Field efficacy of insect pathogen, botanical 
and jasmonic acid for the management of 
wheat midge Sitodiplosis mosellana the 
impact on adult parasitoid ... populations in 
spring wheat
Authors: Govinda Shrestha & Gadi V P. Reddy
This is the peer reviewed version of the following article: see full citation below, which has been 
published in final form at https://dx.doi.org/10.1111/1744-7917.12548. This article may be used 
for non-commercial purposes in accordance with Wiley Terms and Conditions for Self-Archiving.
Shrestha, Govinda, and Gadi V. P. Reddy. "Field efficacy of insect pathogen, botanical and 
jasmonic acid for the management of wheat midge Sitodiplosis mosellana the impact on 
adult parasitoid ... populations in spring wheat." Insect Science (October 2017). 
DOI:10.1111/1744-7917.12548.
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Field efficacy of insect pathogen, botanical, and jasmonic
acid for the management of wheat midge Sitodiplosis
mosellana and the impact on adult parasitoid Macroglenes
penetrans populations in spring wheat
Govinda Shrestha and Gadi V. P. Reddy
Department of Research Centers, Western Triangle Agricultural Research Center, Montana State University, Conrad, Montana, USA
Abstract The wheat midge, Sitodiplosis mosellana, is a serious pest of wheat worldwide.
In North America, management of S. mosellana in spring wheat relies on the timely
application of pesticides, based on midge adults levels caught in pheromone traps or seen
via field scouting during wheat heading. In this context, biopesticides can be an effective
alternative to pesticides for controlling S. mosellanawithin an Integrated PestManagement
program.A field study using insect pathogenic fungusBeauveria bassianaGHA, nematode
Steinernema feltiae with Barricade polymer gel 1%, pyrethrin, combined formulations of
B. bassiana GHA and pyrethrin, Jasmonic acid (JA) and chlorpyrifos (chemical check)
was performed to determine to which extent they affect midge larval populations, kernel
damage levels, grain yield, and quality, and the impacts on adult parasitoid Macroglenes
penetrans populations. The results indicated that biopesticides JA and S. feltiae were the
most effective in reducing larval populations and kernel damage levels, and produced a
higher spring wheat yield when compared to the water control at both study locations (East
Valier and North Valier, Montana, USA). Increased test weight in wheat had been recorded
with two previous biopesticides at East Valier but not for North Valier, when compared over
water control. These results were comparable in efficacy to the chlorpyrifos. This study
also suggested that B. bassiana and pyrethrin may work synergistically, as exemplified by
lower total larval populations and kernel damage levels when applied together. This study
did not demonstrate the effect of any treatments onM. penetrans populations.
Key words biological control; biopesticides; entomopathogen; Integrated Pest
Management
Introduction
The wheat midge (also called the orange wheat blos-
sommidge), Sitodiplosis mosellana (Ge´hin) (Diptera: Ce-
cidomyiidae), a wheat (Triticum spp.) specific-herbivore,
is Palearctic in origin and that was introduced acciden-
tally in North America in the 1800s (Felt, 1912; Olfert
Correspondence: Gadi V. P. Reddy, Department of Research
Centers, Western Triangle Agricultural Research Center, Mon-
tana StateUniversity, 9546Old ShelbyRd, P.O.Box 656,Conrad,
MT 59425, USA. Email: reddy@montana.edu
et al., 2009). Over the last few decades, it has become a
wheat chronic pest in the Northern Great Plains, including
Minnesota, Idaho, North Dakota, Washington and Mon-
tana (Knodel & Ganehiarachchi, 2008; Stougaard et al.,
2014). Also, this pest is distributed widely in many other
parts of the world (Olfert et al., 2009). In Montana, S.
mosellana was first reported in 1990s, but damage to the
wheat crop in this region initially remained low, with only
periodic minor outbreaks. However, in 2006, an outbreak
occurred in north western Montana on spring wheat in
the Flathead County with estimated wheat losses over
$1.5 million in this county alone (Stougaard et al., 2014).
Wheat midge infestations generally reduce wheat yield
from 30%–40%; however, if the infestation is severe, the
yield loss can reach up to 100% (Blodgett, 2007). Un-
fortunately, in recent years, the presence of S. mosellana
appears to be expanding with outbreaks occurring in other
parts (such as northcentral and eastern) of Montana.
Wheat midge is typically univoltine insect pest species,
with mature larvae overwintering in the soil inside co-
coons. When temperatures begin to increase in the spring,
larvae leave their cocoons, pupate and emerge from soil
(Doane et al., 2002; Shanower, 2005). Immediately af-
ter emergence, female adults release sex pheromone (2S,
7R)-2, 7-nonadiyl dibutyrate) which attract males format-
ing (Gries et al., 2000). Mated females fly to find wheat
host plants for oviposition and they lay eggs on wheat
heads, usually in the evening and early morning. Eggs
hatch in 4–7 d, and larvae feed on the surface of newly de-
veloping kernels for 2–3 weeks, causing them to shrivel,
crack, or become distorted (Dexter et al., 1987). Third in-
star larvae drop from wheat heads to the soil, where they
burrow in and form cocoons, usually when rainfall occurs
(Olfert et al., 1985).
To date, chemical insecticides are the main control
method used against S. mosellana in North America. In-
secticides (e.g., organophosphate or pyrethroid) are usu-
ally applied to control adults since larvae are well pro-
tected inside wheat kernels. Insecticide applications are
made when the crop is at the heading stage, considered the
most susceptible stage towheat midge damage (Stougaard
et al., 2014). It is recommended to spray at the economic
threshold of one S. mosellana adult per 4–5 wheat heads
as seen in the evening, or when a pheromone trap catch
exceeds 120 midges/trap/d (Elliott, 1988; Gaafar, 2010;
Chavalle et al., 2014; Stougaard et al., 2014).
