BIOLOGICAL CONTROL OF CEREAL APHIDS IN MICHIGAN WHEAT
By
Shahlo Safarzoda

A THESIS
Submitted to
Michigan State University
in partial fulfillment of the requirements
for the degree of
Entomology - Master of Science
2014

ABSTRACT
BIOLOGICAL CONTROL OF CEREAL APHIDS IN MICHIGAN WHEAT
By
Shahlo Safarzoda
Cereal aphids (Hemiptera Aphididae) are important pests of wheat and can cause yield
loss through both direct feeding injury and indirectly by transmitting viruses. Previous work has
demonstrated that natural enemies are effective in suppressing cereal aphids in wheat fields in
Europe and North America; however, no studies have been done in Michigan. The objectives of
this thesis research were to characterize the natural enemy community in wheat fields and
evaluate the role of different natural enemy groups in regulating cereal aphid population growth.
I investigated these objectives in four winter wheat fields on the Michigan State University
campus farm in East Lansing, Michigan. I monitored and measured the impact of natural
enemies by experimentally excluding or allowing their access to wheat plants infested with
cereal aphids. I found that the natural enemy community in the wheat fields consisted mostly of
foliar-foraging and ground-dwelling predators with relatively few parasitiods. In combination,
these natural enemy groups were very effective at reducing cereal aphid population. I also
investigate the role of each natural enemy feeding guild (foliar-foraging versus ground-dwelling
predators) independently. The result illustrates that ground-dwelling predators were more
effective at suppressing cereal aphid populations than foliar-foraging predators in wheat fields.
Overall, my research demonstrates the importance of biological control in in wheat and suggests
that effective conservation of natural enemy communities can protect wheat from direct damaged
caused by cereal aphids.

ACKNOWLEDGEMENTS

I am sincerely grateful to Dr. Doug Landis for being an outstanding advisor and for
always providing me with opportunities to develop as a scientist. I would like to thank the
members of my graduate committee, Dr. Karim Maredia, Dr. Chris DiFonzo and Dr. Sieg Snap
for their support throughout the completion of this degree. Dr. Karim, I especially appreciate you
providing me the great opportunity to study at Michigan State University and for making me feel
like I am at home while at MSU. I am indebted to Anthony Boughton who allowed me to
conduct my research on the Michigan State University Farm. I am also thankful to Dr. Carolyn
Malmstrom for providing us with aphids from her colony. My graduate degree and research
would not have been possible without funding support from USAID, Central Asia IPM project
and the MSU Entomology Department.
Thank you to current and previous members of the Landis lab for support. I am especially
thankful to Dr. Aaron Fox and Dr. Christie Bahlai. Their guidance helped me write this thesis
and address statistical questions. I am thankful to Dr. Ben Werling for helping me get my first
field project running, and to Julia Perrone, Mitchell Lettow and Brendan Carson for improving
my English language, and for their friendship. Julia thanks for the “garlic mustard” song. I will
never forget it. I am also indebted to many undergrad research assistants, especially Erica Luu
and Katelyn Lewis, who gave daily assistance with field work, data entry, and sample
processing. Thank you so much to Heather Lenartson-Kluge, Linda Gallagher and the rest of the
Entomology Department office staff for always helping to keep my life running smoothly.
Most of all, I have the deepest thanks and appreciation for all members of my family,
present and passed. I love you all so much and this thesis is dedicated to you.
iii

TABLE OF CONTENTS

LIST OF TABLES ......................................................................................................................... vi
LIST OF FIGURES ...................................................................................................................... vii
CHAPTER 1 ...................................................................................................................................1
LITERATURE REVIEW ...............................................................................................................1
Cereal aphids .............................................................................................................................1
Bird cherry oat aphid Rhopalosiphum padi (L.) .......................................................................2
English grain aphid Sitobion avenae (F.) ..................................................................................3
Impacts of aphids ......................................................................................................................3
Aphids as disease vectors ..........................................................................................................4
Yellow dwarf viruses ................................................................................................................5
Control of aphids .......................................................................................................................6
The role of natural enemies in aphid control.............................................................................6
Predators ....................................................................................................................................9
Parasitoids ...............................................................................................................................10
Negative impact of natural enemies ........................................................................................11
Summary .................................................................................................................................12
CHAPTER 2 .................................................................................................................................13
BIOLOGICAL CONTROL OF CEREAL APHIDS ON WHEAT IN MICHIGAN ......................13
Abstract ..........................................................................................................................................13
Introduction ....................................................................................................................................14
Methods..........................................................................................................................................16
Study sites and experimental design .......................................................................................16
Natural enemy community sampling ......................................................................................21
Aphid population growth ........................................................................................................21
Statistical analyses...................................................................................................................22
Results ............................................................................................................................................23
Natural enemy community sampling ......................................................................................23
Aphid population growth ........................................................................................................25
Discussion ......................................................................................................................................25
CHAPTER 3 .................................................................................................................................30
RELATIVE ROLE OF GROUND-DWELLING AND FOLIAR-FORAGING PREDATORS
IN CONTROLLING CEREAL APHIDS IN MICHIGAN WHEAT ............................................30
Abstract ..........................................................................................................................................30
Introduction ....................................................................................................................................31
Methods..........................................................................................................................................34
Study sites ...............................................................................................................................34
Plot establishment ...................................................................................................................34
iv

Predator sampling ....................................................................................................................36
Aphid population growth ........................................................................................................36
Statistical analyses...................................................................................................................37
Results ............................................................................................................................................38
Predator sampling ....................................................................................................................38
Aphid population growth ........................................................................................................41
Discussion ......................................................................................................................................41
CHAPTER 4 .................................................................................................................................46
CONCLUSIONS AND FUTURE DIRECTIONS .........................................................................46
Biological control of cereal aphids on wheat in Michigan ............................................................46
Relative role of ground-dwelling and foliar-foraging predators in controlling cereal aphids .......47
APPENDIX ...................................................................................................................................49
REFERENCES .............................................................................................................................53

v

LIST OF TABLES

Table 1. Agronomic records from Michigan State University campus farm fields used for cereal
aphid and natural enemy studies, East Lansing 2012 and 2013 ....................................................19
Table 2. Mean numbers (± SEM) of natural enemies captured in pitfall traps, yellow sticky cards
and visually observed in four wheat fields in 2012 and 2013, Michigan State University campus
farm East Lansing, Michigan .........................................................................................................24
Table 3. Mean number (± SEM) of most abundant natural enemies captured in pitfall traps,
yellow sticky cards and by visual observation in wheat study sites in Michigan State University
campus, East Lansing, Michigan, 2013 .........................................................................................39

vi

LIST OF FIGURES

Figure 1. Winter wheat fields (shown in white) used as study sites in 2012 (field 1 and 2) and
2013 (field 3 and 4) Michigan State University campus, East Lansing, Michigan .......................17
Figure 2. Example of plot layout (field 2) in completely randomized design using three
treatments; open, closed and sham plots, conducted on the Michigan State University campus,
East Lansing, Michigan. The study area was 30m x 20m, with 5 m between the plots, and 35 m
from any of the field margins.........................................................................................................18
Figure 3. Photo illustrating natural enemy exclusion treatments used in our study A) closed plot
caged to exclude all natural enemies, B) open plot allowing access to all natural enemies and C)
sham plots, which are caged but, with holes on the ground and canopy levels to allow access by
natural enemies ..............................................................................................................................20
Figure 4. Mean cumulative aphid numbers (± SEM) per tiller of; a) Rhopalosiphum padi in
2012, b) R. padi in 2013, c) Sitobion avenae in 2012, d) S. avenae in 2013, among treatment in
closed, exclusion of all natural enemy, open exposed to all natural enemies, and sham to control
for cage effect. ANOVA was used to test statistical differences. Different letters above the
treatments indicate statistically significant differences among aphids
per tillers at α = 0.05 ......................................................................................................................26
Figure 5. Photo illustrating the natural enemy exclusion experiment in Michigan State
University campus wheat fields. Each plot was assigned a cage treatment to exclude different
groups of natural enemies from aphid populations. Treatments included exclusion of A) foliarforaging predators and parasitoids (-F), B) ground-dwelling predators (-G), C) and all natural
enemies (-F -G), and D) open plot (O), which allowed access to all natural enemies and served as
a control .........................................................................................................................................35
Figure 6. Abundance of Carabidae captured in pitfall traps in –G (excluding ground-dwelling
predators),-F-G (excluding all natural enemies), -F (excluding foliar-foraging predators) and O
plots (exposed to all natural enemies) in 2013...............................................................................40
Figure 7. Abundance of Coccinellidae captured in sticky cards in traps in –G (excluding grounddwelling predators),-F-G (excluding all natural enemies), -F (excluding foliar-foraging
predators) and O plots (exposed to all natural enemies) in 2013 ...................................................40
Figure 8. Mean number (± SEM) of R. padi among treatments; -F-G (excluding all natural
enemies), -G (excluding ground-dwelling predators), -F (excluding foliar-foraging predators) and
O (open plot, exposed to all natural enemies) in 2013. ANOVA with repeated measures was
used. For treatment comparisons pairwise t-tests that have been Holm-adjusted were used.
Different letters indicate statistically significant differences within treatments at α = 0.05 during
a sampling period ...........................................................................................................................42

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Figure 9. Mean number (± SEM) of S. avenae among treatments; -F-G (excluding all natural
enemies),-G (excluding ground-dwelling predators), -F (excluding foliar-foraging predators) and
O (open plot, exposed to all natural enemies) in 2013. ANOVA with repeated measures was
used. For treatment comparisons pairwise t-tests that have been Holm-adjusted were used.
Different letters indicate statistically significant differences within treatments at α = 0.05 during
a sampling period ...........................................................................................................................42
Figure 10. Mean number of R. padi (± SEM) alive, missing and dead in the petri dishes
containing Coccinellidae at 3, 6 and 21 hours ...............................................................................52
Figure 11. Mean number of R. padi (± SEM) alive, missing and dead on the petri dish with
Carabidae at 3, 6 and 21 hours ......................................................................................................52

viii

CHAPTER 1
LITERATURE REVIEW
Cereal aphids (Hemiptera Aphididae) are important pests of wheat (Triticum aestivum L.)
and other small grains in many parts of the world (Vickerman and Wratten 1979, Alsuhaibani
1996, Brewer and Elliott 2004, Haley et al. 2004, Li et al. 2013), causing yield loss through both
direct injury and indirect damage (van Emden and Harrington 2007). Many studies have shown
the importance of natural enemies in inhibiting aphid populations (Edwards et al. 1979,
Chambers and Adams 1986, Lang 2003, Brewer and Elliott 2004). Alternatively, natural enemies
have also failed to control aphids in other situations (Holland et al. 1996). In some cases it was
reported that the presence of parasitoids and predators increased virus spread, typically by
increasing aphid movement among plants (Roitberg and Myers 1978, Smyrnioudis et al. 2001).
This review examines the biology and impact of cereal aphids on crops, and the natural enemy
communities associated with cereal aphids.
Cereal Aphids
The bird cherry oat aphid Rhopalosiphum padi (L.), English grain aphid Sitobion avenae
(F.), greenbug Schizaphis graminum (Rondani), and the Russian wheat aphid Diuraphis noxia
(Mordvilko) are the most economically important pests of cereals in the United States (Pike and
Schaffner 1985, Kieckhefer and Kantack 1988, Kieckhefer and Gellner 1992, Pike et al. 1997,
Brewer and Elliott 2004). Most of these species transmit barley yellow dwarf virus (BYDV) and
cereal yellow dwarf viruses (CYDV) (Rochow 1960, Gray et al. 1998, Chapin et al. 2001, Hadi
et al. 2011). Chapin et al. (2001) observed seasonal flight activity, abundance, and vector
potential of cereal aphids in South Carolina. Four species attacked wheat in different seasons of
1

