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Shaun A. Langley

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THE ROLE OF NON-CROPPED VEGETATION IN FACILITATING THE
RESPONSE OF PARASITOIDS TO SOYBEAN APHIDS (APHIS GL YCINES)

By

Shaun A. Langley

A THESIS

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

MASTER OF SCIENCE

Department of Entomology

2007

ABSTRACT

THE ROLE OF NON-CROPPED VEGETATION IN FACILITATING THE
RESPONSE OF PARASITOIDS TO SOYBEAN APHIDS (APHIS GL YCINES)

By
Shaun A. Langley

Soybean aphid, Aphis glycines, has become an important agricultural pest in the
Midwestern United States. Here I present a study that identifies the parasitoid natural
enemy community of the soybean aphid and the role non-crop habitat near soybean plays
in attracting parasitoids to attack the aphid. The parasitoid community consists of
Lysiphlebus testaceipes (Cresson), Binodmys kelloggensz's Pike, Stary, & Brewer,
Aphelinus albipodus (Hayat & Fatima), Aphelinus asychis (Walker), Aphidius colemani
Viereck, Diaeretiella rapae (McIntosh), and Praon sp. Lysiphlebus testaceipes was found
abundantly attacking soybean aphids in soybean fields rather than aphids in adjacent non-
cropped habitat. However, B. kelloggensis apparently did not discriminate between
habitats when foraging for hosts.

I measured plant diversity within three non-cropped habitat treatments and
compared plant diversity with parasitoid recoveries. Lysiphlebus testaceipes responded
positively to increasing plant diversity in treatments mowed twice per month; B.
kelloggensis showed a similarly positive relationship with increasing plant diversity, but
within treatments mowed once at the beginning of the study. The simple farm practice of
mowing field borders is not sufficient to aid in parasitoid transition to use soybean aphid
in soybean, but the role of non-cropped habitat to attract parasitoids to soybean aphid is

clarified when plant diversity of the field border is added to the analysis.

COPYRIGHT BY
SHAUN A. LANGLEY
2007

To Courtney, with my gratitude for your love, patience, and support in helping me

through this project.

iv

ACKNOWLEDGEMENTS

I would like to thank my advisor, Michael Brewer, for his time and patience. His
guidance has taught me the necessary skills to carry out and complete a successful
research project. Furthermore, his knowledge of biological control methodology and his
familiarity with agricultural issues was invaluable in directing me to finding the answers I
needed. I would also like to thank him for his time and dedication in revising my thesis,
and seeing it to completion. Without his feedback, I would not have had the confidence
or support I needed to finish writing. I would like to thank the members of my M.S.
research committee, Doug Landis, Stuart Gage, and Carolyn Malmstrom, for their
expertise and feedback in developing and completing my project and in the analysis of
the results. l am also grateful for all their comments towards improving the quality and
clarity of this manuscript.

1 would like to thank the members of my lab, Takuji Noma and Matthew Kaiser,
for their support in helping me collect and process my samples as well as interpret the
results of my study. Their knowledge of soybean aphids and parasitoids was invaluable in
my understanding of the system. I am also grateful to all the undergraduate students who
have helped me over the past two years in collecting and identifying parasitoids, Martin
Villarreal, Ananda Jenkins, Kim Wagner, Momoko Minakawa, and Jared Natzke.

I extend my gratitude to Chris DiFonzo, Mike J ewett, and Chris Sebolt in
providing me with supplies on short notice that were necessary for me to complete certain

aspects of my research.

I would like to thank Drew Corbin (KBS LTER), Jim Bronson (KBS Dairy
Farm), Stu Bassett (KBS Grounds), Dale Mutch (Extension), Suzanne Sippel (KBS
LTER Data Manager), Terry Davis (Entomology Farm), Kevin Newhouse (Entomology
Farm grounds), and Bill Chase (Horticulture Farm) for their support in every aspect my
research project from construction to implementation. Without their support and
cooperation, I would not have achieved success in my work. In addition, my extreme
gratitude goes out to Rob Tempelman and Randy F otiu for their assistance in helping me
work through the analysis of my data and come to useful and relevant conclusions.

Thank you to Ed Grafius, Adam Byme, Carrie Scheele, Rachel Olson, and Dan
Nortman for their thoughtful comments and dedication to helping me improve the quality
and clarity of Chapter 2. Their support made the work simple and fun.

I would like to extend my many thanks and gratitude to Jill Kolp, Angela
J emstadt, Heather Lenartson, and Linda Gallagher for their secretarial support and
assistance with the financial workings of my research. Thank you to Rich Merritt for his
support as Department Chair and his assistance with helping me coordinate my position
in the department.

Thank you to Jeff Evans, Courtney Jones, Anna Fiedler, Lauren Brown, Cass
Hauserman, Julianna Tuell, Mary Gardiner, Rudy Marin, Dr. Dan Sklansky, Sandra
J apuntich, Steve Kennedy, Amy Wehrman, Joy Landis, Rebecca Lamb, Dr. Larry Olson,
Dave Epstein, and many others for their the friendship and care they showed me during
good and bad times over the last two years. Their support went a long way in helping me

through my graduate experience.

vi

Funding for this research was made possible by Michigan State University’s
Project G.R.E.E.E.N, NC IPM Center Regional Research grant, and the NSF Long-Tenn
Ecological Research Program at Kellogg Biological Research Station in Hickory C omers,
Michigan.

Finally, I would like to extend a special thanks to my new, super awesome wife
Courtney Gallaher, Sir Harold, my parents Mervin and Shirley, siblings, and relatives for
their love and support of me through this time. They have provided me with financial and
emotional support that has made me who I am today. Without their love, I would not

have succeeded and I am grateful to them.

vii

TABLE OF CONTENTS

List oftables ........................................................................................................................ x

List of figures ..................................................................................................................... xi

Key to symbols and abbreviations ................................................................................... xiii
Chapter I

Soybean aphid (Aphis glycines) Biology and Associated Natural Enemies in North

America

Introduction .......................................................................................................................... l

Soybean Aphids — Aphis glycines Matsumura ............................................................... 2

Parasitic Natural Enemies of Soybean Aphid ................................................................. 3

Fundamentals of Biological Control Applied to Soybean Aphid ................................... 5

Spatial Response of Parasitoids to Aphis glycines ......................................................... 5

Chapter Preview .............................................................................................................. 7
Chapter 2

Does Management of Non-Cropped Habitat Near Soybean Fields Benefit (or Create
Spatial Constraints to) the Use of Soybean Aphid (Aphis glycines) by Parasitoids?

Introduction .......................................................................................................................... 8
Methods ............................................................................................................................. 1 I
Study System ................................................................................................................ l I
Study Site ...................................................................................................................... l 1
Statistical Analysis ........................................................................................................ 13
Results ................................................................................................................................ 14
Site Effects .................................................................................................................... 14
Spatial Constraint to Habitat Type ................................................................................ 19
Discussion .......................................................................................................................... 23
Chapter 3
Parasitoid—Host Association Depends on the Diversity of the Background Plant
Community
Introduction ........................................................................................................................ 25
Methods ............................................................................................................................. 26
Study System: Soybean aphid ...................................................................................... 26
Study System: Parasitoid Community .......................................................................... 27
Experimental Design ..................................................................................................... 28
Statistical Analysis ........................................................................................................ 30
Results and Discussion ...................................................................................................... 34

viii

Chapter 4
Research Summary

J ustifications ..................................................................................................................... 44
Linking the results from two studies ................................................................................. 44
Future direction of research .............................................................................................. 45
Implications for biological control ................................................................................... 46
Appendix I ......................................................................................................................... 47
References .......................................................................................................................... 49

ix

List of tables

Table 2.1 Mean values :I: SEM are presented for the number of parasitoids recovered in
each treatment-soybean transect for all field sites at each of the four sampling dates.
Using MANOVA contrast statements, I was able to test a priori hypothesis of differences
in the abundance of parasitoids in non-cropped habitats and soybean. F and P values are
presented for these contrast statement for L. testaceipes and B. kelloggensis, at each of
my four sampling dates ............................................................................. 20