However, demand for alternative methods to control S.
mosellana populations has been recently stimulated due
to the increased risk of insecticide resistance development
from the repeated/heavy use of insecticides, and the con-
cerns associated with the environment and human health
(Koureas et al., 2012; Kim et al., 2017). Potential alter-
native methods for wheat midge control include the use
of resistant wheat varieties (Blake et al., 2014; Chavalle
et al., 2014) and natural enemies such as parasitoids, for
example, Macroglenes penetrans (Kirby) (Hymenoptera:
Pteromalidae), Euxestonotus error (Fitch) and Platy-
gaster tuberosula (Kieffer) (Hymenoptera: Platygastri-
dae) (Olfert et al., 2003; Shanower, 2005; Thompson &
Reddy, 2016), and predators (Floate et al., 1990; Holland
et al., 1996). Wheat midge resistant wheat varieties have
been developed in many parts of the world (e.g., Canada,
Europe andUS) and shown great potential for suppressing
S. mosellana population (Lamb et al., 2002; Blake et al.,
2014; Chavalle et al., 2017). Wheat variety resistance
to S. mosellana is linked to antixenosis (oviposition
deterrent activity) or antibiosis (larval death occurrence
due to presence of Sm1 gene) mechanisms (Lamb et al.,
2002; Blake et al., 2014; Chavalle et al., 2017). A further
potential alternative method is the use of biopesticides
including insect pathogens, botanicals and jasmonic acid
(JA) which can offer a safe and effective alternative
to chemical insecticides for controlling S. mosellana
within an Integrated Pest Management (IPM) program
(El-Wakeil et al., 2010; El-Wakeil & Volkmar, 2012).
Insect pathogens, for example, fungi and nematodes,
natural pathogens of insects, have been formulated and
commercialized as biopesticides. Fungi infect insect hosts
by direct penetration of host cuticles, invade hemocoel
and eventually kill the hosts within 6–7 d (Vega et al.,
2012). Nematode infective juveniles (IJs) enter insect
hosts through natural openings (mouth, spiracles and
anus), penetrate into the hemocoel and then release sym-
biotic bacteria that will kill the hosts within 2 d (Grewal
et al., 2006). Insect pathogens have been successfully ex-
amined or used against a variety of insect pest species
and considered as components of an IPM program (Chan-
dler et al., 2011; Shrestha et al., 2015; Portman et al.,
2016; Shapiro-Ilan et al., 2016). However, the effect of
insect pathogens on S. mosellana has received little atten-
tion, except for the study by Keller and Wilding (1985),
reporting that naturally occurring fungus Entomophthora
brevinucleateNov. (Zygomycota: Entomophthorales) was
pathogenic to adults in winter wheat fields in Switzerland.
Several botanical biopesticides have been developed
from plant extracts, especially from species of Rutaceae,
Lamiaceae, Meliaceae, and Asteraceae that can be toxic
and/or repellent to insect pests (Isman, 2006). The most
widely used or tested botanical products against a va-
riety of insect pests are pyrethrin and azadirachtin, ex-
tracted respectively from chrysanthemum flowers and
neem trees (Isman, 2006). These two products have been
tested against S. mosellana in Germany and Finland but
reported with only limited success (Kurppa & Husberg,
1989; El-Wakeil et al., 2013).
Jasmonic acid, a natural plant hormone derived from
linolenic acid via the octodecanoid pathway, is released by
plants when they are attacked by insect herbivores, which
yields increased production of compounds involved in
resistance to herbivores (Thaler, 1999a,b; Pickett et al.,
2006). Exogenous application of JA has been shown
to induce resistance to various insect pests in crops
such as cotton (against cotton aphids Aphis gossypii
[Glover]) (Omer et al., 2000), tomato (against potato
aphid, Macrosiphum euphorbiae [Thomas]) (Cooper
& Goggin, 2005), rice (against brown planthopper,
Nilaparvata lugens [Sta˚l]) (Senthil-Nathan et al., 2009),
and wheat (against Rhopalosiphum padi [L.]) (Quiroz
et al., 1997). In Germany, JA application has shown to
induce resistance against S. mosellana in fields of winter
wheat plants, thereby protecting kernels from damage
and enhancing yield (El-Wakeil et al., 2010).
In this field study, we evaluated several commercially
available biopesticides for their abilities to reduce S.
mosellana larval population, kernel damage levels and
improve yield and quality of spring wheat. This effort
is a first step in an attempt to identify suitable biopes-
ticide products for wheat midge control. The biopesti-
cides selected for this field study were: (1) the insect
pathogenic fungusBeauveria bassiana (Bals.)Vuill. GHA
(Mycotrol ESO R©) (Ascomycota: Hypocreales), (2) the
nematode Steinernema feltiae (Nematoda: Rhabditida)
(Scanmask R©), (3) JA, (4) pyrethrin (PyGanic EC R© 1.4),
and (5) combined formulations of B. bassiana GHA and
pyrethrin (Xpectro OD R©). The Xpectro product was con-
sidered for this study since it has demonstrated some syn-
ergistic effects on control of other insect pests, for exam-
ple, alfalfaweevilsHypera posticaGyllenhal (Coleoptera:
Curculionidae) and wheat head armyworms Dargida dif-
fusaWalker (Lepidoptera: Noctuidae) (Reddy et al., 2016;
Reddy & Antwi, 2016). Chlorpyrifos (Lorsban R©) was
included as a reference pesticide chemical because this
pesticide is widely used in spring wheat by growers in
Montana and other parts of world to control S. mosel-
lana populations (Chavalle et al., 2014; Stougaard et al.,
2014). In addition, the impact of these biopesticides on
adult population levels of the parasitoidM. penetranswas
examined.