the year. Schizaphis graminum and rice root aphid, Rhopalosiphum rufiabdominalis (Sasaki)
colonized wheat seedlings soon after crop emergence and apterous colonies peaked in December
- January and decreased during the rest of the season. Rhopalosiphum padi was the second most
abundant aphid species and caused more economic loss than S. graminum and R.
rufiabdominalis. Rhopalosiphum padi populations peaked in February and March at 10 aphids
per row meter. Both BYDV and yield loss were significantly associated with R. padi aphid peak
density and aphid-day accumulations. These authors also showed that R. padi was primarily
responsible for transmitting the predominant virus stereotype PAV. Infective alates of R. padi
were collected from December until April. English grain aphid, S. avenae was the last and most
abundant species to infect wheat during all years of the study. It can transmit late season viruses
and also caused direct damage and yield loss, feeding on wheat heads and flag leaves
Bird cherry oat aphid Rhopalosiphum padi (L.)
Rhopalosiphum padi is dark olive green with a reddish-brown patch on the back. The
antenna and cornicles are black. It is holocyclic in northern North America and anholocyclic in
the mid-western and southeastern United States and is the most prominent vector of BYDV and
CYDV (van Emden and Harrington 2007). It feeds on bird cherry Prunus padus (L.) in Europe
and chokecherry Prunus virginiana (L.) in North America as its primary host, and usually infests
wheat as its secondary host, in early spring (Dixon 1971). Rhopalosiphum padi feeds on plant
phloem tissue from which it extracts plant sap (Riedell et al. 2003). The preferred feeding
location of R. padi is at the base of the stem and the lower leaves of cereal seedlings
(Chongrattanameteekul et al. 1991), and they frequently change position as the plants grow
(Qureshi and Michaud 2005). In autumn, gynoparae and males return to bird cherry which
provide the aphids with a rich source of food (Dixon 1971)
2

English grain aphid Sitobion avenae (F.)
Sitobion avenae adults are 2.5 mm long, light green to brown with black antennae,
cornicles, and joints. They overwinter as eggs, late instar nymphs, or adults in many species of
Poaceae (van Emden and Harrington 2007). The overwintering forms are all females, which in
the spring give birth to live young. These progeny mature into wingless females which produce
live offspring without mating. In early spring, the aphids feed on cereal grains. As these plants
mature and become less succulent, winged aphids develop and migrate to wild or cultivated
grasses, where they spend the summer. In the fall, after the winter cereal grain crops are planted,
the aphids return to these crops or volunteer cereals. Males appear during the fall or early winter
and mate with the females, which then lay eggs on the grains where they have been feeding.
Each female lays only about eight eggs. As many as 17 generations occur each year. The
preferred feeding location of S. avenae is the head (Chongrattanameteekul et al. 1991), with
colonies feeding upon the leaves before collecting on the heads among the ripening kernels.
When sufficiently large populations develop, their feeding shrivels the growing kernels. This
aphid species is also a known vector of the barley yellow dwarf virus in the United States.
Impacts of aphids
Infestation of cereals by aphids can result in considerable losses of grain, both in quality
and quantity (Dixon 1977). Cereal aphids cause direct damage through phloem feeding, and
indirect damage via production of honeydew (Vereijken 1979) or transmission of BYDV and
CYDV. The most significant damage occurs in the fall before wheat dormancy. Yield reduction
during the fall by direct feeding of R. padi without transmitting yellow dwarf viruses in winter
wheat can reach 20 to 70% (Cook and Veseth 199, Riedell et al. 1999).

3

Yield loss of wheat and rye caused by R. padi, S. graminum and S. avenae was studied by
Kieckhefer and Kantack (1988) by infecting caged plots at three different plant stages. At
harvest, higher yield loss was observed in plots where aphids fed on the seedling stage (2-3
leaves) in the fall; where an average of 25-30 aphids per plant resulted in a 50% reduction in
wheat yield. Less yield loss occurred when aphids fed during the spring in the boot stage. No
loss was observed when aphids fed on mature plants. The yield crop damage caused by S.
graminum and R. padi, were more than the damage was caused by S. avenae.
Indirect damage by aphids can be due to their production of honeydew, which can cover a
plant's epidermis reducing photosynthesis, promoting senescence, and contributing to the growth
of saprophytic fungi which may also have a negative effect on photosynthesis and leaf duration
(Vereijken 1979, Rabbinge et al. 1981). Vereijken (1979) found that in 3 field tests with S.
avenae, about half the damage caused was attributable to fungal growth on the honeydew
produced by the aphid. It has been shown that in laboratory studies honeydew can cause
approximately 25% yield loss (Rabbinge et al. 1981)
Aphids as disease vectors
Many cereal aphids are also vectors of the yellow dwarf virus, family Luteoviridae (Ajayi
and Dewar 1983, Fereres et al. 1988, Royer et al. 2005). In North America R. padi, S. graminum,
S. avenae, corn leaf aphid Rhopalosiphum maidis (Fitch), and R. rufiabdominale have all been
reported as vectors of yellow dwarf viruses (Irwin and Thresh 1988, Gray et al. 1998, Chapin et
al. 2001). Rhopalosiphum rufiabdominale, R. padi and S. graminum and S. avenae were also
found in wheat in Alabama, Florida and Missouri transmitting yellow dwarf viruses (Hadi et al.
2011, Hadi et al. 2012),

4

Yellow dwarf viruses
Yellow dwarf viruses cause serious disease of wheat worldwide (Plumb and Thresh
1983). Yellow dwarf pathogens include barley yellow dwarf virus (BYDV) and cereal yellow
dwarf virus (CYDV) both of which belong to family Luteoviridae. There are serotypes of BYDV
belonging to the genus Luteovirus, including PAV, RMV, and SGV (Gray et al. 1998). One
species of cereal yellow dwarf virus, cereal yellow dwarf virus-RPV belongs to genus
Polerovirus (Hadi et al. 2011). Symptoms of BYDV include leaf necrosis and discoloration,
stunting, delay or lack of heading (Riedell et al. 1999). Yellow dwarf viruses cause damage to
more than 150 species of grasses (Poaceae) including all small grains. In North America, yield
loss due to the disease on grains can reach up to 60% -70% (Miller and Rasochova 1997, Riedell
et al. 2003, Jimenez-Martinez and Bosque-Perez 2004). These viruses are obligately vectored by
25 aphid species (Miller and Rasochova 1997, Hadi et al. 2012). Unlike direct injury from aphid
feeding where plants can recover after aphids are removed, cereal plants infected with BYDV do
not recover from infection. Viral infection in wheat also increases host susceptibility to fungal
pathogens, drought, and other environmental factors (Irwin and Thresh 1988, Riedell et al.
2007). Epidemics of virus in winter wheat have been observed mostly in the fall and are
primarily due to R. padi activity in North America (Pike and Schaffner 1985, Pike et al. 1997).
Root characters, shoot characters and wheat yield show responses to infection of BYDV
transmitted by R. padi at 2 to 3 leaf stage. Compared to controls, treatment of 2-3 leaf stage
wheat with only R. padi had increased total root length of about 30%, while treatments with R.
padi plus BYDV exhibited a 40% decrease in total root length. Plants infected with R. padi alone
had fewer and shorter tillers, and lower shoot dry weight at anthesis compared to plants that were
not infected with R. padi. Plants infected with BYDV and the combination of the R. padi plus
5

BYDV reached anthesis at later time than the treatments with R. padi and control treatment
(Riedell et al. 2003).
Control of aphids
Chemical, cultural, and biological methods have been used to control aphids and the
spread of viruses in cereals. Insecticides can be effective but are costly to purchase and apply.
Also, repeated use of insecticides can result in development of insecticide resistance, cause
negative impacts on beneficial insects, and increase aphid movement from plant to plant,
resulting in increased virus spread (Irwin and Thresh 1990, Shufran et al. 1997). Host-plant
resistance to aphids is promising but must constantly address the emergence of new aphid
biotypes with the ability to survive on previously resistant plant lines (Roberts and Foster 1983,
Formusoh et al. 1992). Smith et al. (2004) showed that the variety “Treasure” and five other new
varieties from Iran and the former Soviet Union were resistant to D. noxia. Leaf pubescence of
wheat also provides a possible mechanism of resistance to aphids (Roberts and Foster 1983).
Biological control of cereal aphids by natural enemies (parasitoids and predators) can be an
alternative control (Symondson et al. 2002, Brewer and Elliott 2004).
The role of natural enemies in aphid control
Globally, cereal aphids are attacked by variety of natural enemies (Puterka et al. 1993,
Van Emden and Harrington 2007). Cereal crops in North America attract several groups of aphid
natural enemies including ladybeetles (Coccinellidae), adult and larva lacewings (Chrysopidae),
hoverflies larva(Syrphidae), parasitoid wasps (Hymenoptera, Aphidiidae), carabids (Carabidae),
rove beetles (Staphylinidae), and spiders (Araneae) (Mohamed et al. 2000, Chapin et al. 2001,
Brewer and Elliott 2004, Lee et al. 2005). Predators and parasitoids acting either independently
6

or together can reduce aphid population density (Kring et al. 1985, Losey and Denno 1999,
Schmidt et al. 2004, Macfadyen et al. 2009), thereby reducing plant damage and increasing yield
(Östman et al. 2003).
Classical biological control, the importation and release of novel natural enemies, was
conducted against D. noxia, resulting in 29 species of exotic predators and parasitoids being
released in the United States (Hopper et al. 1998, Mohamed et al. 2000). However, only four
hymenopteran parasitoids were recovered (Prokrym et al. 1998). Mohamed et. al. (2000)
conducted a survey to identify parasitoids and predators of D. noxia in organic wheat, barley and
crested wheatgrass (Agropyron cristatum L.), and to determine the impact of weeds on aphids
and their natural enemies. These authors also used cage exclusion methods to understand the
impact of parasitoids and predators on D. noxia. Crested wheatgrass had fewer D. noxia and
natural enemies than wheat and barley. During this study they observed 41 species of predators
and parasitoids including: 15 carabids, 12 coccinellids, 6 spiders, 5 syrphids, 2 nabids, and 2
chrysopid species. The most abundant were coccinellids and nabids, with Hippodamia
convergens and Nabis alternatus the most common species. In this experiment, only one species
of parasitoid, Diaeretiella rapae (Hymenoptera: Braconidae) was found. In an exclusion cage
study, aphid populations were 2.6 to 11.2 times higher in the caged, than in the open plots.
Excluding natural enemies from aphid colonies demonstrates how important natural
enemies are in biological control. Schmidt et al. (2003) studied cereal aphid biological control in
Europe by reducing populations of ground-dwelling predators (spider, carabids, and staphylinids
beetles), flying predators and parasitoids, and combinations of both ground-dwelling and flying
natural enemies. Compared with open fields where access of parasitoids and predators was not
restricted, aphid populations were 18% higher with reduced densities of ground-dwelling
7

