Journal of Integrative Agriculture 2021, 20(3): 804–814

Available online at www.sciencedirect.com

ScienceDirect

RESEARCH ARTICLE

Ovipositional responses of Spodoptera frugiperda on host plants

provide a basis for using Bt-transgenic maize as trap crop in China

HE Li-mei1, 2*, ZHAO Sheng-yuan1*, GAO Xi-wu2, WU Kong-ming1

1
State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of
Agricultural Sciences, Beijing 100193, P.R.China
2
College of Plant Protection, China Agricultural University, Beijing 100193, P.R.China

Abstract
Spodoptera frugiperda, the pest fall armyworm (FAW), is widespread in more than 100 countries. To date, planting insect-
resistant transgenic crops is one of the main control methods in its native countries. In this study we evaluated Bt-transgenic
maize (Bt maize) and non-transgenic (conventional) maize and six other host plants in greenhouse pot experiments and
field trials for oviposition preference by the Chinese populations of FAW. In laboratory trials, female moths preferred to
oviposit on maize with no significant preference between conventional and Bt maize. However, after conventional and
transgenic maize were exposed to FAW larvae and damaged, oviposition was significantly higher on transgenic maize than
on the conventional one. Field trials showed that for plants less damaged at an early stage (seedling stage), oviposition of
FAW on transgenic and conventional maize was significantly higher than that on wheat, sorghum, foxtail millet, peanut and
soybean while showing no significant difference between transgenic or conventional maize. FAW adults mainly laid eggs on
Bt maize, while the larval density and leaf damage rating or percentage of damaged plants were significantly lower than on
conventional maize. Larval density and its damage on conventional maize were significantly higher than that on Bt maize
and the other five hosts. Thus, maize is a highly preferred and suitable host for S. frugiperda feeding and ovipositing, and
Bt maize can be used as trap crop to protect other crops.