Table 3.1 Average proportion cover (3: SEM) for all species detected in each sample in
the mowed A treatment is presented here in this table. Measurements were made by
throwing a 0.25 m quadrant into each treatment four times. Estimates of cover were made
visually taking into account the total number of species within the sample quadrant. Plant
species cover was measured once in late September and again in mid October with the
exception of the Entomology Farm, which was sampled in October only .................. 32

Table 3.2 Average proportion cover (d: SEM) for all species detected in each sample in
the mowed B treatment is presented here in this table (see Table 3.1 for details) .......... 33

Table 3.3 Average proportion cover (i SEM) for all species detected in each sample in
the unmowed treatment is presented here in this table (see Table 3.1 for details) ......... 34

Table 3.4 presents the 2005 parasitoid recoveries from sentinel pots placed in non-
cropped habitats adjacent to soybean fields. Presented are results from a regression of
number of plant species (Nm.g and Nmm) or number of plant families (F max) versus the log
abundance of parasitoids recovered from each treatment ...................................... 37

List of figures

Figure 2.1 Species occurrence across all field sites and sampling dates. Mean number of
parasitoids per sampling row are presented with their respective error bars. Mean values
for recovery of Aphidius ervi and Praon sp. are not reported; less than 5 individuals were
recovered collectively from all samples ......................................................... 16

Figure 2.2 The distribution of B. kelloggensis and L. testaceipes between field sites for
all sampling periods. Mean number of parasitoids per sampling row and their respective
error bars are presented for each of the four field sites ......................................... 17

Figure 2.3 The response of Binodoxys kelloggensis sp. and L. testaceipes to the three
treatments during the October sampling period ................................................. 18

Figure 2.4 The spatial distribution of Binodoxys kelloggensis sp. from crop edge. Rows
A and B are located at the interior and 10m into soybean respectively, rows D and E are
located 10m into and at the interior of the grass treatment, and row c is located at the field
boundary between the two habitat types. This figure shows the response for Binodoxys
kelloggensis sp. during the October sampling period. The spatial dynamics within the
mowed once treatment was statistically significant ............................................. 21

Figure 2.5 The spatial distribution of L. testaceipes from crop edge. Rows A and B are
located at the interior and 10m into soybean respectively, rows D and E are located 10m
into and at the interior of the grass treatment, and row 0 is located at the field boundary
between the two habitat types. This figure shows the response for L. testaceipes during
the October sampling period. The spatial dynamics within the never mowed treatment
were statistically significant ........................................................................ 25

Figure 3.1 illustrates the relationship between parasitoid species recovery on a log scale
(Log Total) and the average number of plant species in each of four samples in each
treatment (ngI- The three treatments presented are the mowed frequently treatment
(Mowed A), the mowed once treatment (Mowed B), and the unmowed treatment. The
results are grouped by species and treatment type. A regression line is calculated using
least squares estimation. The figure above includes the 0.9 confidence interval. Statistical
values for the regression are presented in Table 3.4 ............................................ 38

Figure 3.2 illustrates the relationship between parasitoid species recovery on a log scale
(Log Total) and the maximum number of plant species encountered (NM...) within each
treatment. The three treatments presented are the mowed frequently treatment (Mowed
A), the mowed once treatment (Mowed B), and the early successional/weedy treatment
(Unmowed). The results are grouped by species and treatment type. A regression line is
calculated using least squares estimation. The figure above includes the 0.9 confidence
interval. Statistical values for the regression are presented in Table 3.4 ..................... 39

xi

Figure 3.3 illustrates the relationship between parasitoid species recovery on a log scale
(Log Total) and the maximum number of plant families (Fm...) represented by the plant
species occurring in these treatments. The three treatments presented are the mowed
frequently treatment (Mowed A), the mowed once treatment (Mowed B), and the early
successional/weedy treatment (Unmowed). The results are grouped by species and
treatment type. A regression line is calculated using least squares estimation. The figure
above includes the 0.9 confidence interval. Statistical values for the regression are
presented in Table 3.4 .............................................................................. 40

xii

Key to symbols and abbreviations

ANOVA Analysis ofvariance

°C degrees Celsius

cm centimeters

d days

(if degrees of freedom

F F -distribution

NM Average number of plant species across repeated sampling

Nmm. Maximum number of plant species observed within a treatment

F mm- Maximum number of families represented by plant species within a

treatment.

xiii

Chapter 1
Soybean aphid (Aphis glycines) Biology and Associated Natural Enemies in North
America
Introduction

Agricultural production systems face a number of challenges from natural forces
that can severely limit productivity and crop yields. These forces can include inclement
weather, nutrient availability, and damage from insect pests and other organisms.
Damage to crops by arthropods can alter productivity through the transmission of plant
diseases or through direct feeding.

Arthropod pests have a significant impact on agricultural yields in the United
States. Every year, these pests cause an estimated 13% reduction in crop yields, resulting
in nearly $35 billion in losses (USBC 1998). Pimentel et al. (1993, 1997) estimated that
of all arthropod pests, 40% are considered introduced or invasive species, and cause
losses of up to $13.9 billion per year. Furthermore, Pimentel (2000) estimated the cost in
pesticides used to control these pests cost more than $1.2 billion annually.

The implementation of biological control practices can significantly reduce the
costs of controlling agricultural pest populations. These practices seek to utilize
populations of natural enemies of pests to restrict the growth rate of pest populations to
limit crop damage. There are three major strategies of biological control employed to
boost the ability of these natural enemies to attack certain pests. The first strategy is
importation (i.e. classical biological control), involving releases of natural enemy species
to control target pest species (Murdoch and Chesson 1985). A second related strategy is

species augmentation, releases of existent natural enemies into an environment to boost

the ability of those populations to control pest species. The third strategy is habitat
conservation, which is explored further in this thesis. By understanding the life history of
natural enemy species, we can manipulate habitats, cropped and non-cropped, to better
provide resources necessary for the survival and reproduction of beneficial species. The
idea is that by boosting populations of natural enemies near target pest species, we can
enhance their ability to control pest populations (Dyer and Landis 1996, 1997, Landis and
Marino 1998, Landis and Menalled 1998, Landis et al. 2000, Snyder and Ives 2001).

In the next two chapters, I will explore the interaction of parasitoids and their
environment in an effort to understand how we can boost the ability of these species to
regulate populations of soybean aphid in an agricultural landscape. I will explore (a) the
spatial response of parasitoids to soybean aphid within three types of non-cropped habitat
near soybean aphid (Chapter 2), and (b) the relationship between plant diversity found

within the non-cropped habitats and parasitoids of soybean aphids (Chapter 3).

Soybean Aphids — Aphis glycines Matsumura

The soybean aphid, Aphis glycines Matsumura, recently invaded the United States
into the Midwest. They were found infesting soybean crops in late 2000 in Wisconsin.
The aphid has since expanded its range to include 20 states, and now infests more than
80% of the soybean production region (Wedberg 2000, Ragsdale et al. 2004). Soybean
aphids have been shown to cause upwards of a 40% yield loss in soybean production
(DiFonzo and Hines 2002, Venette and Ragsdale 2004). This represents a significant loss

to an industry that is important to the United States economy.

The soybean aphid employs a typical heteroceous holocyclic life cycle, meaning
that it alternates between plant hosts with sexual reproduction occurring only during one
part of its life cycle. In the United States, Soybean aphids utilize soybeans, Glycines max
(L.), as the annual summer host, and buckthom, Rhammrs cathartica L, as the
predominant winter host. As soybeans begin to senesce, aphids experience a constraint in
resources and females give birth to male and winged aphid forms. These aphids migrate
to their overwintering Rhamnus hosts. Female aphids lay eggs at the base of the stems,
which hatch early in the spring producing a generation of female aphids. In early to mid
June, these female aphids colonize soybean plants where they will reproduce asexually,

giving rise to genetic duplicates of themselves (Ragsdale et al. 2004, Wu et al. 2004).