generalist predators, 70% higher in cages where flying parasitoids and predators were excluded,
and 172% higher when both natural enemies were excluded. Similarly, work by Thies et al.
(2011) in six European regions showed that aphid populations were 28% higher in plots
excluding ground-dwelling predators, 97% higher in plots that excluded both flying natural
enemies, and 199% higher when both enemy groups were excluded. These European results
show that both communities of parasitoids and predators are important in controlling cereal
aphids, but the effect of flying parasitoids and predators was generally stronger than grounddwelling predators, while the combination of the two showed the best result on pest suppression.
Coexistence of different aphid species may have a positive impact on biological control.
For example, Formusoh and Wilde (1993) showed that Coccinella septempunclata (L.) and
Hippodamia convergens (Guerin-Meneville) did not show a preference between S. graminum
and D. noxia. The lack of preference implies the predator feeds on whichever prey species is in
abundance and easily accessible. Therefore, in agroecosystems where both aphid species coexist,
Coccinellidae will prey on more easily accessible S. graminum. The development of resistant
wheat cultivars with minimum leaf curl could allow for the compatibility of biological control
with host plant resistance. Bergeson and Messina (1998) studied direct and indirect impact of R.
padi on increase of D. noxia populations. They found that the presence of the green lacewing
Chrysoperla plorabunda significantly reduced D. noxia populations, and the rolled leaves that D.
noxia cause did not prevent lacewing predation. However, C. plorabunda was less effective in
the experiment where both aphids were present. This might be because R. padi is more
accessible to predators than D. noxia.

8

Predators
Predators are frequently most effective in the early season when aphid populations are
relatively low (Chiverton 1986, 1987, Lang 2003), but can also control population peaks, even in
the presence of alternative prey (Winder 1990). For example von Berg et al. (2009) found that
even with the presence of alternative prey (i.e. thrips, springtails, mites), flying and grounddwelling predators suppressed aphid populations below threshold levels, by switching from
alternative prey to aphids.
Aphidophagus Coccinellidae are often the dominant natural enemy in cereal fields and
other agroecosystems in North America (LaMana and Miller 1996, Obrycki and Kring 1998,
Elliott and Kieckhefer 2000, Wright and DeVries 2000, Clement et al. 2004). Coccinellidae
overwinter as adults (Colunga-Garcia and Gage 1998) and co-occur with R. padi and other cereal
aphids in the spring (Phoofolo et al. 2007). Adult Coccinellids can consume up to 100 aphids per
day (Xue et al. 2009, Hallett et al. 2013) and dramatically reduce aphid numbers in dense patches
as well as when aphid populations are low in wheat fields (Elliott and Kieckhefer 2000). Many
Coccinellids are effective biological control agents of cereal aphids (Rice and Wilde 1988).
Phoofolo et al. (2007) showed that Hippodamia convergens preyed on R. padi and S. graminum.
H. convergens and Coccinella septempunctata are primarily predaceous on aphids, while
Coleomegilla maculata feeds on a variety of plant and other alternative prey in additional to
aphids (Hodek and Honek 1996).
Ground-dwelling predators can also be effective in aphid suppression, and their impact is
thought to be the greatest early in the growing season (Sunderland and Vickerman 1980, Dennis
and Wratten 1991, Lang 2003). Among the ground-dwelling predators, Carabidae probably

9

contribute the most to aphid suppression in cereals. These polyphagous predators often colonize
cereal fields from neighboring habitats (French and Elliott 1999), and are known to consume R.
padi, S. avenae and other aphids species (Edwards et al. 1979, Chiverton 1986). The greatest
impact on aphid populations occurs in early summer (May) when aphid populations are low and
reproduction is slower than in summer. However, Carabidae can continue to impact aphid
densities until aphid populations peak (Winder 1990, Winder et al. 1994). They can reduce aphid
density by preying on aphids directly when the aphids drop from plant (Duffield et al. 1996,
Symondson et al. 2002), or by climbing the plant. In a study examining the relative importance
of ground-dwelling predators on aphid populations, Lang (2003) manipulated populations of
ground beetles and spiders. Excluding ground beetle resulted in an increase in spiders that was
not associated with a reduction in aphid density, and aphid populations were highest in the plots
where Carabidae were removed. Although cereal aphids are considered low quality food for
ground-dwelling predators (Toft 2005), several other studies suggest that ground beetles
regularly consume cereal aphids. Sunderland and Vickerman (1980) dissected the gut of 12,000
individual ground-dwelling predators, collected from winter wheat and barley fields in
Washington. They found that sixteen species of Carabidae, 3 species of Staphylinidae and 1
species of Dermaptera all had aphids in their diet.
Parasitoids
Feng et al. (1991) reported that the parasitoid Aphidius ervi attacked S. avenae,
Diaeretiella rapae, and Aphelinus varipes attacked D. noxia and R. padi. Pike et al. (1997)
documented species abundance, geographic distribution, and seasonal occurrence of the primary
parasitoids of cereal aphids in eastern Washington. They found thirteen species of primary
parasitoids including, Aphelinus albipodus, Aphelinus asychis, Aphidius naphis, Aphidius ervi,
10

Aphidius matricariae, D. rapae, Ephedrus sp, Lysiphlebus testaceipe, Monoctonus
washingtonensis, Praon unicum, Praon occidentale, and Praon yakimanum. The dominant
parasitoids were D. rapae on Russian wheat aphid, L. testaceipes on bird cherry-oat aphid, and
A. naphis, A. ervi, and D. rapae on English grain aphid. Lysiphlebus testaceipes is also an
important parasitoid of cereal aphids in the US Southern Plains (Jones et al. 2005, Jones et al
2007), where it is followed in importance by D. rapae (Giles et al. 2003).
Negative impact of natural enemies
Although the positive impact of natural enemies on control of cereal aphid can be great,
some studies also report negative impacts of predators and parasitoids in wheat. For example,
parasitoids and predators may increase the spread of viruses by increasing aphid movement and
dispersal (Roitberg and Myers, 1978). Aphids have defensive strategies to avoid and escape from
natural enemies by walking or drop off the plant or kicking predators when the predator comes
close (Dixon, 1958). McConnell and Kring (1990) observed that the adults and nymphs of S.
graminum were dislodged 4-5 times more often than they were consumed by parasitoids. In
addition, parasitized aphids remain alive for a few days and if viruliferous, may transmit a virus
to other plants. To study the impact of a predator, C. septempunctata, and a parasitoid, Aphidius
rhopalosiphi, on the spread of BYDV by R. padi, Smyrnioudis (2001) conducted a laboratory
experiment. Viruliferous R. padi were caged with the parasitoid or predator in wheat seedlings
and virus infections were observed after two, seven and fourteen days. In plots without A.
rhopalosiphi, BYDV infestation was greater at 7, 14 days versus plots where A. rhopalosiphi
was present. In plots with the predator, aphids frequently moved between plants and more plants
were infected with BYDV than in the control. After 14 days all plants were infected in plots with
the predator.
11

Summary
Cereal aphids are one of the principal pests of the wheat throughout the world and can cause
economic yield loss by feeding on the plant, producing honeydew or by transmitting yellow
dwarf viruses (Karsten et al. 2009). Naturally occurring enemies that prey on the cereal aphids
can reduce their populations, thereby increasing yield, and reducing the need for chemical
control. The impact of the natural enemy groups on cereal aphid populations, in combination or
alone, is well studied in Europe and parts of North America but to our knowledge biological
control of cereal aphids has not been studied in Michigan wheat. The purposes of this thesis are:
1) quantify the natural enemy community in selected Michigan wheat fields, 2) examine the
impact of natural enemy community on cereal aphid population growth, and 3) compare the
relative contributions of different groups of natural enemies, specifically foliar-foraging versus
ground-dwelling predators.

12

CHAPTER 2
BIOLOGICAL CONTROL OF CEREAL APHIDS ON WHEAT IN MICHIGAN
Abstract
Natural enemies provide important ecosystem services by suppressing populations of
insect pests in many agricultural crops. However, the role of natural enemies against cereal
aphids in Michigan winter wheat (Triticum aestivum L.) is largely unknown. We characterized
the natural enemy community in wheat fields and evaluated their role in controlling cereal aphid
populations, using exclusion cage studies during the spring and summer of 2012 and 2013. The
natural enemy community impacting populations of Rhopalosiphum padi (L.) and Sitobion
avenae (F.) (Hemiptera: Aphididae) were monitored in 1) open plots presenting no barriers to
natural enemies, 2) closed cages excluding all natural enemies, and 3) sham cages with holes to
allow access by the natural enemy community. Our result showed that populations of R. padi
were dramatically higher in natural enemy exclusion plots. The closed plots in our study had a
maximum 57 times higher cumulative aphid-days than the open and sham plots. The maximum
number of R. padi and S. avenae in the closed plots exceeded economic injury levels reaching 38
and 29 per tiller respectively. In contrast, the maximum numbers of cereal aphids in the open and
sham plots were below economic injury levels and did not exceed 3 aphids per tiller. Since the
numbers of cereal aphids in the sham cages were no different from the open cages, we concluded
that any microclimatic effects caused by the cages were insignificant. Our results suggest that the
existing natural enemy community is successfully in suppressing cereal aphid populations in
Michigan winter wheat, and should be actively conserved.
Keywords: Biological control, natural enemy, cereal aphid, Rhopalosiphum padi, Sitobion
avenae
13