Keywords: fall armyworm, oviposition behavior, trap crop, Bt maize

1. Introduction

Native to tropical and subtropical America, the fall armyworm

(FAW), Spodoptera frugiperda (J. E. Smith) (Lepidoptera:
Noctuidae), is a relatively new invasive agricultural pest
Received 26 March, 2020 Accepted 6 July, 2020
HE Li-mei, E-mail: helimei91@163.com; ZHAO Sheng-yuan, in China that quickly became widespread since its first
E-mail: zhaosy90@126.com; Correspondence WU Kong-ming, sighting in December 2018 (Smith and Abbott 1797; Luginbill
E-mail: wukongming@caas.cn
* 1928; Sparks 1979; Johnson 1987; Jiang et al. 2019; Sun
These authors contributed equally to this study.
et al. 2021). As a typical polyphagous pest, S. frugiperda
© 2021 CAAS. Published by Elsevier B.V. This is an open
is highly adaptable to a range of different host plants. Its
access article under the CC BY-NC-ND license (http://
creativecommons.org/licenses/by-nc-nd/4.0/). larvae feed on more than 350 different host plants belonging
doi: 10.1016/S2095-3119(20)63334-2 to 76 plant families, including Poaceae, Asteraceae and
 HE Li-mei et al. Journal of Integrative Agriculture 2021, 20(3): 804–814
Fabaceae (Montezano et al. 2018). Its polyphagy is
one of the main reasons for the continuous damage and
rampant populations of FAW in the agroforestry ecosystem.
Previous studies have shown that adults of some insects
can vary in oviposition preference depending upon the
varietal characteristics, age and size, leaf-feeding damage,
reproductive state and nutrient availability of the plants
(Latheef and Irwin 1979; Thompson 1988). In general,
adults of phytophagous insects prefer to oviposit on species
of host plants that are nutrient-rich and suitable for larval
growth (Berdegue and Trumble 1996).
Planting a trap crop that is much attractive to the pest
can help the main crop from damage. For example, inter-
planting alfalfa strips in cotton fields significantly lowered
Lygus hesperus (Knight) population levels and eliminated
the need for insecticide use on this crop in the United
States (Stern et al. 1964, 1969; Godfrey and Leigh 1994).
In China, the planting of transgenic cotton expressing the
Bacillus thuringiensis (Bt) Cry toxins (Bt cotton) as a trap
crop not only controlled Helicoverpa armigera (Hübner),
but also reduced its presence on other host crops such as
wheat and maize (Wu et al. 2008). Nibouche et al. (2012,
2019) reported that Erianthus arundinaceus ((Retzius)
Jeswiet) is a trap crop for the sugarcane stem borer Chilo
sacchariphagus (Bojer). In addition, mungbean (Vigna
radiatus L.) is a trap crop of Apolygus lucorum (Meyer-
Dur.) to protect Bt-cotton (Lu et al. 2009), and velvetleaf
(Abutilon theophrasti Medicus) can be used to trap Bemisia
tabaci (Gennadius) and Sylepta derogata (Fabricius) (Lin
et al. 2015). Considering these preceding examples, trap
cropping is worth to be explored as a management option
for FAW in China.
Since 1996, the planting of Bt cotton has reduced damage
from numerous serious insect pests (Chitkowski et al. 2003;
Olsen et al. 2005; Wan et al. 2005; Wu and Guo 2005;
Sivasupramaniam et al. 2008; Wu et al. 2008; Tindall et al.
2009). It is also the main method to control and manage
FAW on the American continent (Buntin 2008; Siebert
et al. 2008a, b; Hardke et al. 2011). Although resistance
in FAW to Cry1Ab, Cry1Ac, Cry1Fa and Cry1F toxin from
B. thuringiensis has been reported (Blanco et al. 2010;
Ríos-Díez et al. 2012; Farias et al. 2014; Chandrasena
et al. 2018), the population in China has not developed
significant resistance to toxic proteins of B. thuringiensis,
such as Cry1Ab, Cry1Ac, Cry1F, Cry2Ab and Vip3A (Li G
P et al. 2019). Moreover, a laboratory bioassay indicated
that Chinese domestic Bt-Cry1Ab and Bt-(Cry1Ab+Vip3Aa)
maize has high control efficacy against S. frugiperda in
Yunnan, with the mortality rate of first instar larvae that had
fed on Bt-Cry1Ab being 59.23–65.41% and 100% on Bt-
(Cry1Ab+Vip3Aa) maize, respectively (Zhang and Wu 2019).
805
At least seven host plants of S. frugiperda are global
agricultural crops: in China, FAW larvae have been recorded