Materials and methods
Locations of spring wheat field trials
The experiments were conducted at three locations:
North Valier (N 48° 35.192, W112° 21.169), East Va-
lier (N 48° 30.206, W112° 14.350) and East Conrad (N
48° 14. 403, W111° 60.119), in the Golden Triangle area
of Montana, USA. This area is an important cereal grow-
ing region in Montana and the experiment locations were
known to have had high levels of S. mosellana infestation
in previous years (Pestweb Montana, 2017). The com-
mon cropping system in this area is cereal crops grown
year after year or a fallow (noncrop) period following 1–2
years cereal crop rotation, and the crop lands are mostly
nonirrigated (McVay et al., 2010). Winter wheat is usu-
ally seeded in September with seeding rate of 100–150 kg
seeds/ha, while spring wheat is seeded from April to May
with 150–220 kg seeds/ha (McVay et al., 2010). Average
grain yields recorded from 2005 to 2015were: 2000–2800
kg/ha for winter wheat and 1500–2600 kg/ha for spring
wheat dryland (National Agricultural Statistics Service,
2016). Further information regarding cereal crops man-
agement practices can be obtained from McVay et al.
(2010).
A randomized complete block design (RCBD)with four
replicates per treatment was used. Plots were 8 m × 4 m
and separated from each other by 1mbuffer zones to avoid
cross contamination of treatments. The experiments were
performed in fields planted with the wheat midge sus-
ceptible spring wheat cultivar “Duclair” (Lanning et al.,
2011) in 2016.
Monitoring wheat midge flight behavior with
pheromone traps
To determine the best date for biopesticide application,
the abundance of S. mosellana adult males was monitored
using pheromone traps, as per Bruce et al. (2007). Delta
trapswere baitedwith pheromone lures ([2S, 7S]-nonadiyl
dibutyrate) (Great Lakes IPM, Inc., Vestaburg, MI, USA)
and attached above the sticky card inserts (Scentry R©).
They were installed in experimental fields at a rate of one
trap per field to monitor S. mosellana adult populations.
Traps were painted green to decrease nontarget insects
catch, placed 20 m inside from the field edges, and the
height was adjusted weekly to match the height of the
wheat canopy (Thompson&Reddy, 2016). The traps were
set on June 10, 2016 at each experimental location and
monitored nearly every day from Monday to Friday until
the first week of August.
Application of biopesticide products
Commercial formulations of five biopesticide prod-
ucts were used for the study. Mycotrol ESO R© and Xpec-
tro OD R© were obtained from Lam International (Butte,
MT, USA), Scanmask from Sierra Biological Inc. (Pio-
neer, CA, USA), jasmonic acid from Sigma–Aldrich (St.
Louis, MO, USA) and PyGanic EC R© 1.4 (pyrethrin) from
McLaughlin Gormley King (Minneapolis, MN, USA).
Biopesticide product rates were based on the manufac-
turer’s recommendations (Table 1).
All biopesticide products were thoroughly mixed with
tap water to obtain the desired concentrations (Table 1).
However, for JA and Scanmask preparations, 1 mg JAwas
dissolved in 1 mL acetone and then dispersed in water to
give a solution of 1 mL JA per liter of water (El-Wakeil
et al., 2010), while 1% Barricade polymer gel (Barricade
Table 1 Biopesticide products and rate of application in each treatment.
Treatment Active ingredient Concentration Amount of each product
Water (control) – – –
PyGanic EC R© Pyrethrin 1.4% (w/v) 4.167 ml/L 1.69 L/ha
Mycotrol ESO R© Beauveria bassiana GHA 10.9% 2.50 ml/L 1.02 L/ha
Xpectro R© OD (2.11 × 1010 viable spores/mL) (w/v) B.
bassiana GHA (1%–2%) + Pyrethrin
(0.75%) (w/v)
2.5 ml/L 1.02 L/ha
Barricade and Scanmask Barricade polymer gel and
Steinernema feltiae
Barricade polymer gel 1% +
300 000/m2 nematode
3 × 109 nematodes/ha
Jasmonic acid Jasmonic acid (w/v) 1 mg/L 408 mg/ha
Lorsban R© (chemical
check)
Chlorpyrifos 48% (w/v) 4. 00 mL/L 1.63 L/ha
International, Inc., FL, USA) was added to mixture of
Scanmask and tap water (Table 1). This percentage of gel
mixed with nematode S. feltiae improved control of other
foliar insect pests such as: wheat stem sawflies Cephus
cinctusNorton (Hymenoptera: Cephidae) and flea beetles
Phyllotreta cruciferae Goeze (Coleoptera, Chrysomeli-
dae) (Antwi & Reddy, 2016; Portman et al., 2016). Two
controls were included in the study. A water treatment
served as a negative control (control) and chlorpyrifos
(Lorsban R©) (Dow Agro Science LLC, Indianapolis, IN,
USA) served as a chemical check.
All biopesticide products, plus the two controls, were
applied on the same date at all field experimental trial
locations. However, the East Conrad locationwas not used
for this study in 2016 due to very low incidence of S.
mosellana adult populations based on a pheromone trap
count and the springwheatwas no longer at the susceptible
stage (G. Shrestha personal observation). Treatmentswere
applied using a SOLO backpack sprayer (SOLO, Newport
News, VA,USA). The sprayer was calibrated to deliver ca.