Parasitic Natural Enemies of Soybean Aphid

There is a broad range of parasitic natural enemies (parasitoids) known to utilize
soybean aphids. Some of these parasitoids are broadly recognized in the literature as
being important biological control agents for a variety of agricultural pests. In a review of
hymenopteran parasitoids of A. glycines, Kaiser et al. (2007) identifies at least seven
species of parasitoids (Braconidae and Aphelinidae): Lysiphlebus testaceipes (Cresson),
Aphidius colemani Viereck, Aphelimrs asychis (Walker), Binodoxys kelloggensis Pike,
Stary & Brewer, Aphelinus albipodus (Hayat & Fatima), Diaeretiella rapae (McIntosh),
and Praon sp. We identified one additional species from our field studies, Aphidius ervi
Haliday. This identification was confirmed by Dr. Keith Pike (Washington State

University), and A. givcines is a new host record for this species.

Many of these parasitoid species have been shown to be important in regulating
the populations of other agricultural pests. Lysiphlchus testaceipes has a host breadth of
at least 63 species of Aphis (Kaiser et al. 2007). It is known to be an important enemy in
the control of Russian wheat aphid (Diuraplzis noxia) and English grain aphid
(Rlzopalosiplmm par/i) (Brewer and Elliott 2004).

Binodmjvs kclluggensis is a newly described species ofBraconidae that was
discovered in the fall of 2004 from field samples collected at the Kellogg Biological
Research Station (KBS) LTER by the author and Dr. Takuj i Noma (Pike et al. 2007). The
species was recovered from sentinel soybean aphids on potted plants placed in various
non-cropped habitats (Pike et al. 2007). Although the life history of this parasitoid
species is largely unknown, it is theorized to attack related Aphis sp. in the various non-
cropped habitats from which it was recovered (Pike et al. 2007). Binodoxys kclloggensis
is closely related to a species of Binodmys in China that attacks soybean aphid (Heimpel
and Wu 2003, Heimpel et al. 2004), and is being considered for release in the US.

Aplzclinus albipodus is unique among the soybean aphid parasitoids in being
aphidophagous, meaning that A. albipodus is both parasitic and predaceous (i.e. they use
aphids both as a food resource and as hosts to parasitize) (Lester and Holtzer 2002,
Kaiser et al. 2007). The host breadth of A. albipodus includes 18 species of aphids, a
much more restricted breadth of aphid hosts than is seen with L. testaccipcs. Therefore,
by exploring the interaction of L. tcsraceipes, B. kelloggensis, and A. a/hipodus we can
better understand the interactions oflife history and host breadth in determining the role

non-cropped habitats play in enhancing the efficacy of biocontrol by natural enemies.

Fundamentals of Biological Control Applied to Soybean Aphid

While there are many demonstrations of biological control in the literature, we
focus here on its application to the control of agricultural pests. Society is looking
increasingly to biological control options to limit the effect of insect pest damage.
Biological control seeks to limit the damage by arthropod pests though the use of
predacious, parasitic, and pathogenic enemies (Murdoch et al. 1985, Murdoch and Briggs
1996). Furthermore, biological control seeks to boost populations of these enemies to
increase control of arthropod pests.

The successful application of biological control benefits from an understanding of
the interaction between predators and their prey. Additionally, understanding the
interactions of these predators with their environment is an important aid in considering
habitat manipulation techniques. An important component of this understanding is the
availability of resources necessary for the survival and persistence of the natural enemy
populations. Parasitoids are dependent on the availability of appropriate hosts, food
resources (e. g. nectar), appropriate microclimate, and refuge from disturbance
(environmental and anthropogenic). The spatial distribution of resources can strongly
enhance or detract from the ability of parasitoid populations to respond to and control
agricultural pests (Foster and Ruesink 1984, Landis and Marino 1998, Landis and

Menalled 1998, Siemann et al. 1998).

Spatial Response of Parasitoids to Aphis glycines
Many ecological studies have expressed the importance or positive relationship

between diversity, in terms of plant and herbivore species, in promoting persistence and

success of populations of natural enemies responding to agricultural pests (Price ct al.
1980, Powell 1986, Hunter and Price 1992, Tilman l994, Tilman and Downing l994,
Siemann et al. 1998).

The ability ofparasitoids to effectively respond to and regulate soybean aphid
populations may be influenced by the arrangement of landscape elements. I focus on the
arrangement of non-cropped habitats in relation to soybean fields. Non-cropped
vegetation adjacent to or near soybean fields provides important resources that may be
necessary for the persistence of parasitoid populations, and thus the control of soybean
aphids. Non-cropped habitats may provide a source of nectar by harboring flowering
forbs and a source of alternative hosts. These alternative hosts are thought to play a
particularly important role in the ability of parasitoids populations to persist especially
under circumstances when the primary host is not abundant on the landscape through out
the parasitoids life cycle. This is especially relevant to soybean aphid parasitoids since
the aphid is only abundant in the protected crop, soybean, for three to four months,
compelling natural enemies to be able to utilize a range of other resources to survive

(Rutledge et al. 2004, Wu et al. 2004).

Chapter Preview

In this thesis, I explore the broad question, “Does non—cropped habitat near
soybean fields affect the response of parasitoids to soybean aphid?” In Chapter 2, I
explore the spatial aspectsz, “Does the distance from crop edge alter the ability of
parasitoids to respond to soybean aphid invasion”. In Chapter 3, I explore the plant
diversity aspects, “Does increased habitat diversity, in terms of the number of plant
species encountered by parasitoids, benefit populations of these enemies?” From an
agricultural management viewpoint, I considered whether timing of a simple field border
management technique (mowing) and encouragement of plant diversity may enhance

response of parasitoids to soybean aphid.

Chapter 2
Does management of non-cropped habitat near soybean fields benefit (or create
spatial constraints to) the use of soybean aphid (Aphis glycines) by parasitoids?
Introduction

The soybean aphid, Aphis glvcines Matsumura, is a recent invader to the Midwest
region of the US, and threatens soybean production there, potentially affecting the
ecological integrity of a significant agroecosystern. The aphid was first discovered in the
United States in Wisconsin in 2000, and has since expanded its range to include 20 states
(Wedberg 2000). Soybean aphid originates from China where it feeds on soybeans.
Estimates suggest that 80% of the US. soybean production region is affected by the
soybean aphid, resulting in up to 40% yield losses (DiFonzo 2002, Venette and Ragsdale
2004).

A diverse group of natural enemies prey upon soybean aphids. The natural enemy
community varies from state to state, with a predator community comprised of at least 22
species (Rutledge et al. 2004). Surveys of soybean aphid natural enemies conducted in
Michigan in 2003 and 2004 detected eight (long-term presence in the region) aphid-
specialist parasitoids: Lysiphlebus testaceipes (C resson), Binodmys kelloggensis Pike,
Stary, and Brewer (Pike et al. 2007), Aplrelinus asvclris (Walker), Aphelinus albipodus
(Hayat & Fatima), Diaeretiella rapae (McIntosh), Aplzidius colemani Viereck, Aplzidius
crvi Haliday, and Praon sp. (Langley and Brewer 2004, Pike 2006, Kaiser et al. 2007).
These parasitoids were recovered within soybeans and adjacent vegetation of varying
types (early successional, grassland, and woodlots). They likely parasitize resident aphids

found in alfalfa, corn, wheat, and other grasses. Natural enemies can benefit from using a

range of herbivores to fulfill their needs, particularly at times when soybean aphid is not
abundant and soybean is not in cultivation. These alternative hosts/prey can occur in
neighboring cropped or non-cropped habitats and may regulate the response of natural
enemies to soybean aphid invasions.

The persistence of ecological services (c. g. pollination, pest suppression) provided
by beneficial insects depends on the continued stability of their communities. Largely,
communities are organized around the arrangement of landscape elements in space and
time. Understanding how these communities interact with each other and their
environment is particularly important when contrasting the influence of managed and
unmanaged systems in supporting species aggregations (Powell 1986). More specifically,
understanding how species interact to maintain ecosystem services in an agroecosystem
benefits from contrasting cropped and non-cropped habitats across the landscape.