in fields of maize (Zea mays), wheat (Triticum aestivum),
sorghum (Sorghum bicolor), soybean (Glycine max), peanut
(Arachis hypogaea), cotton (Gossypium spp.) and foxtail
millet (Setaria italica) (Montezano et al. 2018; Jiang et al.
2019). Here, we systematically assessed the oviposition
preference of S. frugiperda on transgenic Bt-Cry1Ab, Bt-
(Cry1Ab+Vip3Aa) and conventional non-transgenic maize
and six other host plants in the laboratory and field. Our
findings further showed that maize was highly preferred
for ovipositing by FAW. Thus, commercial cultivation
of Bt-transgenic maize (Bt maize) as a trap crop can
potentially be used to control this pest. Bt maize may also
be used to protect other crops and improve the control and
management of S. frugiperda in Asia.
2. Materials and methods
2.1. Laboratory pot trials
Laboratory trials were carried out at the Xinxiang Experiment
Station of the Chinese Academy of Agricultural Sciences
(CAAS; 35°18´13.71´´N, 113°55´15.05´´E) in Henan
Province, China. FAW individuals were field-collected in
early 2019 in Dehong Autonomous Prefecture (Yunnan) and
reared for 10 generations in the laboratory. Insects were
kept at (25±1)°C, (75±5)% RH, and 16 h L:8 h D. Larvae
were fed a soybean flour and wheat bran-based diet (Greene
et al. 1976), and 1st to 6th instar FAW larvae were reared
in 22 cm×15 cm×8 cm plastic boxes. Once larvae were
fully developed, they were transferred to plastic trays with
vermiculite for pupation. On the 5th day after pupation, male
and female pupae were separated based on the method of
Zhao et al. (2011).
For experimental purposes, adults were exposed to
seven different hosts: Bt-Cry1Ab maize (10 plants per pot,
C0030.3.5-Nonghua 106, single hybrids, Beijing Dabei
Agricultural Biotechnology Co., Ltd., Beijing, China), Bt-
(Cry1Ab+Vip3Aa) maize (10 plants per pot, DBN3601-
Nonghua 106, single hybrids, Beijing Dabei Agricultural
Biotechnology Co., Ltd., Beijing, China), conventional maize
(10 plants per pot, Nonghua 106, single hybrids, Beijing
Dabei Agricultural Biotechnology Co., Ltd., Beijing, China),
sorghum (12 plants per pot, Jinza 26), peanut (five plants per
pot, Xiaobaisha), wheat (20 plants per pot, Xinong 529), and
cotton (eight plants per pot, Zhongmiansuo 49). All plants
were planted in 500-mL plastic cups containing a 60:35:5
mixture by mass of field soil (from the experimental field
of the Xinxiang Experiment Station of the CAAS), organic
cultivation soil (Huai’an Hui Sheng Horticulture Development
806 HE Li-mei et al. Journal of Integrative Agriculture 2021, 20(3): 804–814
Co., Ltd., Huai’an, Jiangsu, China) and vermiculite (1–3 mm,
Lingshou Xuyang Mining Co., Ltd., Shijiazhuang, Hebei,
China). All plants were grown in a greenhouse at (28±1)°C,
with (80±5)% RH and 16 h L:8 h D.
Oviposition preference of FAW was tested on seedlings
(20 cm tall; 4-leaf maize, 4-leaf sorghum, 5-leaf peanut,
3-leaf wheat and 5-leaf cotton plants) in 50 cm×50 cm×
50 cm cages (200-mesh nylon, seven species of plants
and one pot for each plant per cage) and kept at (25±1)°C
and (75±5)% RH, then 10 pairs of newly emerged adults
(♀:♂=1:1) were transferred to the cage. FAW adults were
fed daily with 5% (v/v) acacia honey water (acacia honey,
Baihua brand, Beijing Baihua Bee Co., Ltd., Beijing, China).
Daily, we counted the egg masses on seedlings (leaves and/
or stems) of each plant, and then collected the egg masses
in a separate 12 cm×17 cm zip-lock bag. After 3 days, we
counted the larvae and unhatched eggs, and summed them
to calculate the number of eggs. All plants were replaced
every day with fresh ones until 8 days after oviposition. The
test was repeated three times.
Oviposition preference of FAW was also tested on
conventional and two Bt maize plants: newly hatched larvae
were collected, transferred to seedlings of Bt-Cry1Ab maize,
Bt-(Cry1Ab+Vip3Aa) maize and conventional maize (35 cm
tall; plants were at the 4- to 5-leaf stage; three larvae per
seedling). Five pairs of newly emerged adults (♀:♂=1:1)
were put in the cage described above and fed daily with 5%