408Lmixture/ha based on nozzle flow andwalking speed.
The plots were sprayed on June 29, 2016, when the wheat
plants were at a susceptible stage to midges (early boot)
and coincided with the peak emergence of wheat midge
adults. Scoutingwas performed to determinewheatmidge
threshold levels for treatment applications. Spraying was
carried out from 7 to 9 pm, when midge adult activity
appeared to be high in the fields.
Wheat midge larvae in white traps
White traps were used to assess the wheat midge larval
populations in the treatment plots, using amethod adapted
from El-Wakeil et al. (2010). The traps, constructed of
plastic dishes (diameter 125 mm; height 65 mm), were
placed in the soil at the base of wheat tillers or stands
in each plot. Each trap was partly filled with tap water
(100–150 mL) and three to four drops of soap detergent.
Four days after treatment, two traps were placed in each
treatment plot. Samples were collected from traps every
week, brought immediately to the laboratory and exam-
ined under a binocular or stereomicroscope to determine
the presence of S. mosellana larvae.
Midge-damaged wheat kernels
Wheatmidge-damaged kernels in the biopesticide treat-
ments and the control plots were assessed when the wheat
kernels were almost ready to harvest. Ten wheat heads
were randomly sampled from each treatment plot, placed
in a brown paper bag, and transported immediately to the
laboratory. Wheat heads were subsequently threshed indi-
vidually by hand to determine the total number of wheat
kernels and the number of midge-damaged kernels per
wheat head. Midge-damaged kernels were characterized
based on criteria (such as shriveled, cracked or deformed
kernels) reported by Knodel and Ganehiarachchi (2008)
and Stougaard et al. (2014).
Macroglenes penetrans adult populations
This study examined that biopesticide treatments and
controls had a significant impact on M. penetrans adult
populations, a wheat midge parasitoid which has recently
been reported in the Golden Triangle area of Montana
(Thompson & Reddy, 2016). A sweep net was used to
estimate the adult parasitoid populations. Sweeping was
conducted with a standard sweep net, and 20 sweeps
were made from each treatment plot. The sampling was
performed the day before treatment and, 3, 7, and 15 d
after treatment.
Yield and quality of wheat kernels
A Hege 140 plot combine was used to harvest the
wheat grains from treatment plots. The precaution was
used to avoid the borders and any overlap of treatment
effects on wheat yield and quality. Each plot was trimmed
from edges, plot length was measured and the wheat grain
threshed from the center of each plot. Wheat grains were
cleanedwith a seed processor (Almaco,Nevada, IA,USA)
andweighed on a scale to determine yield. Test weightwas
measured on a Seedburo test weight scale. The protein and
moisture percentages of seed was determined with NIR
grain analyzer IM 9500 (Perten Instruments, Springfield,
IL, USA).
Statistical analysis
One-way analysis of variance (ANOVA)was performed
to examine the effect biopesticide treatments had onwheat
midge kernel damage levels, yield and quality (testweight,
protein % and moisture %) of spring wheat compared to
the water and chlorpyrifos controls at each study loca-
tion. A normal quantile–quantile plot was performed to
confirm normality of data and equality of variance. No
transformation of data was required to achieve normal
distribution. Tukey’s post hoc test was used for multiple
comparisons among the treatment means. Likewise, for
the sweep net data set, one-way ANOVA was performed
to examine the effect of treatments on total populations of
M. penetrans adults at each study location.
The water traps data were found to be nonnormally
distributed even after the log transformation, and the non-
parametric one-way analysis of variance (Kruskal–Wallis
test), was consequently used to examine treatment ef-
fects onwheatmidge larval populations per sampling time
across the treatments on each sampling date or on total
midge larval populations. A Mann–Whitney U-test was
used as a post hoc test for multiple comparisons between
the means followed by a Bonferroni correction to adjust
the probability (α = 0.01). The data were analysed using
the software statistical package R 2.15.1 (R Development
Core Team, 2017).
Results
Wheat midge adult activity based on pheromone trap
catch and scouting
At all three field locations, the flight activity of wheat
midge adults began at about the same date, June 15–21,
in 2016 (Fig. 1). Within 2 weeks, adult activity acceler-
Fig. 1 Adult wheat midge Sitodiplosis mosellana populations
captured by pheromone traps at the three study locations in
Montana.
ated sharply at East Valier, increased gradually at North
Valier and remained very low at East Conrad (Fig. 1).
The economic threshold level of adult activity that war-
ranted the application of pest control measures in relation
to susceptible stages of spring wheat occurred at only
two (East Valier and North Valier) of the three locations
(Fig. 1). During scouting, the numbers of S. mosellana
adults recorded were>2 flying adults per four–five wheat
heads both in East Valier and North Valier locations while
nearly zero at the East Conrad location. The total cumu-
lative numbers of S. mosellana male adults captured in
pheromone traps at East Valier, North Valier, and East
Conrad locations were: 2397, 855, and 121, respectively
(Fig. 1).
Larval populations
Regardless of treatments or study locations, noS.mosel-
lana larvae were caught in white traps for the first three
sampling dates, with the exception of a few larvae (0.25–
0.50) in the chlorpyrifos and S. feltiae treatments at the
East Valier location, but these differences were not sig-
nificant (χ2 = 9.36; df = 6; P > 0.05, Kruskal–Wallis
test) (Table 2). However, on the fourth and fifth sampling
dates, wheat midge larvae were observed in all treatment
plots in both trial locations. Significant differences in
S. mosellana larvae were recorded between treatments at
the fourth (χ2 = 23.42; df = 6; P < 0.001, Kruskal–
Wallis test) and fifth sampling (χ2 = 18.43; df = 6;
P < 0.01, Kruskal–Wallis test) dates on the East Va-
lier location. In contrast, significant differences in larvae
Table 2 Effects of biopesticides application on total wheat midge Sitodiplosis mosellana larval populations (mean ± SE), recorded in
white water traps (two traps per plot) in spring wheat fields at the two study locations of Montana.