Numerous ecological studies have suggested that parasitoid diversity, in terms of
species richness, is positively correlated with regulation of herbivores (Landis and
Marino 1998, Landis and Menalled 1998, Menalled et al. 1999, Snyder and Ives 2003).
Therefore, maintaining a large parasitoid community might serve to better regulate
population growth rates and subsequent impact of pests on agricultural crops.
Additionally, complex parasitoid communities show increased efficacy compared to less
diverse communities (Montoya et al. 2003).

Since the initial discovery of soybean aphid in the US, surveys of the parasitoid
community have identified a number of species that commonly use the aphid as a host;
yet most observations have shown parasitism to be very low (<1%) (Ragsdale et al. 2004,

Kaiser et al. 2007). Heimpel and Wu (2003) observed L. tesraceipes parasitism rates

exceeding 30% in Minnesota, USA in 2003, although this appears to be an isolated
occurrence. Previous studies have found lag times between the arrival of a new aphid
host and its widespread use by resident parasitoids in large-scale agricultural production
systems (Comell and Lawton, Powell et al. 1998, Brewer et al. 2001, Brewer and Elliott
2004). Although the soybean aphid parasitoids detected in the 2003 and 2004 surveys
(Kellogg Biological Research Station, Hickory Comers, Michigan, USA) (Langley and
Brewer 2004, Kaiser et al. 2007) have broad aphid host ranges (Mackauer and Finlayso.T
1967, Elliott et al. 1994, Elliott et al. 1999a, Elliott et al. 1999b), the habitat affinity of
those parasitoids may slow host range expansion onto new aphid species (Powell et al.
1998)

Here I relate the occurrence and abundance of soybean aphid parasitoids found in
non-cropped managed habitats adjacent to soybean fields (field borders) to those found in
soybean. An early abundance of natural enemies has been shown to significantly contain
aphid growth rates (Fox et al. 2005); thereforeti boosting populations of parasitoids near
agricultural fields can be beneficial if it leads to a more rapid response to pest invasions.

This study utilizes a field experiment in which I altered the treatment of non-
cropped borders adjacent to soybean fields. By understanding how parasitoids respond to
such habitats, we might better understand the conditions required for adaptation to the
invading pest species. I use the data from this study to answer the question, does the
management of adjacent non-cropped habitat using a simple agricultural practice
(mowing) alter the response of endemic parasitoids to the presence of soybean aphid?

This study has implications for the management of field boundaries, particularly those in

connection with soybean production, to encourage the response ofbeneficial natural

enemies to control soybean aphids.

Methods

Study System

Detailed reviews of the life history of Aphis glvcines have been published by
Rutledge et a1 (2004), Voegtlin et al. (2004), and Wu et al. (2004). Briefly, soybean
aphids are heteroceous holocyclic meaning that they have two annual hosts, Glycines max
(soybean), the summer host, and eramnus sp., the overwintering host. Soybean aphids
feed on soybeans from approximately June to October (DiFonzo and Hines 2002,
Ragsdale et al. 2004). As soybean plants begin to senesce in early autumn, apterous
young are produced, facilitating their migration to buckthom. Here the aphids overwinter
as eggs laid at the base of the branches. Reproduction during the summer months occurs
asexually with populations comprised entire of female aphids (Dixon 1998, Ragsdale et
al. 2004). As a result, parasitoids that attack soybean aphid must use habitat and
resources outside of soybean when the aphid or the soybean is not present or robust in

providing resources.

Study Site

This study explores the interactions of non-cropped vegetation and soybean
production lands at three sites across southern Michigan: (1) Kellogg Biological
Research Station (KBS) dairy farm, Hickory Comcrs, MI, USA (42" 24’ N, 85° 24’ W);

(2) Michigan State Horticulture Teaching and Research Center, East Lansing, MI, USA

11

(420 40’ N, 840 29’ W); and (3) Michigan State Entomology Research Farm, East
Lansing, MI, USA (42" 69’ N, 84° 50’ W). I contrasted three treatments varying in their
management intensity, as determined by frequency of mowing of field borders of
soybean fields: ( l) mowed frequently, field was mowed at least once every 2 weeks for
the duration of our study; (2) mowed seasonally, field was mowed at the beginning of our
study and left unmanaged for the remainder of the season; (3) unmowed, habitat left
unmanaged (i.e. not mowed) for more than one year prior to sampling. I sampled two
treatment replicates at the MSU Horticulture Teaching Farm, and one replicate at each of
the other two sites. Each of the four field sites were sampled four times in 2005 (June 20-
21, July 18—19, September 18-19, and October 13-14).

To better understand the role of non-cropped vegetation and parasitoid response, I
sampled for parasitoids in 5 rows along a transect from the interior of the soybean field,
10 m from the edge, edge of the field, 10 m into the non-cropped treatment, and the
interior of the adjacent non-cropped treatment For a detailed description of our sampling
methodology, see Kaiser et. al. (2007). Briefly, within each of these rows, we placed four
potted plants, infested with sentinel soybean aphids, along the length of the treatment and
left them in the field for 2 to 4 days. The potted plants were established by planting
fifteen soybean seeds (variety RT2985, Cropland Genetics, St. Paul, MN) into 15.2 cm
round pots filled with soil (Baccto High Porosity Professional Planting Mix). At exposure
to parasitoids in the field, they were brought back to the laboratory, covered with a fine
cloth mesh, and placed under grow lights (16:8 L:D sodium box lights) in the laboratory

for 7 days at 22°C. At the first sign of mummy

12

formation, 1 clipped plants and placed them in emergence canisters. The canisters were
constructed of heavy cardboard tubes with a funnel attached to one end and sealed at the
other. A vial was attached to the top of the canister to trap parasitoids emerging from
aphids.

After all emergent parasitoids had expired in the vial, they were removed, sorted,
and identified. I examined parasitoid specimens under a dissecting microscope and

identified using published keys and illustrations (Pike et al. 1997).

Statistical Analysis

Because of the wide range of parasitoids recovered, a standard

transformation, WG—5 , was used to normalize the distribution of residuals. I
explored the effects of field site, management style of the field border, and the spatial
distance from crop edge for each soybean-non—crop habitat treatment on the abundance of
recovered parasitoids, using the general linear model procedure in SAS (PROC GLM,
SAS INSTITUTE 2002). Each of the four sampling dates was analyzed independently
because the number of parasitoids detected at each date was assumed independent of all
other sampling dates.

Based on a priori expectations, I designed a series of four contrasts to explore the
effects of management style of the field border and sampling distance from crop edge. I
asked (1) whether there was a difference in parasitoids recovered from among the
different non—crop habitat treatments, (2) whether there was a significant difference in the
abundance of parasitoids in the “mowed frequently” treatment versus the ”mowed once”

and “never mowed” treatments. (3) whether distance from crop edge affected the

13

response of parasitoids in any treatment, and (4) whether parasitoids preferentially
attacked soybean aphids in soybean versus aphids on soybeans in the adjacent grass
habitat. Since these expectations were developed prior to the data analysis, they do
necessitate the use of a Tukey adjustment for multiple comparisons (or other similar
method). Mean values for each test were calculated (PROC MEANS, SAS Institute 2002)

and reported graphically (SIGMAPLOT v9).

Results
Site Effects

Seven species of parasitoids were detected attacking soybean aphid. The three
dominant parasitoids detected were Lysiphlehus testaceipes, Binodorvs kel/oggensis, and
A phelinus alhipodus. Other species detected were Ap/zelimrs asvchis, Aphidius colemam',
Ap/zidius ervi, and Praon sp., but at a much lower frequency (Fig. 2.1). The analysis
focused on the two dominant Brachonidae, L. resraccipes and B. kelloggensis, that were
recovered in all sampling dates and were abundant in October.