Introduction
Common wheat, Triticum aestivum (L.) and related species are among the world’s staple
food crops. Worldwide, about 670 million tons of wheat are grown on 225 million ha of land
annually (Singh et al. 2008). During the 2012 - 2013 growing season, the United States produced
62 million tons of wheat, mostly in the Great Plains and Northwest regions of the country
(USDA-ERS, 2013). However, Michigan is also a major wheat growing state, producing
approximately 1.5 million tons annually, ranking number 13th in production among the 46 wheat
producing states (USDA National Agricultural Statistic Service, 2012).
Cereal aphids (Hemiptera: Aphididae) are the principal pests of wheat throughout the
world. In North America, the aphid pest complex on wheat primarily consists of four aphid
species, the bird cherry-oat aphid (Rhopalosiphum padi L.), English grain aphid (Sitobion avenae
F.), greenbug (Schizaphis graminum Rondani), and Russian wheat aphid (Diuraphis noxia
Mordvilko). These aphids cause economic damage by feeding directly on the plants and
indirectly transmitting barley yellow dwarf viruses (BYDV) (Vickerman and Wratten 1979,
Kieckhefer and Kantack 1988, Kieckhefer and Gellner 1992, Elliott et al. 1998, Chapin et al.
2001, van Emden and Harrington 2007). Additionally, greenbug and Russian wheat aphids inject
a toxin into the leaves via their saliva, causing additional yield reductions (Duveiller et al. 2007).
Previous work showed that a mean density of 25-30 aphids per stem can cause up to 50%
reduction in some yield component (Kieckhefer and Kantack 1988). When aphids transmit plant
viruses, damage can be even greater. For example, yield loss due to BYDV alone can reach up to
60% -70% (Cook and Veseth 1991).
Both chemical and biological methods have been used to manage aphids and reduce the
spread of viruses in cereals. while effective in aphid control, intensive use of insecticides can
14

lead to increased production costs associated with insecticide purchase, handling, and application
(Webster et al. 1995, Meehan et al. 2011), development of insecticide resistance, and increased
aphid movement from plant to plant increasing virus spread (Teetes et al. 1975, Irwin and Thresh
1988, Shufran et al. 1996), and negative effects on human health and the environment
(Flickinger et al. 1991). Insecticides can also reduce the abundance and diversity of predatory
insects that regulate aphid populations (Brown et al. 1983, Basedow et al. 1985, Wiles and
Jepson 1992, Banken and Stark 1998, Geiger et al. 2010). Fostering biological control organisms
in an early season crop like winter wheat may have important implications for biocontrol in later
season crops like corn and soybean, as mobile natural enemies may move to adjacent crops after
early season crops are harvested (Sivakoff et al. 2012).
Biological control of pests by natural enemy communities is an important ecosystem
service (Östman et al. 2001, Losey and Vaughan 2006, Swinton et al. 2006). Naturally occurring
enemies that prey on aphids can prevent populations from multiplying beyond economic
thresholds and prevent yield loss (Edwards et al.1979, Chiverton 1986, Larsson 2005, Bianchi et
al., 2006, Karsten et al., 2009), thereby reducing the need for insecticide use. Reducing chemical
inputs can in turn increase populations of beneficial insects. For example, in an organic wheat
field, the abundance of natural enemies and aphid control were higher than in a conventional
field (Krauss et al. 2011). Östman et al. (2001) showed that R. padi establishment was lower in
organic compared to conventional fields which could be a result of higher numbers of natural
enemies. Numerous studies have used exclusion cages to measure the effect of natural enemies
on aphid populations. In one European study, cereal aphid populations were 172% higher on
wheat plants when natural enemies were excluded (Schmidt et al. 2003). Another study
conducted in wheat also showed that cereal aphid numbers were 12 times higher when predators
15

were excluded (Hopper et al. 1994).
The complex of aphid natural enemies in cereal crops has been described for Europe
(Thies et al. 2011), Germany (Schmidt et al. 2003) and the United Kingdom (Chambers et al.
1986, Winder et al. 1994). In North America the natural enemy community of cereal aphids was
reviewed (Brewer and Elliott 2004) and studied in South Dakota (Elliott et al. 1998), eastern
Washington (Pike and Schaffner 1985, Clement et al. 2004), and Colorado (Mohamed et al.
2000, Lee et al. 2005) but, to our knowledge, has not been described in Michigan or the
Midwest. To investigate the role of natural enemies in controlling cereal aphid populations in
East Lansing, Michigan wheat fields, we conducted exclusion cage field studies in 2012 and
2013. The overall goal of this research was 1) to characterize the natural enemy community, and
2) determine its effect on aphid population growth in Michigan winter wheat fields.
Methods
Study sites and experimental design
Experiments were conducted in four different winter wheat fields in 2012 (2 fields) and 2013 (2
fields) on the Michigan State University campus, East Lansing, Michigan (Figure 1). The fields
were planted in October of 2011 and 2012. Each field received herbicide, fungicide and
fertilizers at rates determined by the farm manager (Table 1). No insecticides were applied in the
fields in either year. In each field, a 30 x 20 m area was delineated at least 35 m from the field
edge. Individual plots within this area were established 5 m equidistant from each other in a
completely randomized design (Figure 2). Treatments included open plots, which provided
unrestricted access of natural enemies to aphids, closed plots which excluded all natural enemies,
and sham cages to control for cage effects. Open plots consisted of circular area of 0.36 m,

16

N
0

500 m

Figure 1. Winter wheat fields (shown in white) used as study sites in 2012 (field 1 and 2) and
2013 (field 3 and 4) Michigan State University campus, East Lansing, Michigan.

17

20m
35 m

30 m

Open
Closed
Sham

Figure 2. Example of plot layout (field 2) in completely randomized design using three
treatments; open, closed and sham plots, conducted on the Michigan State University campus,
East Lansing, Michigan. The study area was 30m x 20m, with 5 m between the plots, and 35 m
from any of the field margins.

18

Table 1. Agronomic records from Michigan State University campus farm fields used for cereal aphid and natural enemy studies, East
Lansing 2012 and 2013.
Studies sites

Year

Area / ha

Cultivar

Seeding

Fungicide mg / ha

Herbicide

Field 1
2012
8.7
Unknown 10/5/2011
94.6
Affinity Broadspec*
Field 2
2012
18.5
Unknown 10/18/2011
94.6
Affinity Broadspec
Field 3
2013
12.1
Red Devil 10/4/2012
0
Affinity Broadspec
Field 4
2013
9.5
Ruby Red 10/17/2012
0
Affinity Broadspec
TM
*DuPont Thifensulfuron-methyl – 25%, Tribenuron- methyl- 25%, other ingredients – 50%

19

Fertilizer
rate/ ha kg/ha
46-0-0
46-0-0
46-0-0
46-0-0

73.9
181
41.3
83.5

without any barrier to natural enemies. Closed plots consisted of 1 m tall, 0.36 m diameter
tomato support cages, covered with sewn sleeves of no-see-um mesh (approx. 625 holes per 6.45
cm, Skeeta, Bradenton, FL). The bottoms of the cages were buried 15 cm into the ground to
prevent access by ground-dwelling predators. The top of the sleeves were tied with nylon cord to
prevent flying predators from entering. The sham cages were identical to closed plots with the
exception that the sleeves had multiple 10 cm slits on each side and at the bottom of the mesh
allowing entry of predators and parasitoids, including foliar-foraging and ground-dwelling
natural enemies (Figure 3). All treatments were replicated five times per field in a completely
randomized design.

A

B

C

Figure 3. Photo illustrating natural enemy exclusion treatments used in our study A) closed plot
caged to exclude all natural enemies, B) open plot allowing access to all natural enemies and C)
sham plots, which are caged but, with holes on the ground and canopy levels to allow access by
natural enemies.

20

Natural enemy community sampling
To characterize the overall natural enemy community in the wheat fields, we used a
variety of sampling methods. To sample the ground-dwelling predator community, pitfall traps
(n = 4, plastic Solo cups, 11 cm in diameter and 14 cm in depth) 1/3rd filled with 40 % propylene
glycol solution were established next to the plots and 4 m apart from one another. In addition, 23
x 28 cm yellow sticky card traps (n = 4, PHEROCON AM, Great Lakes IPM, Vestaburg,
Michigan) were placed next to the pitfall traps to sample flying predators. The yellow sticky
cards were hung on a plastic step-in fence posts (Zareba Systems, Lititz, PA), and positioned just
above the plant canopy. Finally, on each sample date, natural enemies were counted by visual
observation for a fixed time (five minutes) in each plot. Any natural enemies found in closed
plots were manually removed during the sampling. All the predators were identified in the field
or returned to the laboratory for identification. Araneae and Opiliones were identified to order
while most other organisms were identified to family. Due to their potential importance in aphid
control, Coccinellidae were identified to species. Coccinellidae that were difficult to identify in
the fields or were missing identifying features on sticky cards were categorized as “other
Coccinellidae”. The overall average of each natural enemy taxa with standard error of the mean
(SEM) was calculated by field and by year.
Aphid population growth
For the experiment, virus free R. padi were obtained from an MSU laboratory colony (C.
Malmstrom lab). The aphid colonies were maintained on wheat and oat (Avena sativa L.) plants
in a greenhouse under natural light conditions, supplemented by sodium plant growth lights
operating at 16 L : 8 D, and maintained at 18o C to 26o C, and 65 - 70 % RH. Wheat and oat

21

plants were sown in 10 cm square pots. When the plants were about 15 cm tall, they were
infested with mixed stages of R. padi. New plants were added to the colony as needed, and old
plants were discarded.
On May 18, 2012 and May 14, 2013 cage treatments were established when wheat plants
were at the six-seven Feekes growth stage (Miller 1999,Wise et al. 2011) in 2012, and at the six
Feekes growth stage in 2013. Each plot was infested with 50 laboratory reared R. padi of mixed
adult and nymphal stages. Prior to aphid infestation, other insects were removed from each plot
by hand, and by vacuuming the plots using a modified leaf blower (Fiedler and Landis 2007).
Aphid infected leaves with 50 R. padi from the greenhouse plants were cut off and placed
between the leaves of the middle wheat plant of each plot. In 2012, the initial establishment of
R.padi in the plots was very low and all plots were reinfested with 50 additional aphids on May
23. After infestation aphid abundance was assessed once per week for three consecutive weeks
by counting all aphids on all plants within the plots. Alate and apterous aphids were recorded
separately. In both years, naturally occurring S. avenae were also observed and were counted
separately. To control for the effect of sampling, all the plots, even if they did not have any
aphids, were manipulated as if counts were being taken to ensure all plants and aphids received
the same amount of disturbance.
Statistical analyses
Statistical analyses tested the hypothesis that the natural enemy community suppresses
aphid population growth. To provide a meaningful comparison of experiment aphid pressure, and
to meet assumptions of homogeneity and variance, cumulative aphid-days were used instead of
raw aphid counts. Cumulative aphid-days was calculated by the following equation

22

d

CAD  
i 1

( Ai  Ai 1 )(Di  Di 1 )
2

Where d is total days sampled, Ai is the population of aphids on day i, Di date of sample i.
Plots where aphids failed to establish from the beginning were excluded from statistical analyses.
ANOVA procedures (R version 3.0.2, R Core Team 2013) were used to analyze cumulative
aphid-days (for each species, sites and years), with the aphids per tiller on the treatments (open,
closed, sham) and field as factors. If significant differences occurred, means were compared by
Tukey's Honestly Significant Difference (HSD) test (α = 0.05).
Results
Natural enemy community
Using all three sampling methods, we collected a total of 4,065 natural enemies
representing 13 taxa. Overall, seven taxa of ground-dwelling natural enemies were captured in
pitfall traps over both years. In 2012, the most common family in field 1 were Formicidae
followed by Araneae, Carabidae and Opiliones (Table 2). In contrast, in field 2 the most
common natural enemies were Araneae followed by Carabidae. In 2013, in field 3 and field 4
Carabidae were the most common taxa followed by Araneae and Staphylinidae.
Yellow sticky cards captured six families of flying predators. In 2012, in field 1 the most
common family was Dolichopodidae followed by Chrysopidae and Syrphidae while in field 2 the
most common family was Syrphidae followed by Chrysopidae and Dolichopodidae and
Harmonia axyridis. In 2013, Syrphidae were the most common natural enemies in both fields
followed by Nabidae in field 3, Cantharidae and the coccinellid Coleomegilla maculata in field
4.
23

Table 2. Mean numbers (± SEM) of natural enemies captured in pitfall traps, yellow sticky cards
and visually observed in four wheat fields in 2012 and 2013, Michigan State University campus
farm East Lansing, Michigan.

