during:
A. Trial one; and B. Trial two. One randomly selected replicate had cages that were

not switched to show the trend if cages were not switched.

142

 

Figure 4.21. Mean (i SEM) abundance of Leucopis midge larvae in based on a
combination of 3-minute non-intrusive visual examination followed by hand
examinations of foliage in the open, exclusion, and frame treatments during 2002.
The arrow indicates when open and exclusion cages over 1 m2 plots were switched
during: A. Trial one; and B. Trial two. One randomly selected replicate had cages

that were not switched to show the trend if cages were not switched.

143

"o 30 . W, 7 , ,- , v E i
g lA.
E 70 i -—O—Exclusion then Open 0’ T
m 60 -. —D—Open then Exclusion
5.. I
8‘ +Frame
g 50 " - - -O - - Exclusion control
E2 :3 40 i , - 0:996" “"1901
10' :3
g ::: 30 -
E «2
-—- 20 '
.2
Q
g 10 -
3 .
'3 O .. I
E g '3 '3 3 '5' 3' s '3
‘U H '7 "l' '7‘ '7 '7‘ '7 H
E 0,3 N ‘° 2 2 1°. 5:} 3
'0

80 - — of- i g
5 B.
::'
-— 70 .
E
m
,_ 60 .
a i
E - '
m 3 4o ._
dj 0
a; .5. _‘
g ._ 30 1
a 8 1
5. 20 ~
.52 .
Q. . .
8 10 j-
a: r E
3 0 iH—W—l—m—G'
f"; T? L? 37: :3 3 3’ 3°

tn 0\ m 1‘ ~ . .

2 —. —- N N m v 00

 

lZ-Aug

25-v~ 7* f f f f. i i i~i M,,._‘
A. l

20 l r:.—Exclusion then O_pen (
1
l

55 I —D—Open then Exclusion

:15 1 +Frame : l
:.:: 1 \ ' '0 --Exclusion control g ,' g l
‘49 g l I I s

u g 1 -__:='_'_- 'Ommr°'__ % .' a '.

r: 10 ~ .

cc:

.5:

2

Mean 0. insidiosus (1; SEM) per 3

 

 

 

g '5' '5 '3 '5 '5' '3 '3

--. 7 7 H 7 -.~ '-.~ '7

0;, m o :5 v 00 N o
25---. ,h, , , 7 - 1

 

 

 

Mean 0. insidiosus (i SEM) per 3
Mm and foliar obs

 

 

lS-Jul
l9-Jul
23-Jul l
27-Jul

3 l-Jul
4-Aug
8-Aug
12-Aug

Figure 4.22. Mean (i SEM) abundance of Orius insidiosus (Say) based on a
combination of 3-minute non-intrusive visual examination followed by a hand
examinations of foliage in the open, exclusion, and frame treatments during 2002.
The arrow indicates when open and exclusion cages over 1 m2 plots were switched
during: A. Trial one; and B. Trial two. One randomly selected replicate had cages

that were not switched to show the trend if cages were not switched.

144

Literature Cited

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Chang, GO, and P. Kareiva. 1999. The case for indigenous generalists in biological
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Chen, K., and KR. Hopper. 1997. Diuraphis noxia (Homoptera: Aphididae)
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Colfer, R.G, and J .A. Rosenheim. 2001. Predation on immature parasitoids and its
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Dixon, A. F. G. 1985. Aphid ecology. Blackie and Son. New York.

Frazer, B. D., and N. Gilbert. 1976. Coccinellids and aphids: a quantitative study of
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Garcia, J .F ., and RJ. O’Neil. 2000. Effect of Coleus size and variegation on attack
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Grasswitz, T.R., and E. Burts. 1995. Effect of native natural enemies and
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aphidimyza (Rondani) on the population dynamics of the green apple aphid, Aphid
pomi De Geer. International Journal of Pest Management. 41(3): 176-183.

Han, X. 1997. Population dynamics of soybean aphid Aphis glycines and its natural
enemies in fields. Hubei Agricultural Sciences. 2:22-24.

Hance, T. 1987. Predation impact of carabids at different population densities on
Aphisfabae development in sugar beet. Pedobiologia. 30: 251-262.

145

Hilbeck, A., C. Eckel, and G. Kennedy. 1997. Predation on Colorado potato beetle
eggs by generalist predators in research and commercial potato plantings. Biological
Control. 8: 191-196.

Hirano, K., K. Honda, and S. Miyai. 1996. Effects of temperature on development,
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Landis, D.A., and W. Van der Werf. 1997. Early-season aphid predation impacts
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371 .