Field site was a significant factor for the October sampling period (when
parasitoids were most abundant) in predicting the response of L. testiceipes and B.
kelloggensis attacking sentinel soybean aphids on potted plants placed in non-cropped
habitats. Lysip/rlebus testaceipes showed a differential response to soybean aphid across
field sites, with an increased response to sentinel soybean aphids at KBS during the
October sampling period compared to the other sampling dates (F333 = 20.03; P < 0.0001)

(Fig. 2.2). Binodmys kcllriggensis responded similarly to sentinel soybean aphids at the

KBS site during the October sampling period (F333 = 26.41; P .< 0.0001), far exceeding
the numbers recovered at the other sites.

An analysis of samples across different sampling dates revealed a large difference
in the number of parasitoids recovered from each sample (data not presented). Most
notably, there was a dramatic increase in the total number of parasitoids detected during
October compared to other sampling dates.

Treatment (non-cropped management regime) was considered in the MANOVA
in concert with site location and spatial position of pots along the transect. When these
factors were taken into account together, treatment was not a statistically significant
factor for either L. teslaceipes or B. kel/oggensis in the October sample. (F2.173 = 0.14, P =

0.8670 and F1173 = 0.98, P = 0.3786 respectively) (Fig 2.3).

15

 

16

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Mean Parasitoids per Row
00

 

 

 

 

 

 

 

 

 

 

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Figure 2.1 Species occurrence across all field sites and sampling dates. Mean number of
parasitoids per sampling row are presented with their respective error bars. Mean values
for recovery of Aphidius ervi and Praon sp. are not reported; less than 5 individuals were
recovered collectively from all samples.

16

 

 

50

- B. kelloggensis
[:1 L. testaceipes

 

 

40-

 

30*

20‘

Mean Parasitoids per Row

 

 

 

 

 

 

 

Figure 2.2 The distribution of B. kelloggensis and L. testaceipes among field sites for all
sampling periods. Mean number of parasitoids per sampling row and their respective
error bars are presented for each of the four field sites.

17

 

 

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Frequently Seasonally Unmowed

Mowing Regime

Figure 2.3 The response of Binodoxys kelloggensis sp. and L. testaceipes to the three
treatments during the October sampling period

Spatial Constraint to Habitat Type

Overall, I found the distance from crop edge to be a significant factor (when
measured as a main effect) in explaining the distribution of parasitoids for B. kelloggensis
(Table 2.1). By exploring distance from crop edge using predetermined contrasts. I was
able to obtain greater resolution into potential effects. Binodoxys kelloggensis was
marginally influenced by distance in the seasonally mowed treatment when sampled in
July (FL 33 = 2.52; P = 0.1 1) (Fig. 2.4). Distance to crop edge was not influential for
Binodorvs kel/oggcnsis within any other treatment or sampling date. Lysiphlebus
testaceipcs was influenced by distance to crop edge within the seasonally mowed
treatment in September (Fl. 33 = 3.87; P = 0.05) and in the unmowed treatment in October
(Fl, 33 = 4.45; P = 0.0.04) (Fig. 2.5).

Finally I contrasted the preference of parasitoids for soybean aphids in either field
border or soybean habitats (combining the individual effects of each treatment to obtain
an overall estimate of the influence of distance to crop edge). This effect was significant

for L. Icstaceipes during the October sampling periods (Fl~ 33 = 7.49; P = 0.01) (Fig. 2.3).

19

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-10 m 0 m 10 m Interior
Soybean ——> Non-Cropped Habitat

Figure 2.4 The spatial distribution of Binodoxys kelloggensis from crop edge. This figure
shows the response for Binodoxjys kelloggensis during the October sampling period. The
spatial dynamics within the mowed once treatment was statistically significant.

21

250

 

 

 

 

 

 

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Figure 2.5 The spatial distribution of L. testaceipes from crop edge. This figure shows the
response for L. testaceipes during the October sampling period. The spatial dynamics
within the never mowed treatment were statistically significant. _

22

Discussion

Species identity plays a considerable role in determining the interaction of
parasitoids and soybean aphids within the non-cropped habitat treatments. Lysip/zlebus
testaceipes and B. kelloggensis were recovered in highest abundance during the October
sampling date. This was most likely affected by having harvested the soybeans prior to
placing pots in the field, resulting in increased detection of sentinel aphids on potted
soybean plants. Lysrphlebus testaceipes strongly discriminated between cropped and non-
cropped habitat types and favors hosts found in soybean (Fig. 2.3). However, B.
kelloggensis shows less habitat constraint, readily parasitizing hosts within non—cropped
and soybean fields. Although the significance of these responses varied with sampling
date and treatment, there is a general trend towards the outlined species differences,
particularly when the parasitoids were most abundant in October.

Non-cropped habitats had a species-specific effect on the response of parasitoids
to soybean aphid. Lysip/rlebus' testaccipes was more abundant in the soybean habitat than
in non-cropped habitats during the October sampling period (Fig = 8.05, P = 0.0051).
This trend was not true for B. kelloggensis individuals; when considering non-cropped
habitats versus soybean, there was no indication of preference during the October sample
(Fm = 0.02, P = 0.8789). This effect is likely driven by a combination of factors including
the availability of resources necessary for the persistence of parasitoid populations, as
well as refuge from disturbances commonly experienced in agricultural landscapes.

By mowing crop edges once a year to promote the growth of weedy flowering
plants, the response of parasitoids to soybean aphid may be enhanced. Chapter 3 takes a

closer look at the influence of plant diversity on parasitoid activity. I suggest that the

23

underlying reasons for the enhanced response seen with B. kelloggensis will likely
translate to other similar parasitoids to attacking crop pests in other systems; however, if
the primary goal is to promote the enhancement of crop specific parasitoids (e. g. L.

testaceipcs), the management of crop boarders will not have any impact on response.

24

Chapter 3
Parasitoid-Host Association Depends on the Diversity of the Background Plant
Community
Introduction

Numerous studies have explored the importance of plant community diversity in
enhancing the activity of natural enemies to control arthropod pests in agricultural
communities. Siemann et al (1998) found that arthropod species richness depended upon
the number of plant species in a given plot. Hunter and Price (1992) concluded that a
high diversity of herbivores may support a high diversity of parasites and other natural
enemies. This suggests that the vegetation diversity of a community may indirectly
contribute to increased diversity of natural enemy species. Furthermore, these diverse
plant communities likely provide additional resources that are important for parasitoid
survival, including nectar, refuge from disturbance, and a stable microclimate (Menalled
et al. 1999).

The soybean aphid, Aphis glycines Matsumura, is a recent invader of Midwest
soybean production, being first discovered in Wisconsin in late 2000 (Wedberg, Ragsdale
et al. 2004). Since this time, populations of the aphid have grown rapidly and spread to
nearly every state in the Midwest. Soybean aphids have been recorded to cause more than
a 40% reduction in soybean yields (DiFonzo and Hines 2002). A diverse complex of
natural enemies has been recorded attacking soybean aphids in agricultural fields
including at least 21 species of predators and 7 species of parasitic wasps (Langley and

Brewer 2004, Kaiser et al. 2007).

25

A number of factors have been theorized as being important in promoting
biocontrol of soybean aphid by parasitic wasps. Agricultural landscapes typically host a
diversity of plant communities in addition to agricultural crops. Non-cropped early
successional habitats may provide important resources necessary for the persistence of
natural enemies, particularly parasitoids. These resources include nectar, microclimate,
refuge from disturbance, and a range of alternative hosts (Price et al. 1980, Powell 1986,
Hawkins et al. 1993). These resources are theorized to play a particularly important role
in the biological control of soybean aphid, since the aphid is only present on its
agricultural summer host, soybean, in significant numbers for about three to four months
a year in the Midwestern United States (Dixon 1998, Rutledge et al. 2004). Here we
consider the link between vegetational diversity in non-cropped habitats adjacent to
soybean fields and the response of parasitoids to attack soybean aphids on sentinel plants

placed in these communities.