Collection methods
Pitfall trap
Coccinellidae
Carabidae
Formicidae
Araneae
Opiliones
Elateridae
Staphylinidae
Yellow sticky card
C. maculata
H. convergens
C. septempunctata
H. axyridis
Other Coccinellidae
Dolichopodidae
Chrysopidae
Syrphidae
Nabidae
Cantharidae
Visual observation
C. maculata
C. septempunctata
C. septempunctata larvae
H. axyridis
H. axyridis larvae
Other Coccinellidae larvae
Chrysopidae larvae
Syrphidae
Carabidae
Araneae
Anthocoridae

2012
Field 1
0.2 ± 0.1
9.1 ± 1.7
30.7 ± 10.2
12.8 ± 1.7
7.1 ± 1.4
0.4 ± 0.2
NA

0.2
0.6
0.3
0.4
0.2
2.9
2.4
1.7

±
±
±
±
±
±
±
±
0
0.1 ±

0.3
0.2
0.2
0.1
0.2
0.1
0.3
0.1
0.1

0
±
±
±
±
±
±
±
0
±
±

Field 2
0.7 ± 0.2
4.6 ± 1.2
2.6 ± 0.8
17.5 ± 1.8
1.4 ± 0.3
0
NA

0.1
0.2
0.1
0.2
0.1
1.1
0.8
0.5

0.4
0. 6
0.3
2.0
0.4
3.1
5.1
10.1

±
±
±
±
±
±
±
±
0
0.3 ±

0.0

0.1
0.1
0.1
0.0
0.1
0.0
0.1

0.1
0.1
0.1
0.3
0.2
0.3
0.1
0.6
0.2

0.1
0.0

24

0
±
±
±
0
±
±
±
±
±
±

0.1
0.3
0.2
0.4
0.2
0.7
1.0
1.6
0.2

0.0
0.0
0.0
0.1
0.1
0.1
0.0
0.2
0.1

2013
Field 3
Field 4
0.1 ± 0.1
1.2 ± 0.5
14.9 ± 3.5
12.8 ± 2.1
2.9 ± 1.2
7.6 ± 1.9
10.8 ± 2.0
7.5 ± 1.5
0.1 ± 0.1
0.3 ± 0.2
0.1 ± 0.1
0.2 ± 0.1
7.6 ± 2.4
4.9 ± 1.3

0.4 ± 0.2
0
0
0
0.2 ± 0.1
0
0.8 ± 0.3
4.8 ± 1.4
1.2 ± 0.8
0.8 ± 0.3

1.2 ± 0.3
0
0.1 ± 0.1
0
0.2 ± 0.2
0
0.3 ± 0.2
4.0 ± 1.0
0.3 ± 0.2
1.4 ± 0.6

0.3 ± 0.1
0.1 ± 0.1
0
0.2 ± 0.1
0.03 ± 0.03
0
0.1 ± 0.1
0.2 ± 0.1
0.2 ± 0.1
0.1 ± 0.0
0.1 ± 0.1

0.5 ± 0.1
0.3 ± 0.1
0
0.2 ± 0.1
0.1 ± 0.0
0
0
0.3 ± 0.1
0
0
0.1 ± 0.0

During the visual sampling, six natural enemy families were observed. In 2012, C.
septempunctata and Syrphidae were the most commonly observed in field 1. In contrast, Araneae
were the most commonly observed taxa in field 2, followed by Coccinellidae larvae and
Syrphidae adult. In 2013, the most common taxa were adult C. maculata in both fields, following
by adult Harmonia axyridis, Syrphidae, Carabidae and Anthocoridae in field 3, and adult C.
septempunctata, H. axyridis and Syrphidae in field 4.
Aphid population growth
Exclusion of natural enemies resulted in dramatically increased R. padi and S. avenae
populations in both years (Figure 4). Cumulative aphid-days for R. padi varied significantly
between years (F1, 52= 26.9, p = <0.001), sites (F1, 52= 6.3, p = 0.01) and treatments (F2, 52 = 10.9,
p = < 0.001). In 2012, R. padi numbers were lower than in 2013. Despite differences in years and
sites, the treatment patterns were the same. Closed plots always had higher cumulative R. padi
days per tiller than open and sham, with open and sham cages not significantly different from
each other. Cumulative S. avenae days per tiller also varied significantly between treatments (F1,
52 =3.9,

p = 0.03), while year and sites were not significant. The closed plots for S. avenae

contained significantly higher cumulative aphid number per tiller than sham and open plots, with
sham cages not significantly different from open plots.
Discussion
The natural enemy community effectively controlled aphid population densities in wheat
in two sites in both years. Similar to studies in other North American wheat growing regions
(Mohamed et al. 2000, Brewer and Elliott 2004, Clement et al. 2004, Elliott et al. 2006) we
found Coccinellidae adults and larvae, Chrysopidae adult and larvae, Syrphidae adults, and
25

80

a)

b)

2012

2013

70
A
60

Mean cumulative aphid abundance / tiller

Field 3

Field 1

50

Field 4

Field 2

40

C

30
20
10

B

A
B

C

0
Closed
90

Open

Sham

Closed

c)

Open

Sham

B

C

Open

Sham

d)

80
70

60
50

A

40
30
20
A

10

B

C

0
Closed

Open

Sham

Closed

Figure 4. Mean cumulative aphid numbers (± SEM) per tiller of; a) Rhopalosiphum padi in
2012, b) R. padi in 2013, c) Sitobion avenae in 2012, d) S. avenae in 2013, among treatment in
closed, exclusion of all natural enemy, open exposed to all natural enemies, and sham to control
for cage effect. ANOVA was used to test statistical differences. Different letters above the
treatments indicate statistically significant differences among aphids per tillers at α = 0.05.

26

numerous ground-dwelling predators Carabidae, Staphylinidae, Araneae and Opiliones were the
most frequently collected natural enemies in our wheat fields. In other studies, the convergent
lady beetle, H. convergens, and the common damsel bug Nabidae were the most common
predators observed (Rice and Wilde 1988, Elliott et al. 1998, Mohamed et al. 2000), but in our
research H. convergens was observed only in 2012, and Nabidae were only observed in 2013.
Also, unlike other studies, we did not observe Syrphidae larvae or parasitoid wasps. This may be
due to the relatively low aphid population at the field level or the early season timing of our
study. In contrast, we observed relatively high numbers of Opiliones, Elateridae, Cantharidae,
and Anthocoridae. These communities of ground-dwelling and foliar-foraging natural enemies,
acting either independently or together, can reduce aphid population density (Symondson et al.
2002, Schmidt et al. 2003, Schmidt et al. 2004, Macfadyen et al. 2009, Thies et al. 2011).
Numerous studies show that adult Coccinellidae can suppress cereal aphid populations (Rice and
Wilde 1988, Elliott and Kieckhefer 1990, Messina and Hanks 1998) Also, results have shown
that certain Carabidae consume R. padi and S. avenae (Edwards et al. 1979, Griffiths et al. 1985,
Chiverton 1986) and can reduce aphid density (Symondson et al. 2002) by climbing the plant
(Vickerman and Wratten 1979) or by preying on aphids when they drop from plants (Duffield et
al. 1996). Previous authors showed that certain predator taxa interact synergistically to consume
more aphids and reduce aphid populations in combination (Soluk 1993). For example,
coccinellid foraging reduces aphid populations directly by predation, but also indirectly by
dislodging aphids from the vegetation onto the ground where they can be consumed by
Carabidae (Losey and Denno 1999).
Aphid populations per tiller for both species varied across sites and years, and were
significantly higher in closed versus open or sham plots. In no case were aphid numbers in sham
27

cages statistically different from the open cages, suggesting that cages effects were minimal, a
finding that conforms earlier work in soybean (Costamagna et al. 2008, Gardiner et al. 2009). In
contrast, the closed plots in our study had up to 57 times higher cumulative aphid-days than the
open plots. Exclusion studies looking at aphid numbers per cage found similar results. An
exclusion cage study in Colorado reported that cereal aphid numbers were between 2.6 and 11.2
times higher in caged wheat plots compared to open plots (Mohamed et al. 2000). Other studies
reported cereal aphid numbers three to six times higher when predators were excluded
(Chambers et al. 1983, Holland and Thomas 1997).
Natural enemies are important for Michigan wheat production because they can keep
aphid populations below damaging levels. The average numbers of S. avenae we found in the
closed plots reached 42 aphids per tiller, while in the open plots numbers of S. avenae never
exceeded 1 per tiller. The average numbers of R. padi in our study reached 62 aphids per tiller in
the closed plots The open plot had an average of 7 aphids of R. padi per tiller, which is much less
than the economic thresholds. The economic threshold in Michigan for both species is 12-15
aphids per tiller (C. Difanzo). Although we did not take yield measurements, based on these
thresholds it appears that aphid numbers in our closed plots were high enough to cause yield
damage.
Under the conditions we studied natural enemies regularly provided sufficient aphid
suppuration, to keep cereal aphids population below economically damaging levels. In contrast,
the use of preventive insecticides may be harmful to existing and effective natural enemy
communities (Wiles and Jepson 1992, Banken and Stark 1998), and result in pest resurgence
(Dutcher 2007). Some Michigan farmers have been adopting preventive spray to counter
occasional pest including the True Armyworm (Pseudaletia unipuncta Haworth) (Ben Werling
28

personal communication) In contrast, our result suggests insecticide sprays should only be used
when natural enemies cannot control the aphid population and the aphid is above the economic
threshold. Relying on natural biological control provided by aphid predators and only using
chemical control when necessary will help insure more economical and sustainable insect pest
management in Michigan wheat.