(v/v) acacia honey water. Two days later, maize seedlings
that had been damaged by FAW larvae were placed in
the cage with adults (three lines of maize and one pot for
each maize line per cage). FAW larvae remained on the
plants for the duration of the experiment. A preliminary
bioassay confirmed that FAW 1st instar larvae fed on and
damaged Bt-Cry1Ab maize and Bt-(Cry1Ab+Vip3Aa) maize
seedlings, although their survival rate on Bt-Cry1Ab maize
was 34.59–40.77% and 0% on Bt-(Cry1Ab+Vip3Aa) maize
(Zhang and Wu 2019). We counted the egg masses, then
collected the egg masses from the leaves or stems of each
plant and scattered them into individual egg with a brush.
We then counted the eggs on each plant daily until 7 days
after oviposition. On the last day of the experiment, the
damage caused by FAW on all leaves on each plant was
visually rated as shown in Table 1 (Davis and Williams 1994;
Williams et al. 2006). The test was repeated three times.
2.2. Field plot trials
For field trials at the experiment station of the Plant
Protection Institute of Chinese Academy of Agricultural
Sciences (CAAS; 22°41´13´´N, 101°53´22´´E) in Shuicheng
Village, Pu’er City, Yunnan Province, we used a single factor
experimental design with a totally randomized block. All
crops were planted manually, and the plant spacing and
row spacing were, respectively, 28 and 60 cm for maize and
sorghum, 4–6 and 20 cm for wheat and foxtail millet, 6 and
35 cm for soybean, 15 and 25 cm for peanut. Single-hybrid
maize varieties were used in field trials.
Oviposition preference of FAW was tested on Bt and
conventional maize (with three repetitions for each plant;
total: six plots, each 30 m2): Bt-Cry1Ab maize (C0030.3.5-
Nonghua 106, Beijing Dabei Agricultural Biotechnology
Co., Ltd., Beijing, China) and conventional maize (Nonghua
106, Beijing Dabei Agricultural Biotechnology, China). All
plants were sown on June 2, 2019, and urea (20 kg 667
m–2, N content ≥46.4%, Yunnan Yuntianhua Co., Ltd.,
Kunming, China) and compound fertilizer (15 kg 667 m–2,
CNP content ≥45%, Stanley Chemical Fertilizer Co., Ltd.,
Linshu, Shandong, China) were applied as a top dressing.
On June 15, June 19, June 21, June 23, June 26, July 7,
July 18 and July 28 (i.e., 13, 17, 19, 21, 24, 35, 46 and
56 days after sowing when maize plants were at the 3-leaf,
5-leaf, 6-leaf, 7-leaf, 8-leaf, 10-leaf, tasseling and silking
stages, respectively), the FAW egg masses on each plant
were counted. We used a five-spot sampling method and
sampled 20 plants at random from each location (Lin et al.
2015; Sun et al. 2019). Leaf damage caused by FAW on
maize was visually rated (Table 1).
Oviposition preference of FAW females also was tested
on different host plants. Seven hosts were used, with
three repetitions for each host (total: 21 plots, each 30
m2). The seven tested hosts were Bt-(Cry1Ab+Vip3Aa)
maize (DBN3601-Nonghua 106), conventional maize
(Nonghua 106), sorghum (provided by local farmer), peanut
(provided by local farmer), wheat (Chuanmai 1131), soybean
(Zhonghuang 37) and foxtail millet (Langu 3). All plants were
sown on October 3, 2019, and urea (20 kg 667 m–2, N content
≥46.4%, Yunnan Yuntianhua Co., Ltd., Kunming, China) and
compound fertilizer (15 kg 667 m–2, CNP content ≥45%,
Stanley Chemical Fertilizer Co., Ltd., Linshu, Shandong,
China) were applied as a top dressing. On October 20,
November 3, November 22, December 5 and December 20
(i.e., 17, 31, 50, 63 and 78 days after sowing), we counted
the FAW egg masses and larvae on undamaged plants
and the damaged plants by FAW, and the survey data were
summarized and sorted by month. In October, November
and December, plants were at seedling, vegetative growth
and reproductive growth stages, respectively. We used a
five-spot sampling method and sampled 20 plants randomly
from each location (Lin et al. 2015; Sun et al. 2019). Plants
were examined for damage by FAW, counted and rated
according to signs and symptoms of FAW damage (FAO
and CABI 2019). Any plant with a translucent window hole,
 HE Li-mei et al. Journal of Integrative Agriculture 2021, 20(3): 804–814 807