Methods
Study System: Soybean aphid
The soybean aphid, is a major pest to soybean production throughout the
Midwestern region of the United States. The aphid was first discovered in the United
States in 2000 in Wisconsin (Wedberg 2000). It has since expanded its range to include
more than 20 states throughout the region, representing more than 80% of the soybean
production region (Ragsdale et al. 2004). Soybean aphid feeding can result in a yield

reduction upwards of 40% (DiFonzo and Hines 2002).

26

A number of recent reviews of soybean aphid biology provide a detailed look at
the life history of the species (Rutledge et al. 2004, Voegtlin et al. 2004, Wu et al. 2004).
Briefly, soybean aphids are heteroceous holocyclic species meaning that they have
alternate between two hosts throughout the year and sexually reproduce only during part
of the species life cycle. Soybean aphids utilize two seasonal hosts, Glycines max
(soybean) during the summer months and Rhamnus sp. (buckthom) during the winter.
The hosts used by soybean aphid in the United States mirror those used by the aphid in its
native range in China (Takahashi et al. 1993).

The soybean aphid life cycle begins in the spring when nymphs hatch from the
overwintering eggs laid on the winter Rhamnus hosts. This first generation gives rise to a
second, entirely female, generation of aphids that remain on the Rhamnus host. These
females reproduce asexually giving rise to subsequent generations of female aphids. The
resulting generations are typically winged, facilitating their migration to their summer
soybean host. This migration occurs early to mid June throughout the Midwestern United
States. Once aphids establish themselves on the summer host and find conditions
acceptable they produce Wingless, apterous, progeny. As soybean plants begin to senesce
in early autumn, soybean aphids produce winged, alate, progeny whom migrate back to
buckthom where they reproduce sexually with newly produced male morphs and lay

overwintering eggs at the base of branches.

Study System: Parasitoid Community
We selected three species of parasitoids for inclusion in our analysis here. Two

Braconidae species, Lysiphlehus testaceipes and Binodoxys kelloggensis were selected

27

due to their contrasting abundance in cropped vs. non-cropped habitats (see Chapter 2).
Lysip/zlebus testaccipes is documented to attack aphids within a variety of cropping
systems, including bird cherry-oat aphid (Rhopalosiphmn padi L.) in corn and Russian
wheat aphid (Diuraphis noxia) in wheat fields (Brewer et al. 2005). In contrast, B.
kel/oggensis has only been detected within soybean fields and attacking soybean aphid
placed in non-cropped early successional communities near soybean fields (see Chapter
2).

Finally, we selected Aphelinus albipodus for inclusion in our analysis due to its
relatively high abundance compared with other species in the 2005 study (see Fig. 2.1),
and its contrasting life history traits. Aphelinus albipodus differs from other Braconidae
species in that is aphidophageous, meaning that it utilizes the aphids as a host to
parasitize as well as a food resource. We hypothesize that this difference in feeding

strategy will result in a reduced sensitivity to noncrop habitat resources.

Experimental Design

We conducted our study in a variety of early successional communities near
soybean fields in central Michigan, USA at the Michigan State University Horticulture
Teaching and Research Center (42" 40’ N, 84° 29’ W) and the Entomology Research
Farm, East Lansing, Michigan, USA (42° 69‘ N, 840 50’ W), and in Southwestern
Michigan at the Kellogg Biological Research Station (KBS), Hickory Comers, Michigan,
USA (42" 24’ N, 850 24’W). In 2005 we sampled three communities varying in their
management regime: mowed twice a month (Treatment: mowed frequently), mowed once

in the spring (Treatment: mowed seasonally), and a community that was undisturbed for

28

1 yr prior to our study (Treatment: Unmowed). Each treatment community was
represented once at KBS and the MSU Entomology Research Farm, and twice at the
MSU Horticulture Teaching and Research Center.

We sampled parasitoids in these communities by placing sentinel soybean aphids
on potted plants in the field. Briefly, soybean aphids were reared under laboratory
conditions (22°C, 16:8 L:D) and transferred to potted soybean plants. Potted soybean
plants were setup by placing fifteen seeds (variety RT2985, Cropland Genetics, St. Paul,
MN) into 15.2 cm round pots filled with soil (Baccto High Porosity Professional Planting
Mix). Infestation rates were determined to be approximately 1,300 aphids per pot. Aphids
were permitted to reproduce on these potted plants for 3 (I under ambient laboratory
conditions (22°C, 16:8 L:D sodium box lights) prior to being placed in the field. The
plants were transported to the field and placed within the various non-cropped
communities along a transect from the soybean-non-cropped margin to the interior of the
non-cropped community. Along this transect, plants were placed at the interior, 10 m
from the edge and at the edge of the community. At each position along the transect, four
pots were spaced equally along the width of the non-cropped community or soybean
field. The aphids on these plants were exposed to parasitoids for 3 d and returned to the
lab. The plants were covered with cloth mesh fastened to the pot with an elastic band
under ambient laboratory conditions. After 10-14 (I (or when mummies began to
develop), plants were clipped at the base below the cotyledon and put into emergence
canisters. The canisters were constructed of heavy cardboard tubes with a funnel attached
to one end and sealed at the other. A vial was attached to the top of the canister to trap

parasitoids emerging from aphids (see Kaiser et al. 2007). After all emergent parasitoids

29

had expired in the vial, they were removed, sorted, and identified. I examined parasitoid
specimens under a dissecting microscope and identified using published keys and
illustrations (Pike et al. 1997).

To measure diversity in each treatment plot, I counted the number of plant species
in a 0.5 m x 0.5 m quadrant and made visual estimates of the percent cover for each
species in that quadrant. This was repeated four times for each treatment replicate at each
of the four field locations. Additionally, I calculated the maximum number of species
represented as well as the number of plant families represented by these species within
each treatment. Plant identifications were made using Gleason and Cronquist (1991),
Edsall (1985), and Klimas (1974). Distribution was verified using Gleason and Cronquist

(1991) and biocolleetion data from the KBS LTER (2007).

Statistical Analysis

Along each row on the transect for each treatment and replicate, I used the sum of
parasitoids recovered from all pots as a measure of response to soybean aphid. To
measure the interaction between parasitoid recovery from sentinel soybean aphids and
diversity of plants in each treatment, I applied a regression model to the number of
parasitoids recovered from each treatment replicate versus NWg (the average number of
plant species recorded within each of four samples), NM,- (the total number of plant
species observed within each treatment), and F mm (the number of plant families
represented by species observed). I repeated this analysis for Aphelinus albipodus,

Binodmjvs kel/oggensis, and Litrsiplzlebus testaccipes.

30

 

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Results and Discussion

Plant identifications and relative proportion ground cover are presented in Tables
3.1 to 3.3. Across all sites and treatments, plant species in the families Poaceae and
Asteraceae tended to be most abundant. There was not a significant difference in the total
numbers of plant species observed across all four sites in each treatment, but significant
differences across management styles of the noncropped areas occurred at the site level.
For example, at KBS, there were 12 species of plants present in the mowed A treatment;
while there were only four species of plants at the Entomology Farm in the mowed A
treatment. For the mowed B treatment, there were 17 species of plants represented across
all sites. Horticulture East had the most number of plant species (1 1), while Horticulture
West and Entomology had the least (6). Finally, in the unmowed treatment there were 16
species of plants observed. Horticulture West had the most number of plant species (10),
while Entomology had the least number observed (5). There was a high degree of
variability in terms of the proportion ground cover for each species; therefore, the
regression analysis focused on plant species diversity.