29

CHAPTER 3
RELATIVE ROLE OF GROUND-DWELLING AND FOLIAR-FORAGING
PREDATORS IN CONTROLLING CEREAL APHIDS IN, MICHIGAN WHEAT
Abstract
Diverse communities of natural enemies are important biological control agents of cereal
aphids. Depending on their foraging strategies, aphid natural enemies can be categorized as
foliar-foraging predators and parasitoids or ground-dwelling predators, and both guilds have
been shown to contribute to suppressing cereal aphid population growth. We investigated the
effect of each natural enemy guild independently and together on field populations of
Rhopalosiphum padi (L.) and Sitobion avenae (F.) (Hemiptera: Aphidae) in two Michigan State
University campus wheat (Triticum aestivum L.) fields. We experimentally manipulated natural
enemies with cages and barriers to exclude 1) foliar-foraging predators and parasitoids, 2)
ground-dwelling predators, 3) and all natural enemies, and compared aphid populations per tiller
in these treatments to open plots as a control. Populations of R. padi were dramatically and
significantly higher in all natural enemy exclusion plots. Additionally, R. padi densities were
significantly higher in plots where ground-dwelling predators were excluded compared to plots
where foliar-foraging predators were excluded. No statistically significant differences were
observed in numbers of S. avenae between treatments. Our results suggest that, ground-dwelling
predators play a larger role in cereal aphid suppression than foliar-foraging natural enemies, and
in combination, predators can almost completely halt aphid population growth. We conclude that
existing natural enemy communities can be highly effective in biological control of aphids under
the conditions we studied.
Keywords: Cereal aphids, natural enemies, foliar-foraging predators, ground-dwelling predators.

30

Introduction
Cereal aphids (Hemiptera: Aphididae) are serious pests of grain crops worldwide
(Alsuhaibani 1996, Mohamed et al. 2000). However, naturally occurring predators and
parasitoids can frequently reduce aphid population growth and subsequent yield losses
(Helenius 1990, Dennis and Wratten 1991, Östman et al. 2001, Lang 2003, Östman et al. 2003,
Schmidt et al. 2003, Bianchi et al. 2006), reducing the need for chemical control (Krauss et al.
2011). Cereal aphids are attacked by a wide variety of natural enemies with different foraging
strategies (Chambers et al. 1986). Foliar-foraging natural enemies include Coccinellidae
(Coleoptera), Chrysopidae (Neuroptera), Syrphidae (Diptera), and parasitoid wasps
(Hymenoptera). These taxa typically forage in the upper vegetation of cereal plants, often fly
between plants while foraging, and predominantly feed on aphids (Chambers et al. 1983).
Ground-dwelling generalist predators include Carabidae (Coleoptera), Staphylinidae
(Coleoptera), and Araneae. These enemies live and forage near the ground and may include
diverse prey in their diets, including aphids (Symondson et al. 2002). Ground-dwelling predators
primarily prey on aphids occurring on the lower portion of the plant, or that have fallen from the
plant due to disturbance. Both groups of natural enemies, acting independently or together, can
reduce aphid population density (Symondson et al. 2002, Schmidt et al. 2004), in turn reducing
plant damage and increasing yield (Östman et al. 2003).
Some studies show that foliar-foraging and ground-dwelling predators can interact
synergistically, suppressing aphid populations to greater extent than when they act independently
(Schmidt et al. 2003, Straub et al. 2008). For example, Losey and Denno (1999) found that in
alfalfa in the absence of foliar-foraging predators, ground-dwelling predators had a very small
effect on aphid populations. However, when foliar-foraging Coccinellidae predators were added
31

to the system, the effect of both predator groups on aphid suppression was higher than the sum of
each community. The reason for this synergetic effect was that Coccinellidae foraging caused
aphids to drop from the vegetation onto the ground, where they were consumed by Carabidae
(Losey and Denno 1999).
Various have examined the role of natural enemies in suppressing cereal aphids. Thies et
al. (2011) manipulated the natural enemy community in cages in cereal fields in five European
regions and demonstrated that, compared to the open field, aphid populations were 28% higher
with reduced densities of ground-dwelling predators, 97% higher with reduced densities of flying
parasitoids and predators, and 199% higher with the removal of both enemy groups. Similar
observations were made by Schmidt et al. (2003) in cereal fields in Germany where aphid
populations were 18% higher with reduced densities of ground-dwelling predators, 70% higher
with reduced densities of flying parasitoids and predators, and 172% higher with reduced
densities of both natural enemies groups. These studies show that although both foliar and
ground-dwelling natural enemy communities can be important in controlling cereal aphids, the
absolute effect of foliar natural enemies is often stronger, and the greatest pest suppression
occurs when these two communities act in combination.
Foliar-foraging predators, especially Coccinellidae, are often the dominant natural enemy
of aphids in cereal fields and many agroecosystems in North America (LaMana and Miller 1996,
Obrycki and Kring 1998, Elliott and Kieckhefer 2000, Wright and DeVries 2000, Clement et al.
2004). Most species of Coccinellidae overwinter as adults (Colunga-Garcia and Gage 1998) and
simultaneously occur with the bird cherry oat aphid, Rhopalosiphum padi (L.), and other cereal
aphids in the spring (Phoofolo et al. 2007). Adult Coccinellids are capable of consuming up
to100 aphids per day (Xue et al. 2009, Hallett et al. 2013) and dramatically reduce aphid
32

numbers in wheat fields (Elliott and Kieckhefer 2000).
The impact of the ground-dwelling predator guild is thought to be the greatest early in the
growing season (Sunderland and Vickerman 1980, Dennis and Wratten 1991, Lang 2003),
although they continue to feed on aphids up until aphid populations peak in cereals in early
summer (Winder 1990, Winder et al. 1994). Among the ground-dwelling predators, Carabidae
probably contribute the most to aphid suppression in cereal crops. These polyphagous predators
often colonize cereal fields from neighboring habitats (French and Elliott 1999), and are known
to consume R. padi, English grain aphids, Sitobion avenae (F.), and other aphids species
(Edwards et al. 1979, Chiverton 1986). They can reduce aphid density by preying on aphids
directly when the aphids drop from plant (Duffield et al. 1996, Symondson et al. 2002), or by
climbing the plant. In a study examining the relative importance of ground-dwelling predators on
aphid populations, Lang (2003) manipulated populations of ground beetles and spiders and found
that aphid population was highest in the plots where Carabidae were removed implying a
substantial predation impact of ground beetles.
The American Midwest is a major wheat producing area; however, studies have not been
performed in wheat in this region to understand the effect of natural enemies on cereal aphid
suppression. The purpose of this study was to determine the effect of ground-dwelling and foliarforaging predator guilds on cereal aphid suppression in Michigan. We used predator exclusion
barriers to exclude different groups of natural enemies from populations of two species of aphid
occurring in wheat fields on Michigan State University campus, East Lansing Michigan.
Our hypotheses for the study were 1) the natural enemy community as whole would
significantly suppress aphid populations, and 2) foliar-foraging predators are more effective in

33

suppression of cereal aphid density than ground-dwelling predators.
Methods
Study sites
The experiments were conducted in 2013 in two winter wheat fields (Triticum aestivum
L.) on the Michigan State University campus farm, East Lansing, Michigan. The wheat varieties
were Red Devil and Ruby Red and were planted in the fall of 2012. Each field received
herbicide, fungicide and fertilizers at rates determined by the university farm Manager (Table 1
chapter 2). No insecticides were applied in either field.
Plot establishment
On May 14, we selected a 30 x 20 m area at least 30-35 m from a field edge. Within this
area, individual 1 x 1 m plots were established 5 m equidistant from each other. The plots were
assigned to 4 different treatments in a completely randomized design. Treatments included:
exclusion of foliar-foraging predators and parasitoids (-F), exclusion of ground-dwelling
predators (-G), exclusion of both foliar and ground-dwelling natural enemies (-F-G), and fully
open plots (O), which were exposed to all natural enemies. Each of the four cage treatments
consisted of a 1 m3 PVC frame, erected around the plots, with the legs buried in the soil. In the
plots excluding ground-dwelling predators (-G), and in the plots excluding all natural enemies
(F-G), a 30 cm tall corrugated plastic barrier was erected around the PVC frame. The bottom 10
cm of this barrier was buried in the soil so that 20 cm was left above ground to restrict access by
ground-dwelling predators (Figure 5 A, B). To exclude all natural enemies (-F-G) and foliarforaging predators and parasitoids (-F), the top and all sides of the PVC frame were covered with
no-see-um mesh (approx. 625 holes per 6.45 cm, Skeeta, Bradenton, FL), to prevent flying
34

predators from entering the cage. To exclude all natural enemies (-F-G), the bottoms of the mesh
were buried 5 cm into the ground while in –F plots, the bottoms of the mesh were raised 2 cm
above the ground to allow access by ground-dwelling predators (Figure 5 C). Finally, open plots
(O) consisted of 1 x 1 m area demarcated with flags, without any barrier to natural enemies
(Figure 5 D). All treatments were replicated five times in each field

A

B

C

D

Figure 5. Photo illustrating the natural enemy exclusion experiment in Michigan State
University campus wheat fields. Each plot was assigned a cage treatment to exclude different
groups of natural enemies from aphid populations. Treatments included exclusion of A) foliarforaging predators and parasitoids (-F), B) ground-dwelling predators (-G), C) and all natural
enemies (-F -G), and D) open plot (O), which allowed access to all natural enemies and served as
a control.
35

Predator sampling
Natural enemies were sampled weekly from May 21 until June 5. To sample the grounddwelling predator community, pitfall traps (plastic Solo cups, 11 cm diameter and 14 cm depth)
1/3rd filled with 40 % propylene glycol solution were established inside of each plot and 5 m
apart from one another. Twenty pitfall traps were placed at each study site. To capture foliar
predators, 23 x 28 cm yellow sticky card traps (PHEROCON AM, Great Lakes IPM, Vestaburg,
Michigan) were placed in the center of the sampling plots. The yellow sticky cards were hung on
a 1 m plastic step-in fence post (Zareba Systems, Lititz, PA) above the plant canopy and were
moved up as the plant canopy grew. Also, on each sample date, natural enemies were counted by
visual observation of each plot for five minutes. The visually observed natural enemies were
identified in the field and the natural enemies on the traps returned to the laboratory for
identification. Araneae and Opiliones were identified to order while all other organisms were
identified to family, except Coccinellidae which were identified to species. Coccinellidae that
were difficult to identify under field conditions were categorized as “other Coccinellidae”.
Aphid population growth
Virus free R. padi were obtained from a laboratory colony (C. Malmstrom, MSU). The
aphid colonies were maintained on wheat and oat (Avena sativa L.) plants in a greenhouse under
natural light conditions, supplemented by sodium plant growth lights operating at 16 L : 8 D, and
maintained at 18o C to 26o C, and 65-70 % RH. Wheat and oat plants were sown in 10 cm square
pots. When the plants were about 15 cm tall, they were infested with mixed stages of R. padi.
New plants were added to the colony as needed, and old plants were discarded
On May 14, 2013 at the Feekes stage five all plots were infested with 100 laboratory
36

reared R. padi of mixed adult and nymphal stages. Before the aphid infestation, natural enemies
were removed from each plot by hand or vacuuming the plots using a modified leaf blower
(Fiedler and Landis 2007). The aphids were transferred to the treatment plants by cutting leaves
infested with aphids from the cultured greenhouse plants and placing them between the leaves of
the middle wheat plant of the plot. Aphid abundance was assessed once per week after
infestation, by counting all aphids on all plants within the plots. Both alate and apterous aphids
were recorded. On the first sampling date, naturally occurring S. avenae were also observed, so
from that date on, counts of S. avenae were also recorded. To control for the sampling effect, all
the plots, even if they did not have any aphids, were manipulated as if counts were being taken to
ensure all plants and insects (aphid sand natural enemies) received the same amount of
disturbance.
Statistical analyses
Statistical analyses were done to test the hypothesis that foliar-foraging predators are
more effective on suppressing cereal aphid population then ground-dwelling predators, and that
in combination both natural enemy guilds suppress aphid population growth to greater degree
than, when they act independently. ANOVA procedures (R version 3.0.2, R Core Team 2013)
were used to analyze the aphid population growth per tiller in 4 treatments (-F, -G, -F –G, O
plots). An ANOVA of aphid observations by cage treatment specifying repeated-measures by
plot was nested within site, as this model structure produced residuals that conformed to the
assumptions of ANOVA most closely. We used pairwise t-tests that had been Holm-adjusted for
multiple comparisons to compare treatments.