Wheat midge larvae (Mean ± SE)
Treatment
Jul 7 Jul 14 Jul 21 Jul 28 Aug 5 Total larvae
North Valier
Water (control) 0.00 ± 0.00 0.00 ± 0.00 0.00 ± 0.00 5.50 ± 0.65a 1.25 ± 0.48a 6.75 ± 0.85a
Steinernema feltiae 0.00 ± 0.00 0.00 ± 0.00 0.00 ± 0.00 1.00 ± 0.41b 0.75 ± 0.25a 1.75 ± 0.48c
Jasmonic acid 0.00 ± 0.00 0.00 ± 0.00 0.00 ± 0.00 2.25 ± 0.48bc 0.75 ± 0.25a 3.00 ± 0.70bc
Beauveria bassiana GHA 0.00 ± 0.00 0.00 ± 0.00 0.00 ± 0.00 4.75 ± 0.63a 1.25 ± 0.48a 6.00 ± 0.91ab
B. bassiana GHA + pyrethrin 0.00 ± 0.00 0.00 ± 0.00 0.00 ± 0.00 1.75 ± 0.25b 0.75 ± 0.25a 2.50 ± 0.29c
Pyrethrin 0.00 ± 0.00 0.00 ± 0.00 0.00 ± 0.00 4.50 ± 0.29a 2.25 ± 0.48a 6.75 ± 0.63a
Chlorpyrifos (chemical check) 0.00 ± 0.00 0.00 ± 0.00 0.00 ± 0.00 0.50 ± 0.29bc 0.50 ± 0.50a 1.00 ± 0.70c
P value NS NS NS 0.001 NS 0.001
East Valier
Water (control) 0.00 ± 0.00 0.00 ± 0.00 0.00 ± 0.00 8.25 ± 0.63a 4.25 ± 0.48a 12.50 ± 1.04a
Steinernema feltiae 0.00 ± 0.00 0.00 ± 0.00 0.50 ± 0.29 2.50 ± 0.28b 1.25 ± 0.62ab 4.25 ± 0.25bc
Jasmonic acid 0.00 ± 0.00 0.00 ± 0.00 0.00 ± 0.00 2.50 ± 0.29b 0.75 ± 0.25b 3.25 ± 0.25c
Beauveria bassiana GHA 0.00 ± 0.00 0.00 ± 0.00 0.00 ± 0.00 7.50 ± 1.19a 2.50 ± 0.65ab 10.00 ± 0.91ab
B. bassiana GHA + pyrethrin 0.00 ± 0.00 0.00 ± 0.00 0.00 ± 0.00 4.25 ± 0.48ab 2.25 ± 0.48ab 6.50 ± 0.29bc
Pyrethrin 0.00 ± 0.00 0.00 ± 0.00 0.00 ± 0.00 4.75 ± 0.65a 3.50 ± 0.29a 8.25 ± 0.48ab
Chlorpyrifos (chemical check) 0.00 ± 0.00 0.00 ± 0.00 0.25 ± 0.25 1.75 ± 0.62b 0.75 ± 0.48b 2.75 ± 0.75c
P value NS NS NS 0.001 0.01 0.001
Note: NS indicates the no significant. Mean values within columns bearing the different letters within each location are significantly
different (Mann–Whitney U-tests followed by Bonferroni correction [α = 0.01]).
numbers were found only on the fourth sampling date
(χ2 = 22.82; df = 6; P < 0.001, Kruskal–Wallis test)
but without effect on the fifth sampling date (χ2 = 8.70;
df= 6; P> 0.05, Kruskal–Wallis test) in the North Valier
location.
On the fourth sampling date at the East Valier location,
among biopesticide treatment plots, significantly fewer S.
mosellana larvae were recorded for the treatments with
S. feltiae (2.50 ± 0.28) and JA (2.50 ± 0.29), while the
remaining treatments showed no significant differences
compared to the water control (8.25 ± 0.63) (Table 2).
On the fifth sampling date, however, significantly fewer
S. mosellana larvae were found only in the JA treatment
(0.75± 0.25) compared to the water control (4.25± 0.48)
(Table 2).
Similarly, at the North Valier location, significantly
fewer S. mosellana larvae were recorded for the treat-
ments with S. feltiae (1.00 ± 0.41) and JA (2.25 ±
0.48) compared to the water control (5.50 ± 0.65) on
the fourth sampling date (Table 2). Moreover, the com-
bined application of B. bassiana and pyrethrin also re-
duced larval populations, but this effect was not observed
when B. bassiana or pyrethrin was applied individually
(Table 2).
With respect to the total larval populations, the study
showed that biopesticide treated plots with JA, S. feltiae
and combined application of B. bassiana and pyrethrin
had significantly fewer larvae than the water treatment
at both study locations; East Valier (χ2 = 24.75; df =
6; P < 0.001, Kruskal–Wallis test) and North Valier
(χ2 = 21.67; df = 6; P < 0.001, Kruskal–Wallis test).
Other biopesticide treatments were not significantly dif-
ferent from water control (Table 2).