Table 3.4 presents statistics for the regression plant diversity, in terms of average
number of plant species in each sample (NM), the maximum number of plant species in a
given treatment (NM), or the maximum number of plant families represented by the
species of plants in a given treatment (F mm). The regression analysis presented here
suggests there may be a species-dependent relationship between habitat diversity
(measured as the number of plant species) and the ability of parasitoids to respond to
soybean aphids placed in the non-cropped habitats. The strongest indication of a

relationship was seen in the regression of Lysiphlebus tes'raceipcs versus Nam in the

34

mowed A treatment (P = 0.053). The regression suggests there is a positive relationship
between habitat diversity and parasitoid abundance (Figure 3.1). There is no evidence for
a relationship between diversity and parasitoid abundance when I consider Nmm— by L.
testucezpes in any treatment (Figure 3.2). There is also evidence to suggest there is a
positive relationship between plant species diversity (when either ng or NM, are
considered) and parasitoid abundance for B. kelloggensis in the mowed B treatment (F =
3.184, P = 0.102 and F = 3.23, P = 0.1 respectively) (Fig. 3.1 and Fig. 3.2). There was no
discemable relationship found in the regression between habitat diversity and parasitoid

abundance for A. alhipodus (P-values > 0.25) (Table 3.4).

35

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SPECIES

 

 

 

 

 

 

 

 

 

 

 

 

 

Figure 3.1 The relationship between the log parasitoid species (Log Total) and the
average number of plant species in each of four samples in each treatment (N). The three

Aphelinus Binodoxys Lysiphlebus

PI I I I I jq L_I I I I f 1‘ _I I I I I "6

_ .. -_ .. 15
'—
_ 2 2 .. _ -4 8
Frequently . / 5 _ \/ ~ - _// «3 3
... n ‘ .. '—

_ / ‘ " .. .. ‘ " . /: ‘1

"1 1 .5 1 1 1 1'4 ”1 1 [‘0 _ '- n 1 1 L 1 1- o

g '- T j— l I _ 1., I I ‘— l '1 r-T l T I I '16
a '- - r- -1 1- -1 5 '—
u1 - . . , _ - .. .4 8
0 Seasonally » \/ ~ - .. 5 — a «3 3
z L ., _ )- J .. .. n n _ 2 g

g " ./ H - / - P " ‘1

2 _ n1 [1“ 1 1"”1 "Ii/ll 1 L 1"“ 1/1\1 1 1 0

__I I I I I I _I I I I I I_ _T I I I I I 6

._ .1 p .. .. .4 5
. f—
_/ ._ .,
Unmowed — - — ~ - .\_/ -3 5'
— / - 5 . . ~ ~ \ -2 g

- .. a . ” - - /:\ J1

21,. 1 1 1 1 1" L.1” “1 J 1 1 1‘ _ n 5| 1 1 1 1‘ 0

3 4 5 6 7 8 3 4 5 6 7 8 3 4 5 6 7 8
N N N

treatments presented were either mowed frequently, seasonally, or left unmowed. The
results are grouped by species and treatment type. A regression line is calculated using
least squares estimation. The figure above includes the 0.9 confidence interval. Statistical
values for the regression are presented in Table 3.4.

37

SPECIES

 

 

 

 

 

 

Aphelinus Binodoxys Lysiphlebus
_I I I I I_‘ _I I I I I4 _I I I I I_ 6
.. .1 .. T .. -l 5
,_
- - - a — " -4 8
Frequently ~ ~ - \/ - ~ . . « 3 '1
\/ .. _/ g
.. .4 .. / _ .. - 2 I?-
~ - l - _ .1
11/ /\ /
n i 1‘ . n r. . 1 . . 3 2 ‘1 . r 0
LL] -I I T I ‘ PI T I I _I I I I I...
2 J 6
o " ‘ ‘ ‘ ‘5 .—
Eé.’ - n .4 _ _ .- '/ .44 8
_ _ _ 1 " -l
g Seasonally \/ L .. f 1 3 3
E " / ~ 1- a 1- / 41 g
0 ..
2 b1 1 n F 1 1‘ "'1 1 14 T1 1 H1 1 1‘ 0
_I I I I Id l". I fifi _T I I I I4 6
_ J _ a _ a 5
. l—
. . . - - . . - 4 8
Unmowed ~ - - 1; . » \/ ‘3 3
L « - ‘”"" - ~ ”It ,. « 2 '4
/ \ I);
>— 1} _ l— fl\ .1 1. \ -1
l l n l l 1+ _1 ’1‘“ 1 I I4 bl in“ ‘ l J-i 0

 

 

 

 

 

 

 

0 51015200 51015200 5101520
MaxN MaxN MaxN

Figure 3.2 The relationship between log parasitoid species recovery (Log Total) and the
maximum number of plant species encountered (MAX N) within each treatment. The
three treatments were either mowed frequently, seasonally, or left unmowed. The results
are grouped by species and treatment type. A regression line is calculated using least
squares estimation. The figure above includes the 0.9 confidence interval. Statistical
values for the regression are presented in Table 3.4.

38

SPECIES
Aphelinus Binodoxys Lysiphlebus

I I I I I T I I I T I I I I I I I I I I

._ ul— —

 

q
.4
d

I

1

If

1

I

J; l

TVIOLOO'I

Frequently — \/ - _ \/ - t
/

l l
l I
l 1
I I
h
b
on: :::_'v :
l I

h
-
h-
1-

 

J_
.1
..
q
.1
-
d
..
..
..
ad
-I
.1-
.l
q
-l-
-I
q
.1
d
d

 

Seasonally

44

M‘-
.. / .11. _, dr

0
_1 1 1 1 l 1 1 1 L‘ 4/1\
I I

l

 

J 1 J 1
I

-ll—

 

r I

Unmowed ~ /
n\
F1 1 I 1 1 '4 *1 °\ 1 1 1 1‘ ‘1 i\1‘ 1 1 T
2 3 4 5 6 7 2 5 6 7 8 9 2 3 4 5 6 7
MaxF MaxF MaxF

-I
C
q-
.1
fl

MOWING REGIME
_ . >\\ ..
o—smwhmmo—chIoI-moao-smwemm
'IVlOiSO'I

"lVlOiSO‘I

 

 

 

 

 

 

-
b
-
-

 

ml-
OJ
m-
(D

Figure 3.3 The relationship between parasitoid species recovery on a log scale (Log
Total) and the maximum number of plant families (Max F) represented by the plant
species occurring in these treatments. The three treatments were either mowed frequently,
seasonally, or left unmowed. The results are grouped by species and treatment type. A
regression line is calculated using least squares estimation. The figure above includes the
0.9 confidence interval. Statistical values for the regression are presented in Table 3.4.

39

The observed relationships between plant species diversity and parasitoid
abundance are likely influenced strongly by the specific life history characteristics of
each particular species. Lysiphlebus testaceipes is an aphid specialist parasitoid with a
large host breadth. Kaiser et a1 (2007) reports the number of documented hosts to exceed
147 species. In field samples of parasitoids attacking soybean aphid in the Midwest, L.
testaceipes was the most abundant parasitoid recovered in soybean in 2004 and 2005
(Kaiser et al. 2007). Additionally, it was the most abundant parasitoid recovered in non-
cropped habitats sampled in 2005 (See Chapter 2). Related Lysiphlebus sp. are considered
the most significant (of 15 species) in limiting the population growth of soybean aphid in
China (Liu et al. 2004, Wu et al. 2004). Lysiphlebus testaceipes responds positively to
increasing plant diversity (Nam) in habitats adjacent to soybean field that are mowed
frequently (F = 4.5] l, P = 0.053). However, there was no statistically significant
relationship in the response of L. testaceipes to increasing plant diversity (Nam) in either
the mowed B or unmowed treatments (P = 0.907 and P: 0.645 respectively). This
suggests that L. testaceipes is partly responding to treatments based on their level of plant
diversity, but does not rely solely on this characteristic in its habitat selection.

Binodoxys kelloggensis is considered a close relative to Binodoxys spp.
documented attacking soybean aphid in Asia (Singh and Sinha 1982, Heimpel and Wu
2003, Heimpel et al. 2004). Although B. kelloggensis is native to the United States, we
believe its rapid adaptation to the presence of soybean aphid (as measured by its
willingness to attack A. glycines) in an unfavorable habitat suggests the species is capable
of searching out the aphid in the absence of other environmental cues. Binodoxvs

kelloggensis responded positively to increasing plant diversity (Na,g and Nmm.) in the

40

mowed B treatment (mowed once before the start of my experiment) (F = 3.184, P =
0.102 and F = 3.23, P = 0.1 respectively). This too suggests that B. kclloggcnsis responds
in part to plant diversity, but does not rely on it solely for habitat selection.