37

Results
Predator sampling
Overall, using all three methods of sampling we captured a total of 4,567 individual
natural enemies. In the pitfall traps, seven taxa of natural enemies were captured. No enclosure
method completely prevented the occurrence of natural enemies (Table 3). In the –F-G plots, the
most frequently captured taxa were Staphylinidae followed by Carabidae, Aranea and
Formicidae. In contrast, in –G, -F, and O plots, the Carabidae were the most common taxon,
followed by Araneae, and Staphylinidae. Overall, the numbers of ground-dwelling predators
captured in the –F-G and -G plots were less than they were on the –F and O plots.
On yellow sticky cards, we captured five families of flying predators. In -F -G plots, a
single Coccinellidae was captured. In the -G plots Syrphidae were the most common family
captured, followed by Cantharidae. In –F plots, the Coccinellid Coleomegilla maculata, followed
by Syrphidae were the most common taxa captured, and in O plots, Syrphidae followed by C.
maculata and Cantharidae were most frequently captured.
In visual observations, we occasionally observed adult C. maculata, C. septempunctata,
Syrphidae, Formicidae, Araneae and Opiliones in the -F -G plots. In -G plots C. maculata
followed by Syrphidae, were most commonly observed. In the –F plots, C. maculata followed by
Araneae and Carabidae were most commonly observed. In the O plots, the natural enemy
commonly was dominated by C. maculata followed by Syrphidae and Carabidae.
For Carabidae and Coccinellidae, often the most important predators of cereal aphids, the
exclusion techniques sufficiently reduced their numbers to allow us to examine their effect on
aphid population growth (Figures 6 and 7).
38

Table 3. Mean number (± SEM) of most abundant natural enemies captured in pitfall traps,
yellow sticky cards and by visual observation in wheat study sites in Michigan State University
campus, East Lansing, Michigan, 2013.
Collection methods

Plots
-F-G

Pitfall traps
Coccinellidae
Carabidae
Formicidae
Araneae
Opiliones
Elateridae
Staphylinidae
Yellow sticky card
C. maculata
H. convergens
C. septempunctata
Other Coccinellidae
Chrysopidae
Syrphidae
Nabidae
Cantharidae
Visual observations
C. maculata
C. septempunctata
C. septempunctata larvae
H. axyridis
Other Coccinellidae larvae
Crabidae
Syrphidae
Formicidae
Araneae
Opiliones
Cantharidae
Chrysopidae
Nabidae

-G

-F

O

0.1 ± 0.0
3.5 ± 0.6
1.3 ± 0.4
2.0 ± 0.5
0.1 ± 0.0
0.2 ± 0.1
3.7 ± 0.9

0.5 ± 0.2
4.2 ± 0.9
1.9 ± 0.5
3.8 ± 0.5
0.1 ± 0.1
0.2 ± 0.1
3.8 ± 0.7

0.5 ± 0.3
15.4 ± 2.0
3.0 ± 0.7
10.4 ± 1.0
0.4 ± 0.2
0.1 ± 0.1
8.0 ± 1.8

0.9 ± 0.3
12.9 ± 1.1
1.2 ± 0.3
11.1 ± 1.4
0.1 ± 0.1
0.0 ± 0.0
6.5 ± 1.2

0.0 ± 0.0
0.0 ± 0.0
0.0 ± 0.0
0.03 ± 0.03
0.0 ± 0.0
0.0 ± 0.0
0.0 ± 0.0
0.0 ± 0.0

0.5 ± 0.1
0.03 ± 0.0
0.1 ± 0.1
0.2 ± 0.1
0.6 ± 0.3
2.5 ± 0.5
0.1 ± 0.1
1.0 ± 0.2

0.4 ± 0.1
0.0 ± 0.0
0.0 ± 0.0
0.03 ± 0.03
0.03 ± 0.03
0.2 ± 0.1
0.0 ± 0.0
0.03 ± 0.03

0.7 ± 0.2
0.0 ± 0.0
0.03 ± 0.03
0.4 ± 0.1
0.6 ± 0.2
2.6 ± 0.5
0.3 ± 0.2
0.7 ± 0.3

0.7 ± 0.2
0.1 ± 0.1
0.0 ± 0.0
0.0 ± 0.0
0.0 ± 0.0
0.0 ± 0.0
0.1 ± 0.0
0.2 ± 0.1
0.2 ± 0.1
0.1 ± 0.1
0.0 ± 0.0
0.0 ± 0.0
0.0 ± 0.0

1.8 ± 0.4
0.1 ± 0.1
0.2 ± 0.1
0.1 ± 0.0
0.1 ± 0.1
0.1 ± 0.0
1.9 ± 0.4
0.2 ± 0.1
0.4 ± 0.2
0.03 ± 0.0
0.03 ± 0.0
0.03 ± 0.0
0.0 ± 0.0

0.8 ± 0.3
0.03 ± 0.03
0.0 ± 0.0
0.0 ± 0.0
0.0 ± 0.0
0.5 ± 0.2
0.2 ± 0.1
0.2 ± 0.1
0.6 ± 0.3
0.1 ± 0.0
0.0 ± 0.0
0.0 ± 0.0
0.03 ± 0.03

1.6 ± 0.4
0.2 ± 0.1
0.3 0 0.1
0.1 ± 0.0
0.2 ± 0.1
0.4 ± 0.2
0.8 ± 0.2
0.2 ± 0.1
0.2 ± 0.1
0.03 ± 0.03
0.03 ± 0.03
0.03 ± 0.03
0.0 ± 0.0

39

25
-G
-F-G

Carabidae / trap

20

-F
O

15
10

5
0
5/21/2013

5/29/2013

6/5/2013

Figure 6. Abundance of Carabidae captured in pitfall traps in –G (excluding ground-dwelling
predators),-F-G (excluding all natural enemies), -F (excluding foliar-foraging predators) and O
plots (exposed to all natural enemies) in 2013.

1.4

-G

Coccinellidae / trap

1.2

-F-G
-F

1

O

0.8
0.6
0.4
0.2
0
5/21/2013

5/29/2013

6/5/2013

Figure 7. Abundance of Coccinellidae captured in sticky cards in traps in –G (excluding grounddwelling predators),-F-G (excluding all natural enemies), -F (excluding foliar-foraging
predators) and O plots (exposed to all natural enemies) in 2013.
40

Aphid population growth
Treatments manipulating natural enemies had different effects on population growth of R.
padi and S. avenae. R. padi populations varied significantly among treatments (F3, 113 = 11.2, p =
< 0.001), and there was no significant site effect. In -F-G plots, R. padi increased from 100
aphids / m2 to a mean of 3750 / m2 (> 5 aphids / tiller) over the three week interval (Figure 8).
Aphid increase was significantly lower when foliar-foraging predators had access to plots (-G
plots). Aphid population increases were even lower when ground-dwelling predators alone (-F
plots) had access to plots. Finally, in plots where all natural enemies had access (O plots), aphid
populations were lower than all other 3 treatments and did not increase during the 3 week period
(mean= 28.3 / m2 or < 0.10 aphids / tiller) indicating that the natural enemy community as a
whole was very effective in preventing R. padi increases.
S. avenae population were dramatically lower than R. padi. Although ANOVA suggested
that populations varied significantly between treatments (F3, 113=3.7, p = 0.05), Posthoc pairwise
comparisons did not find any statistically significant differences, although the general pattern of
population growth by treatments was largely similar to that of R. padi (Figure 9).
Discussion
From our previous study (Chapter 2) we know that existing natural enemy communities
in wheat are effective at suppressing cereal aphid populations below economic thresholds. The
main objective of this study was to determine the relative contribution of natural enemy feeding
guilds (foliar-foraging versus ground-dwelling predators) to cereal aphid population suppression.
Similar to other studies in North America (Elliott and Kieckhefer 1990, Elliott et al. 1991,
Mohamed et al. 2000, Brewer and Elliott 2004) the most common taxa of foliar-foraging
41

Mean Rhopalosiphum padi /tiller

7
6

-F-G

-G

-F

O

a

5
4
3
2
a

b

1
a

b

c

d

b

c

c

d

d

0
5.21.2013

5.29.13

6.5.13

Figure 8. Mean number (± SEM) of R. padi among treatments; -F-G (excluding all natural
enemies), -G (excluding ground-dwelling predators), -F (excluding foliar-foraging predators) and
O (open plot, exposed to all natural enemies) in 2013. ANOVA with repeated measures was
used. For treatment comparisons pairwise t-tests that have been Holm-adjusted were used.
Different letters indicate statistically significant differences within treatments at α = 0.05 during
a sampling period.
-F-G

Mean Sitobion avenae /tiller

3

-G
2.5

-F
O

2
1.5
1
0.5
0
5.21.2013

5.29.13

6.5.13

Figure 9. Mean number (± SEM) of S. avenae among treatments; -F-G (excluding all natural
enemies),-G (excluding ground-dwelling predators), -F (excluding foliar-foraging predators) and
O (open plot, exposed to all natural enemies) in 2013. ANOVA with repeated measures was
used. For treatment comparisons pairwise t-tests that have been Holm-adjusted were used.
Different letters indicate statistically significant differences within treatments at α = 0.05 during
a sampling period.