Midge-damaged wheat kernels
In overall, higher wheat kernel damage inflicted by S.
mosellana larvae was observed at East Valier in contrast
to the North Valier location (Fig. 2). Mean levels of ker-
nel damage in biopesticides/controls treated plots ranged
from 20% to 48% for East Valier location and from 11%
to 23% for North Valier location (Fig. 2). However, this
study showed that biopesticide treatments had significant
impact on wheat midge kernels damage at both study lo-
cations: East Valier (df = 6,258; F = 11.7; P < 0.001)
and North Valier (df = 6,267; F = 7.40; P < 0.001).
Interestingly, among the biopesticide treatment plots,
the significantly lower kernel damage percentages were
Fig. 2 Effect of biopesticides application on the percentage of
damaged kernels inflicted by wheat midge Sitodiplosis mosel-
lana larvae in spring wheat (cv. Duclair) at the two study loca-
tions in Montana. Bars bearing the same uppercase or lowercase
letters are not significantly different (Tukey’s test, P > 0.05).
observed when wheat plots were treated with JA, S. fel-
tiae or combined application of B. bassiana and pyrethrin
over water control plots at both study locations (Fig. 2). In
contrast, the other two biopesticide treatments; pyrethrin
and B. bassiana did not protect the wheat kernels from
wheat midge larval damage and the kernel damage levels
were similar to water treated plots (Fig. 2).
Yield
To assess the impact of biopesticide treatments onwheat
grain yield, the obtained yield data of each biopesticide
treatment plot was compared with yield from the wa-
ter (control) and chlorpyrifos (chemical check) treatment
plots. The results showed that biopesticide treatments had
a significant impact on wheat grain yield at both study
locations: East Valier (df = 6,21; F = 8.03; P < 0.001)
and North Valier (df = 6,21; F = 11.27; P < 0.001).
Grain yield at the East Valier location was significantly
higher for treatments with the S. feltiae or JA as compared
to the treatment with water control (Fig. 3). Moreover,
the yield of these two biopesticide treatments was simi-
lar with chlorpyrifos treatment yield, without significant
difference (Fig. 3). In contrast, wheat plots treated with
B. bassiana, pyrethrin or their combined treatments had
not produced higher grain yield when compared over wa-
ter sprayed plots (Fig. 3).
Fig. 3 Effect of biopesticides application on yield of wheat
midge Sitodiplosis mosellana infested springwheat (cv. Duclair)
at the two study locations in Montana. Bars bearing the same
uppercase or lowercase letters are not significantly different
(Tukey’s test, P > 0.05).
Concerning yield results from North Valier location,
similarly the treatments with JA and S. feltiae produced
the higher grain yields compared to water control treat-
ment (Fig. 3). In addition, higher grain yields were fur-
ther recorded when B. bassiana and pyrethrin applied
together in comparison to when they applied individually
(Fig. 3).
Quality
Test weight, protein % and moisture % were examined
as a part of wheat kernel quality to determine whether
the biopesticide treatments had an effect on these param-
eters compared to the water and chlorpyrifos controls.
This study demonstrated that treatments had a signifi-
cant impact in a test weight at the East Valier location
(df = 6,21; F = 8.96; P < 0.001) while without ef-
fect at North Valier (df = 6,21; F = 2.26, P > 0.05)
(Table 3). The biopesticide treatments with JA (796.81
± 2.25) and S. feltiae (790.33 ± 6.66) had significantly
higher test weights while the remaining treatments had
no significant difference, when compared to the water
control (748.81 ± 4.03). Overall, test weight across treat-
ments varied from 731 to 796 (kg/cubic meter) and 762
to 800 (kg/cubic meter) respectively at East Valier and
North Valier locations (Table 3).
Table 3 Effect of biopesticides application on some quality parameters of wheat midge Sitodiplosis mosellana infested spring wheat
(cv. Duclair) at the two study locations of Montana.
Quality parameters (Mean ± SE)
Treatment
Test weight (kg/m3) Protein % Moisture %
North Valier
Water (control) 762.01 ± 14.71a 16.72 ± 0.22a 10.25 ± 0.01a
Steinernema feltiae 799.74 ± 7.34a 17.09 ± 0.28a 10.32 ± 0.03a
Jasmonic acid 794.65 ± 6.01a 17.05 ± 0.26a 10.27 ± 0.04a
Beauveria bassiana GHA 780.57 ± 6.51a 17.09 ± 0.28a 10.26 ± 0.03a
Beauveria bassiana GHA + pyrethrin 791.58± 5.35a 16.72 ± 0.32a 10.25 ± 0.04a
Pyrethrin 789.30 ± 6.65a 16.90 ± 0.27a 10.30 ± 0.03a
Chlorpyrifos (chemical check) 789.40 ± 4.54a 16.95 ± 0.16a 10.26 ± 0.03a
East Valier
Water (control) 748.14 ± 4.03c 16.61 ± 0.13a 10.57 ± 0.02a
Steinernema feltiae 790.33 ± 6.66ab 16.36 ± 0.48a 10.61 ± 0.03a
Jasmonic acid 796.81 ± 2.25ab 16.52 ± 0.37a 10.53 ± 0.04a
Beauveria bassiana GHA 731.13 ± 13.32bc 16.75 ± 0.64a 10.49 ± 0.05a
Beauveria bassiana GHA + pyrethrin 752.01 ± 9.08bc 17.23 ± 0.15a 10.51 ± 0.03a
Pyrethrin 760.90 ± 11.56abc 17.10 ± 0.46a 10.50 ± 0.03a
Chlorpyrifos (chemical check) 794.13 ± 8.71ab 17.45 ± 0.27a 10.50 ± 0.02a
Note: Mean values within columns bearing the same letters within each location are not significantly different (Tukey’s test, P > 0.05).