Aphelinus albipoa’us are aphidophageous parasitoids, meaning they rely on aphids
as a source of hosts and as a food resource (i.e. the adults are predaceous). As a result, A.
albipoa’us should theoretically be more willing to utilize a broad range aphid species not
only for their ability to serve as hosts to parasitize. This is confirmed by Kaiser et al.
(2007) in his review of the documented host breadth of the species, 18 aphid species
feeding on plants from 8 families. Aphelinus albipodus does not appear to respond to
plant diversity (in terms of NM, Nmax, or F mm.) under any of my three management
regimes (see Table 3.4). This suggests that plant diversity is not a critical characteristic
for A. albipoa’us in its habitat selection; but instead A. albipodus relies on a number of
other characteristics not taken into account with this study. Many of these other factors
may also drive the habitat selection of L. testaceipes and B. kelloggensis and should be
considered an important focus for future research endeavors.

In summary, the analysis in this paper suggests there is a relationship between
plant species diversity in non-cropped habitats and the abundance of parasitoids
responding to sentinel soybean aphids on potted plants placed in non-cropped habitats
adjacent to soybean. Encouraging plant diversity in habitats near soybean fields can
improve conditions whereby parasitoid species can access important resources. When
parasitoid-plant diversity associations were detected, these effects were positive and
species dependent. The strength of these associations varies by parasitoid species,

supporting the view that species-specific traits are relevant in habitat management. This

41

is especially useful to take into account when recommendations for the management of
agricultural landscapes to increase the occurrence of habitat types that will promote the
biological control of agricultural aphid pests, particularly when that control leads to

increased crop yields and reduced economic costs.

42

Chapter 4

Research Summary

The research outlined in this thesis was conducted with the explicit goal of
evaluating the role non-cropped vegetation near soybean fields plays in facilitating the
responsiveness of parasitoid natural enemies to soybean aphids. I measured the response
of these parasitoids by introducing soybean aphids on potted soybean plants on the
landscape where soybean and non-cropped habitats merge. The analysis presented in the
preceding chapters seeks to answer two questions: (1) “Does management of non-
cropped habitat near soybean fields benefit or constrain the use of soybean aphids by
parasitoids?”, and (2) “Does plant diversity affect the response of parasitoids to soybean
aphids?”

l explored the interaction of parasitoids and soybean aphids in three types of non-
cropped early successional habitat. Non-cropped habitats adjacent to soybean fields were
manipulated in one of three ways in terms of the frequency of mowing. Habitat
treatments were either mowed twice per month (Mowed Frequently), once at the
beginning of the study (Mowed Seasonally), or left undisturbed (Unmowed). Each
soybean-treatment pair was replicated at 3 locations across southern Michigan. I placed
soybean pots along a transect from inside the non—cropped habitat into the soybean field
in order to determine whether the distance from one habit into the other played a role in
directing parasitoid response to soybean aphids. In a separate analysis, I considered the
whether plant species diversity facilitated or deterred parasitism of soybean aphids on

potted soybean plants.

43

Justifications

Parasitoids are important natural enemies of agricultural pests in the United
States. These enemies have the potential to control pests below an economic threshold,
thereby reducing the need for additional chemical controls (Pimentel et al. 2000, 'DiFonzo
and Hines 2001); however, their success is dependent on a variety of environmental
factors. The spatial distribution of resources (e. g. nectar, microclimate, and host species)
can enhance or detract the ability of parasitoids to successfiilly limit the populations of
target pest species (Foster and Ruesink 1984, Landis and Menalled 1998, Siemann et al.
1998, Landis et al. 2000). The spatial arrangement of non-cropped habitats near soybean
fields may be particularly important in the ability of parasitoid natural enemies to respond
to soybean aphids. These habitats provide many of the resources critical for the survival
of parasitoids (Landis and Marino 1998).

Numerous ecological studies have established a positive relationship between
diversity, in terms of plant and herbivore species, and the persistence of natural enemies
(Price et al. 1980, Powell 1986, Hunter and Price 1992, Tilman l994, Tilman and
Downing 1994, Siemann et al. 1998). This lends support to the idea that promoting plant
and insect diversity on the landscape by utilizing non-cropped habitats may increase the

ability of parasitoids to respond to soybean aphids.

Linking the results from two studies
In this study, 1 analyzed the response of Lysiphlebus testaceipes, Binodoxys
kelloggensis, and Aphelinus albipodus to soybean aphids on potted soybean plants.

Lysiphlebus testaceipes and B. kclloggensis were selected primarily because their

44

presumed similarity as Braconidae allows me to evaluate the importance of life history
traits of an otherwise unknown parasitoid species, B. kel/aggensis. Additionally, by
including A. albipodus in my analysis, I am able to consider the interaction of diversity
and species life history.

Binodoxys kelloggensts shows no preference between soybean aphids on potted
plants when those plants were placed in either soybean or non-cropped habitat (F 1.2 =
0.02, P = 0.8; Figure 2.4). Furthermore, the distance of the potted plants from soybean
habitat does not alter the tendency of B. kelloggensis to parasitize soybean aphids on the
potted plants. In contrast, L. testaceipes was determined to favor soybeans on potted
plants when those plants were placed in soybean habitat over those in non-cropped
vegetation. Presumably, the observed importance of distance from soybean habitat is a by
product of an overall preference for soybean habitat.

Plant diversity did not appear to have a consistent relationship with parasitism of
soybean aphids when those aphids were placed in non-cropped habitat. Lysiphlebus
testaceipes responded positively to plant diversity in the treatment mowed frequently
(mowed every 2 weeks), but not the other treatments. Furthermore, B. kelloggensis and A.

albipodus did not appear to respond to increasing plant diversity.

Future direction of research

If indeed life history traits dictate the relationship between a parasitoid’s
environment and its propensity to attack soybean aphids in varying habitats, then there
are unknown differences between the life histories of B. kelloggensis and L. testaceipes

that need to be explored further. There are a number of plausible explanations for the

45

observed differences between the two parasitoid species. A broad host breadth may
permit a species to adapt to the presence of different host species. Alternatively, plant
volatiles, mobility and foraging capacity,abiotic conditions, scale of the arrangement and
pattern of vegetation elements, and other factors may be important in each species’
response to an introduced prey item, such as soybean aphid..

The underlying theory that increasing plant diversity should lead to increasing
persistence and activity of natural enemy species was consistent with the results, but not
in a compelling fashion (trend were consistent but not strong statistically). As noted,
other habitat characteristics may be affecting the relationship of plant diversity and
parasitoid abundance. As a newly described species, biological characteristics of
Binodoxys kclloggcnsis need to be investigated, including its host breadth, responsiveness

to environmental cues, and scale that it responds to environmental cues.

Implications for biological control

My study has important implications for biological control. Most notably, by
understanding the importance that non-cropped edge habitats play in facilitating a
response to agricultural pests by natural enemies, we can better manage landscapes to
promote the effectiveness of biological control. I have shown that by altering the
frequency of mowing of edge habitats to maintain early successional (weedy)
communities, we can create an environment that is suitable for parasitoids. If one can
increase the availability of these habitats, thereby boosting background parasitoid

population levels, we can assure a more efficient response to soybean aphids.

46

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.: 2006-07

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

The Role of non-cropped vegetation in facilitating the response of parasitoids to
soybean aphids (Aphis glycines)

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

Entomology Museum, Michigan State University (MSU)

Other Museums:

United States National Museum (USNM)
Washington State University — Prosser

Academy of Sciences, Czech Republic, Braniéovska

lnvestigator’s Name(s) (typed)
Shaun Arthur Langley

 

 

Date 06 April 2007

*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.

47

Pages

I

of

1

Appendix 1.]

 

Voucher Specimen Data
e

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48

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