42

predators that we found were adult Syrphidae, adult and larval Coccinellidae, adult Chrysopidae,
Cantharidae and Nabidae, and the most common ground-dwelling predators were Carabidae,
Staphylinidae, Araneae and Opiliones. Dissimilar to other North American studies, we observed
very low numbers of parasitoid wasps. The overall abundance of ground-dwelling predators,
especially Carabidae, in our study were higher than the density of foliar-foraging predators.
Similar to other studies (Chambers et al. 1986, Brewer and Elliott 2004), our results
showed both foliar-foraging and ground-dwelling predators in combination were effective at
suppressing aphid populations. In fact, when both predator groups were present (in the open
plots), aphid population growth was even less than what we would have expected by combining
the results from the top closed and bottom closed cages. This significantly lower aphid
population growth provided by the combination of foliar-foraging and ground-dwelling predators
suggests a synergy between the different natural enemy feeding groups. Losey and Denno (1999)
showed the synergystic interaction of ground-dwelling and foliar-foraging predators on pea
aphid in alfalfa. The aphids, in response to foraging Coccinelidae, dropped from the alfalfa
canopy to the ground where they were consumed by ground-dwelling predators. Our results
confirm that in combination these two foraging groups better suppress aphid populations than
when acting alone.
In our study, ground-dwelling predators alone were more effective than foliar-foraging
predators. These results are in contrast to previous European work (Schmidt et al. 2003, Thies et
al. 2011) where foliar-foraging predators and parasitoids were more effective. Schmidt et al.
(2003) conducted an experiment in the early season (May) in Germany and found that parasitoid
wasps provided more effective aphid control than ground-dwelling predators. Thies et al. (2011)
conducted a similar experiment in five European regions and their results suggested that
43

parasitoids and foliar-foraging predators were more important in controlling cereal aphids than
ground-dwelling predators, but the relative importance of parasitoids and foliar-foraging
predators greatly differed among European regions.
The increased efficacy of ground-dwelling predators that we observed in the present
study might be due the early season importance of ground-dwelling predators. Many studies
(Chiverton 1986, Kromp 1999, Lang 2003) suggesting that the effects of ground-dwelling
predators on suppressing aphids are strongest in early May, when aphid densities in cereals are
low and reproduction is slower than in summer. In contrast, flying predators like Coccinellidae
which primarily feed on aphids (Elliott et al. 1998) usually become more important once aphid
population densities become higher (Evans and Youssef 1992). Our study in wheat fields also
was conducted in the early season, starting in the middle of May and continuing until the 6th of
June. Finally, aphids are most easily accessed by ground-dwelling predators when they are
dislodged to the ground by predators, wind or rainfall (Winder 1990).
In conclusion, the role of ground-dwelling predators in controlling cereal aphids should
be reconsidered. They appeared to be more important in suppressing aphid population than
foliar-foraging predators. Future studies need to determine the factors, such as landscape
characteristics, management practices, and climate that make ground-dwelling predators more
effective and abundant in Michigan wheat fields.
This study highlights the importance of conservation biocontrol to enhance resident
natural enemy populations. Natural enemy populations can be fostered by providing favorable
micro-habitats for them (Thomas et al. 1991). Collins et al. (2002) showed that the presence of
beetle banks (grassy ridges) in the middle of wheat fields increased the number of Carabidae,

44

which in turn decreased cereal aphid populations. Dong et al. (2012) showed that the presence of
a ryegrass-margin on the edge of wheat fields enhanced the population density of Coccinellidae.
Providing habitat for these important predators can enhance biological control services against
aphids and other pests.

45

CHAPTER 4

CONCLUSIONS AND FUTURE DIRECTIONS
Biological control of cereal aphids on wheat in Michigan
Cereal aphids (Hemiptera: Aphidae) are serious pests of grain crops worldwide
(Alsuhaibani 1996, Mohamed et al. 2000). Previous research has demonstrated that natural
enemies that prey on aphids are important in inhibiting aphid population growth and reducing
subsequent yield losses (Helenius 1990, Dennis and Wratten 1991, Östman et al. 2001, Lang
2003, Östman et al. 2003, Schmidt et al. 2003, Bianchi et al. 2006), which in turn reduces the
need for chemical control (Krauss et al. 2011). In North America, the natural enemy community
in wheat (Triticum aestivum L.) studied in the Southern and Western great Plants (Pike and
Schaffner 1985, Mohamed et al. 2000, Clement et al. 2004, Brewer and Elliott 2004Lee et al.
2005) but, to our knowledge, has not been described in Michigan or the Midwest. The objectives
of this thesis research were to characterize the natural enemy community in Michigan wheat
fields and evaluate the role of different natural enemy groups together and independently on
cereal aphid population growth. We investigated these objectives in 4 winter wheat fields in the
Michigan State University campus in East Lansing, Michigan.
Overall, we found that the natural enemy community at our study sites, effectively
controlled aphid population densities in wheat. The community that consisted of foliar-foraging
predators including Coccinellidae species Chrysopidae, Syrphidae, Nabidae Cantharidae and
Anthocoridae, as well as numerous ground-dwelling predators Carabidae, Staphylinidae,
Araneae and Opiliones. In contrast to other regions, parasitoid wasps were rarely observed in our
study locations.

46

The effect of natural enemy community on aphid population densities was studied using
artificially infested Rhopalosiphum padi (L.) and natural occurring Sitobion avenae (L.). Our
work illustrated that populations for both species across sites and years were significantly higher
in caged plots where natural enemies were reduced compared to sham and open plots and that
were partly or totally exposed to natural enemies. Aphid numbers in sham cages were
statistically not different from the open plots, suggesting that cage effects were minimal. The
maximum number of cereal aphids in caged plots with reduced natural enemies was over the
economic threshold, but in plots where natural enemies were not reduced, the maximum number
of aphids was much less than the economic thresholds level. This result indicates that natural
enemies can contribute to control cereal aphids in the wheat fields
Relative role of ground-dwelling and foliar-foraging predators in controlling cereal aphids
In addition to evaluating the overall impact of all natural enemies together on aphid
population growth, this study also illustrated the relative role of each natural enemy feeding
guild, foliar-foraging versus ground-dwelling predators independently. The results confirmed
that, these guilds better suppressed aphid population growth in combination than when they acted
alone, and resulted in negative aphid population growth over 3 weeks suggesting a synergy
between foliar-foraging and ground-dwelling predators.
The abundance of ground-dwelling predators, especially Carabidae, was higher than the
density of foliar-foraging predators. Although many others studies (Schmidt et al. 2003, Thies et
al. 2011) showed that foliar-foraging predators were more important in decreasing aphid
populations, our result showed the opposite. Our work illustrated that ground-dwelling predators
alone suppressed aphid population growth more than foliar-foraging predators alone. Therefore,
the role of ground-dwelling predators in controlling cereal aphids should be reconsidered. They
47

appeared to be more important in suppressing aphid population than foliar-foraging predators in
wheat fields under Michigan State University campus, East Lansing, Michigan growing
conditions. Future studies need to determine the factors, such as landscape characteristics,
management practices, and climate that make ground-dwelling predators more effective and
abundant in Michigan wheat fields.
Natural enemies are important for Michigan wheat production because they can keep
aphid populations below damaging levels. From our study it is clear that natural enemies can
contribute to cereal aphid control and insecticides are not uniformly needed. Prescriptive
insecticide use may be harmful to existing and effective natural enemy communities (Wiles and
Jepson 1992) and may result in pest resurgence (Dutcher 2007). Our result suggests insecticide
sprays should only be used when natural enemies cannot control the aphid population and aphid
numbers are above the economic threshold. Relying on natural biological control provided by
aphid predators and only using chemical control when necessary will help insure more
economical and sustainable insect pest management in Michigan wheat.

48

APPENDIX

49

APPENDIX

Identifying natural enemies consume bird cherry oat aphids under laboratory conditions
The bird cherry oat aphid (Rhopalosiphum padi L.) can cause direct and indirect damage
to wheat (Triticum aestivum L.) and other small grains by feeding on leaves and as a vector of
barley yellow dwarf virus (BYDV) (Vickerman and Wratten 1979).While many predaceous and
omnivorous arthropods can be found in Michigan wheat fields, less is known about which
species may be the most important predators. To help determine which of the predators found in
field samples many be important in aphid suppression, we conducted a laboratory assay to
determine which potential predators in wheat consumed the greatest number of aphids. Results of
this preliminary study were used to help interpret and direct subsequent field studies.

Methods
Adult Carabidae and Coccinellidae beetles were collected from wheat fields on the
campus of Michigan State University, East Lansing, Michigan during May 2012 and tested as
potential natural enemies of wheat aphids. We used dry (without any killing solution) 11 plastic
Solo cups; 11 cm diameter and 14 cm depth pitfall traps to collect carabid beetles, and swept
vegetation to collect coccinellids. Pitfall traps were set out at approximately 5 PM and natural
enemies collected the following morning at approximately 8 AM. Potential predators were
individual held at 21-250 C in a growth chamber and provided with water from a moistened
dental wick until used in feeding trials that day. Rhopalosiphum padi were obtained from a
laboratory colony reared on potted wheat maintained at 21-250 C, L: 18 / D: 6 in a growth
chamber. For each feeding trial, two uninfested wheat leaves were cut in half and the four pieces
placed in 100 mm x 15mm Petri dishes lined with filter paper size 8.5 cm to which 2.5 ml water
50

was added to maintain constant humidity. To avoid damaging aphid mouth parts, aphids were
collected from infested plants by gently tapping leaves over a paper sheet to allow them to
remove stylets and drop naturally, or by gently pushing the aphid from behind with the brush tip
until it began to move. A mix of adult and nymphs (approximately 50:50) were then transferred
to a leaf in each Petri dish using a moisten paint brush. Aphids were held in a growth chamber at
21-250 C, L: 18 / D: 6 and 50 - 60% relative humidity and allowed to settle and begin feeding for
30 minutes prior to introduction of a potential predator.
At the beginning of each trial a single natural enemy was placed in each Petri dish (n = 10
replicates per predator) and returned to the growth chamber. After 3, 6 and 21h, dishes were
observed to determine the number of remaining aphids. Aphids that died but were not consumed
were not counted as predated.

Results
Two species of Coccinellidae beetles; Coccinella septempunctata, and Harmonia axyridis and
four species of Carabidae; Poecilus chalcites, Scarites subterraneus, Anisodactylus rusticus, and
Anisodactylus santaecrusis, were collected in sufficient numbers to conduct feeding trials. Both
species of Coccinellidae were effective on consuming R. Padi (Figure 10), while the two
Carabidae species S. subterraneus and A. rusticus were more effective than Poecilus chalcites
and A. santaecrusis (Figure 11).

51

Coccinella septempunctata

Harmonia axyridis

apid /dish

6
5

3 hours

4

6 hours

3

21 hours

2
1
0
alive

consumed

dead

alive

consumed

dead

Figure 10. Mean number of R. padi (± SEM) alive, missing and dead in the petri dishes
containing Coccinellidae at 3, 6 and 21 hours

aphid/ dish

6
5
4
3
2
1
0

3 hours
6 hours
21 hours

aphid / dish

alive
6
5
4
3
2
1
0

Poecilus chalcites

Scarites subterraneus

consumed

dead

alive

Anisodactylus rusticus

alive

consumed

consumed

dead

Anisodactylus santaecrusis

alive

dead

consumed

dead

Figure 11. Mean number of R. padi (± SEM) alive, missing and dead on the petri dish with
Carabidae at 3, 6 and 21 hours

52

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53

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