ragged edges or holes in its growth point, leaf, stem or fruit
was recorded as damaged.
2.3. Statistical analysis
Differences in the number of eggs or egg masses, larval
number, leaf damage rating and percentage of damaged
plants for the different hosts were analyzed using a one-
way analysis of variance (ANOVA), with proportional data
first arcsine square-root-transformed to meet assumptions
of normality and heteroscedasticity. Tukey’s honestly
significant difference (HSD) test was used as a post hoc test.
Student’s t-test was used to test for significant differences
in number of egg masses, larval number and leaf damage
rating between conventional and Bt-Cry1Ab maize from the
plot trial. All data were analyzed using SPSS version 20
(IBM, Armonk, NY, USA). Data in the text and figure are
mean±SE.
3. Results
3.1. Oviposition preference of S. frugiperda on
different hosts
Adults oviposited eggs on all seven host plants, but the host
species affected oviposition behavior (Fig. 1). There were

Table 1 Leaf damage ratings

Rating Definition of damage
0 No visible leaf damage
1 Only pin-hole damage
2 Pin-hole and small circular hole damage to leaves
3 Pin-hole, small circular lesions and a few small elongated lesions of up to 1.3 cm long on whorl and furl leaves
4 Several small to mid-sized (1.3 to 2.5 cm long) elongated lesions on a few whorl and furl leaves
5 Several large (>2.5 cm long) elongated lesions on a few whorl and furl leaves and/or a few small to mid-sized uniform to
irregular-shaped holes eaten from the whorl and/or furl leaves
6 Several large elongated lesions on several whorl and furl leaves and/or several large uniform to irregular-shaped holes eaten
from furl and whorl leaves
7 Many elongated lesions of all sizes on several whorl and furl leaves plus several large uniform to irregular-shaped holes
eaten from the whorl and furl leaves
8 Many elongated lesions of all sizes on most whorl and furl leaves plus many mid-sized to large uniform to irregular shaped
holes eaten from the whorl and furl leaves
9 Whorl and furl leaves almost totally destroyed

A B
No. of eggs No. of egg masses

Total no. of egg masses per cage

Bt-Cry1Ab maize 3 000
Total no. of eggs per cage
Daily no. of egg masses

8 Bt-(Cry1Ab+Vip3Aa) maize a 20
Conventional maize a
6 Sorghum
Peanut ab 15
per cage

Wheat 2 000
4 Cotton abc
ab ab
10
2 1 000 bc
b bc bc 5
b b
0 bc
1st 2nd 3rd 4th 5th 6th 7th 8th
Days of investigation (d) 0 0
ze

ze

ze

ut

at

n
to
hu

an

he
ai

ai

ai

C
ot
m

)m

lm

rg

Pe

Bt-Cry1Ab maize
So
b

na
Daily no. of eggs per cage

Aa
1A

Bt-(Cry1Ab+Vip3Aa) maize
io
p3
ry

900
nt

Conventional maize
-C

Vi

ve

Sorghum
b+
Bt

on
1A

Peanut
C

600
ry

Wheat
-(C

Cotton
Bt

300

0
1st 2nd 3rd 4th 5th 6th 7th 8th
Days of investigation (d)

Fig. 1 Daily number of egg masses (A), eggs (C) and total number of egg masses and eggs (B) laid by Spodoptera frugiperda on
seven hosts. Bar is SE (n=3). Different lowercase letters indicate a significant difference in the number of eggs or egg masses
among the hosts at P<0.05 level in a one-way ANOVA followed by Tukey’s HSD.
808 HE Li-mei et al. Journal of Integrative Agriculture 2021, 20(3): 804–814