There were no significant differences among biopesti-
cide treatments or controls in protein % or moisture % at
either study location: East Valier (protein: df = 6,20; F =
0.52; P > 0.05; moisture: df = 6,20; F = 0.95; P > 0.05)
and North Valier (protein: df = 6,20; F = 0.74; P > 0.05
andmoisture: df= 6,20;F= 0.60;P> 0.05). The average
protein and moisture were 16%–17% and 10%–11%,
respectively, across treatments or locations (Table 3).
Macroglenes penetrans adult populations
Regardless of locations, biopesticide or chlorpyrifos
treatments had no significant impact on total population
of M. penetrans adults: East Valier (df = 6,21; F = 0.54;
P> 0.05) andNorthValier (df= 6,21;F= 2.15;P> 0.05)
locations. The total mean number of parasitoid adults per
treatment plot ranged from 1 to 3 at both study locations
(Fig. 4).
Discussion
The results of this field based study indicated that biopes-
ticide products JA and S. feltiae with 1% Barricade poly-
mer gel have the ability to reduce S. mosellana larval
populations, kernel damage levels and to increase grain
yield of spring wheat when compared to the water control
treatment at both study locations East Valier and North
Fig. 4 Effect of biopesticides application on totalMacroglenes
penetrans adult populations. Post application data (3, 7, and 15
d after treatments) were merged together for statistical analysis.
Bars bearing the same uppercase or lowercase letters are not
significantly different (Tukey’s test, P > 0.05).
Valier. Increased test weight in wheat grains were also
recorded for the plots treated with JA and S. feltiae at
the East Valier location but not at the North Valier loca-
tion, when compared over water control treatment. The JA
and S. feltiae results were comparable in efficacy to the
standard pesticide, chlorpyrifos. This study also suggested
that B. bassiana and pyrethrin may work synergistically
as exemplified by lower total larval population and higher
kernel protection when they were both used together, but
without effects when applied individually. This study did
not conclude the effect of any treatments including chlor-
pyrifos on wheat midge parasitoid adults M. penetrans
population levels.
Various methods have been employed to estimate the
larval populations of S. mosellana in spring or winter
wheat crop fields when examining the efficacy of chemi-
cal insecticides, biopesticides, or pest pressure in the fol-
lowing year (Doane et al., 1987; El-Wakeil et al., 2010;
Gaafar et al., 2011; Chavalle et al., 2014). For exam-
ple, Chavalle et al. (2014) determined the impact of sev-
eral chemical insecticides on the larval populations of S.
mosellana based on the dissection of wheat heads fol-
lowed by counting the larvae before they dropped from
wheat heads onto the soil. Another method used was to
collect soil samples from S. mosellana-infested fields be-
fore (spring) or after (fall) crop harvest and wash samples
to determine the number of larvae in fields to better pre-
dict pest pressure following year (Doane et al., 1987). In
addition, white traps have also been effectively used to
estimate larval populations of S. mosellana while ascer-
taining the efficacy of chemical or biopesticide products
(El-Wakeil et al., 2010; Gaafar et al., 2011; El-Wakeil &
Volkmar, 2012). White traps can be installed at the soil
surface near the base of wheat tillers or stands to catch
larvae migrating from wheat heads to the soil at the end
of the growing season.
Our data support previous studies that have found white
traps could be used to estimate larval populations in wheat
midge-infested fields. As predicted, S. mosellana larvae
were recorded mostly at the fourth and fifth sampling
dates regardless of locations or treatments since rainfall
occurred 2–3 d prior to both samplings (NRCS, 2016) and
the precipitation is known to trigger larvae to fall onto
the soil from wheat heads at the end of cropping season
(El-Wakeil et al., 2010; Thompson & Reddy, 2016).
In our study, comparatively higher S. mosellana larval
populations were recorded in white traps at the East Valier
than at the North Valier. This observation was supported
by the pheromone trap data, with sixteen hundred male
adults recorded at the East Valier, but only two hundred
at the North Valier during the most susceptible stages of
wheat. The treatments clearly showed the significant im-
pacts on total larval populations of S. mosellana on spring
wheat and the significantly fewer larvae were found for
plots treated with JA, S. feltiae and combined formula-
tion of B. bassiana and pyrethrin when compared to the
water treatment at both study locations. Our results for
JA resemble the findings of El-Wakeil et al. (2010), who
reported significantly lower numbers of S. mosellana lar-
vae in winter wheat fields sprayed with JA compared to
the untreated plot. No previous reports are available on
the impact to S. mosellana larval populations of the other
biopesticides examined in our trial. The lack of individ-
ual effects of B. bassiana or pyrethrin applications on
larval populations or other studied parameters could be
due to mode of action and presumably with these biopes-
ticides inability to reduce the daily fecundity of wheat
midge adults. Furthermore, abiotic factors (e.g., sunlight,
temperature) may have contributed to their lack of ef-
fect, since the previous studies have shown that fungus
or pyrethrin half-life can decline rapidly (2 h to 3 d) in
outdoor environments (Inglis et al., 1995; Angioni et al.,
2005; Jaronski, 2010).
Determining the ability of chemical insecticide or
biopesticide products to protect wheat kernels fromwheat
midge larval damage is fundamental for determining po-
tential control options (Elliott, 1988; El-Wakeil et al.,
2010; Chavalle et al., 2014). Several studies have ex-
amined the ability of various chemical insecticide or
biopesticide products to protect spring or winter wheat
kernels from S. mosellana larval damage in the Europe
and North America (Elliott, 1988; El-Wakeil et al., 2010;
El-Wakeil et al., 2013; Chavalle et al., 2014). For ex-
ample, Elliott (1988) reported that chlorpyrifos and en-
dosulfan protected 60%–75% of wheat kernels from S.
mosellana larval damage. This finding is similar to our
chlorpyrifos treatment results from both study locations.