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146

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147

APPENDIX A

Effects of soybean varieties on A. glycines survival and reproduction

This test was conducted to determine how adult A. glycines survival and
reproduction on the soybean varieties Mycogen (5152RR) and Pioneer (93B82) that
were used in our 2001 and 2002 field and laboratory studies, compared to other

common soybean varieties used in Michigan.

Materials and Methods
Insects.

During late June 2002, soybean aphids, Aphis glycines Matsumura, were
collected from soybean fields in East Lansing, Michigan. Aphids were transferred to
greenhouse grown Mycogen (5152) soybean plants and reared in a growth chamber
held at approximately 25 0C and 70 percent relative humidity and a photoperiod of
16:8 (L:D).

Plant Preference.

Six varieties of commonly grown soybean in Michigan were used for this
study: Mycogen (5152RR), Pioneer (93B82), Michigan Grown (Jock), Asgrow
(AG2602), DSR 232 (Nematode Resistant Variety), and Garst (D261RR). Plants
were grown from seed in the greenhouse in 10 cm2 diameter pots. When plants
reached the V3 stage, they were transfer to the lab for testing. Apterous adult A.
glycines were confined on plants in 1 cm circumference clip cages constructed of 1.8
cm diameter Cresline® PVC pipe and their survival and reproduction measured over

3 days.

148

Five adult A. glycines were placed on each plant, two in one cage, and three in
another, attached to the underside of the middle (V2) trifoliate soybean leaf. Six
replicates (plants) of each variety were used, and a set of three replications of each
variety were randomly selected and placed in a one of two growth chambers held at
approximately 25 i 1 0C degrees Celsius and 80 percent relative humidity. Three
complete trials of this experiment were conducted.

Aphids were confined to these cages for 72 h (three days), and at 24 h (1 day),
48 h (2 days), and 72 h (3 days), data was collected on the total number of adults
remaining and the offspring produced on each variety to detennine if there was a
difference in adult survivorship or offspring production between varieties.

Analysis.

Adult survival and nymph production over the course of three days was

determined by a Chi-square test at P g 0.05, using the GENMOD procedure of SAS

(SAS Institute 2001).

Results

There was no significant effect of soybean variety on adult A. glycines
survival in any trial (Table 1, 2, 3). Adult numbers generally decreased slightly
during the three days of the trial due to either natural mortality, accidental crushing of
aphids when replacing clip cages, or a combination of both. There was a significant
effect of day (P: 0.02) only in trial three, where aphid survival decreased
significantly from day one to three (Table 3).

In contrast, soybean variety significantly affected nymph production and
survival. There was a significant variety effect in all three trials (P < 0.002; P < 0.001;

P < 0.001), as well as a significant block effect (P < 0.002; P < 0.004) in trials two

149

and three. There was also a significant (P < 0.001; P < 0.001; P < 0.001) day effect in
all three trials, as nymph numbers generally increased over time.

Looking across the trials several trends emerge. Asgrow (AG2602) had the
highest final nymph production at three days in two of the three trials while DSR 232
had the lowest nymph production in two of the three trials. Mycogen (5152RR) and
Pioneer (93B82) were never significantly different from each other in nymph
production or survival. They were also never different from the variety with the
highest nymph production/survival in any trial. These results indicate that these two

varieties are suitable host for A. glycines nymph production/ survival.

Discussion

These tests showed that A. glycines adults are capable of surviving on a variety
of soybean cultivars used in Michigan. We found no evidence that adult survival
differs among any of the six varieties tested. We did detect differences in nymph
production/survival among the six cultivars. The cultivars selected for field trials did
not differ from the best variety in their suitability for nymphs; therefore, it is highly
unlikely that the field trial results are biased due to poor adult survival or low
offspring production/survival. This experiment shows that in relation to A. glycines
adult survival and reproduction, the varieties selected were broadly representative of
what Michigan farmers may experience. It was also observed that the nematode
resistant variety DSR 232 may be less suitable for A. glycines and should be explored
further in lab and field trials to determine its utility in an A. glycines management

program.

150

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153

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.: 2002-11

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

BIOLOGICAL CONTROL OF THE SOYBEAN APHID, APHIS GLYCINES
MATSUMURA (HOMOPTERA: APHIDIDAE)

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

Entomology Museum, Michigan State University (MSU)

Other Museums:

Investigator’s Name(s) (typed)
Tvler 8. Fox

 

 

Date 12/9/02

*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.

154

 

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