Chavalle et al. (2014) and El-Wakeil et al. (2013) also in-
dicated higher wheat kernel protection from chlorpyrifos
but did not quantify the level of kernel protection in their
studies.
In a previous study, El-Wakeil et al. (2010) demon-
strated that exogenous application of JA on winter wheat
crop provided more than 75% protection to kernels com-
pared to the water control treatment. Our results are in line
with this finding, with more than 80% of the kernels pro-
tected from S. mosellana larval damage by the application
of JA at both of our study locations. Although the possi-
ble mechanisms that could have impacted such enhanced
protection from wheat midge larvae are fairly unknown, it
was likely that the application of JA induced spring wheat
plants to release volatilies or produce secondary metabo-
lites that acted as a repellent to S. mosellana (Senthil-
Nathan et al., 2009; El-Wakeil et al., 2010). Furthermore,
when wheat midges were exposed to JA treated wheat
plants, adult fecundity and larval feeding may have been
further reduced, since it has been demonstrated with other
insect pest species (Omer et al., 2000; Cooper & Goggin,
2005; Senthil-Nathan et al., 2009).
This study found that the insect pathogenic nematode
(IPN) S. feltiaewith 1%Barricade polymer gel effectively
protected wheat kernels from S. mosellana larval feeding.
IPNs have been most successfully used against different
soil inhabiting insect pest species (Kaya & Gaugler,
1993). However, with the development of a suitable ad-
juvant (Barricade polymer gel) that can protect infective
juveniles from ultraviolet rays or extend their survival on
aboveground foliage (Antwi & Reddy, 2016; Shapiro-Ilan
et al., 2016); IPNs can now be considered for use against
aboveground crop insect pests as well (Antwi & Reddy,
2016; Portman et al., 2016; Shapiro-Ilan et al., 2016).
Among the several nematode species, S. feltiae has been
recognized to have many advantages including a broad
host range, high virulence, adaptability to a wide range of
temperatures (10–30 °C) and an ability to seek their target
host (Gaugler et al., 1989). Furthermore, in Montana, S.
feltiae has recently been found to be the most effective
nematode species against a wide range of important
foliar insect pests including wheat stem sawflies and flea
beetles when applied in conjunction with 1% Barricade
under field conditions (Antwi & Reddy, 2016; Portman
et al., 2016). Thus, our findings and those of these
previous field studies indicate that S. feltiae has the
potential to be used against several foliar insect pests in
Montana and can be combined with many IPM programs.
In contrast, this study suggests that separate application
of B. bassiana or pyrethrin will be ineffective in reducing
kernel damage levels caused by S. mosellana larvae. This
is corroborated by the fact that no information has been
found in the literature on the successful use of B. bassiana
or pyrethrin in relation to S. mosellana management.
Although both biopesticides can be disregarded for use
in wheat midge management when applied separately,
the significantly higher kernel protection provided
by their combined application at the North Valier
location suggests that they might have a place in IPM
programs.
In addition to lower levels of wheat kernel damage,
higher grain yields were found when wheat plots were
treated with JA and S. feltiae compared over the wa-
ter control treatment, at both study locations. A similar
relationship between kernel damage and yield data has
been reported in several previous studies (Elliott, 1988;
El-Wakeil et al., 2010; El-Wakeil et al., 2013; Chavalle
et al., 2014).
With respect to the parasitoid study, our results could
not conclude directly that treatments have any negative
impacts onM. penetrans adults’ population. This could be
due to the low parasitoid population levels recorded irre-
spective of treatments/locations or because of parasitoids
mobile nature that relatively small research plots could
be insufficient on determining these impacts. In contrast,
there was also the possibility that parasitoids could be un-
affected by chlorpyrifos or biopesticide treatments since
the emergence of M. penetrans usually occurred 10 d
after the S. mosellana with the highest peak emergence
(Thompson&Reddy, 2016). Based on this finding and the
nature of wheat midge and parasitoid emergence patterns,
it warrants further laboratory and long-term field inves-
tigations that determine whether the direct and indirect
exposure to synthetic insecticide or biopesticide have any
negative impact on the parasitoid biology and population
development.
In summary, our results indicate that the biopesticides
JA and S. feltiae with 1% Barricade polymer gel would
be suitable for the management of wheat midge in spring
wheat in Montana. However, further cost/benefit analysis
study is needed to determine if the application of these
biopesticide products is economical and sustainable for
spring wheat growers in Montana.
Acknowledgments
The authors would like to thank Cory Crawford, Jody
Habel, and Ramsey Offerdal for providing the field sites
to conduct field trails. Appreciation is also extended to
special project coordinator Dan Picard (WTARC, Mon-
tana State University) for his help in connecting spring
wheat growers with research team members, and sum-
mer intern Connie Miller and research assistant Debra
Miller (WTARC,Montana State University) for their hard
work in processing wheat midge kernel damage sam-
ples. This work was supported by the Montana Wheat
and Barley Committee and USDA National Institute of
Food and Agriculture, Multi-state Project S-1052 and
the Working Group on Improving Microbial Control of
Arthropod Pests Covering Research in Montana [acces-
sion# 232056].
Disclosure
The authors disclose no potential conflicts of interest as-
sociated with this manuscript.
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Manuscript received April 2, 2017
Final version received August 24, 2017
Accepted September 21, 2017
C© 2017 Institute of Zoology, Chinese Academy of Sciences, 00, 1–13