significant differences in the total number of egg masses
(F6, 14=6.037, P=0.003, Fig. 1-C) and eggs (F6, 14=8.278,
P=0.001, Fig. 1-C) among the seven hosts. Overall,
S. frugiperda females laid the most egg masses (16.67±2.85
per cage) and eggs (1865.67±529.84 per cage) on
conventional maize plants, followed by Bt-(Cry1Ab+Vip3Aa)
maize plants and Bt-Cry1Ab maize plants, which are higher
than on peanut, sorghum, wheat and cotton. However,
there was no significant difference in the number of egg
masses and eggs among the two Bt maize hosts and the
conventional maize. Notably, most of the eggs were located
on the abaxial side of leaves; some were distributed on the
adaxial side of leaves and on stems.
the total number of egg masses (F2, 6=23.527, P=0.001,
Fig. 2-C) and eggs (F2, 6=54.942, P<0.001, Fig. 2-C) of
S. frugiperda among the larvae-damaged conventional
maize, Bt-Cry1Ab maize and Bt-(Cry1Ab+Vip3Aa) maize
plants. Overall, S. frugiperda females laid the most egg
masses (18.67±2.18 per cage) and eggs (1 909.00±119.96
per cage) on less-damaged Bt-(Cry1Ab+Vip3Aa) maize
plants, while laying fewer egg masses (4.00±0.58 per cage)
and eggs (225.67±32.09 per cage) on seriously damaged
conventional maize plants.
3.3. Oviposition preference of S. frugiperda for Bt
and conventional maize in the field

3.2. Ovipositional response of S. frugiperda among
three maize genotypes
The damage level of leaves was significantly greater on
conventional maize than on Bt maize (F2, 87=1 376.538,
P<0.001): 0.21±0.01 on Bt-(Cry1Ab+Vip3Aa) maize plants,
0.87±0.04 on Bt-Cry1Ab maize plants and 2.48±0.04 on
conventional maize plants. That is, Bt-(Cry1Ab+Vip3Aa) and
Bt-Cry1Ab maize plants were less damaged by S. frugiperda
larvae, while conventional maize plants were seriously
damaged by S. frugiperda larvae.
Adults oviposited eggs on all damaged maize plants
(Fig. 2); however, there was a significant difference in
In the field, S. frugiperda adults laid a similar number of
egg masses on Bt-Cry1Ab and conventional maize when
plants were at the 3-leaf stage (t=0.158, df=4, P=0.882,
Fig. 3-A). However, females in general laid more egg
masses on Bt-Cry1Ab than on conventional maize plants:
the difference was significant for the number of S. frugiperda
egg masses when maize was at the 5-leaf (t=11.717, df=4,
P<0.001, Fig. 3-A), 6-leaf (t=5.196, df=4, P=0.007, Fig. 3-A),
7-leaf (t=5.000, df=4, P=0.007, Fig. 3-A), 8-leaf (t=11.000,
df=4, P<0.001, Fig. 3-A), 10-leaf (t=4.000, df=4, P=0.016,
Fig. 3-A) and tasseling (t=3.000, df=4, P=0.040, Fig. 3-A)
stages. Overall, FAW adults preferred to lay eggs on Bt-
Cry1Ab than on conventional maize plants (t=10.076, df=4,

A B
No. of eggs No. of egg masses

Total no. of egg masses per cage

12
Bt-Cry1Ab maize 2 500 25
Daily no. of egg masses

Bt-(Cry1Ab+Vip3Aa) maize a
Total no. of eggs per cage

a
9 Conventional maize 2 000 20
per cage

6
1 500 15
3 b
1 000 b 10
0 b
1st 2nd 3rd 4th 5th 6th 7th 500 c 5
Days of investigation (d)
0 0
C
e

ze

ze
z

1 000
Daily no. of eggs per cage

ai

ai

ai

Bt-Cry1Ab maize
m

)m

lm
b

na
a

Bt-(Cry1Ab+Vip3Aa) maize
1A

800
3A

io
ry

Conventional maize
ip

t
en
-C

+V

600
v
Bt

on
b
1A

C
ry

400
-(C
Bt

200
0
1st 2nd 3rd 4th 5th 6th 7th
Days of investigation (d)

Fig. 2 Daily number of egg masses (A), eggs (C) and total number of egg masses and eggs (B) laid by Spodoptera frugiperda
on one conventional and two Bt-transgenic maize plants damaged by three newly hatched larvae. Bar is SE (n=3). Different
lowercase letters indicate a significant difference in the number of eggs or egg masses among the hosts at P<0.05 level in a one-
way ANOVA followed by Tukey’s HSD.
 HE Li-mei et al. Journal of Integrative Agriculture 2021, 20(3): 804–814 809

Conventional maize Bt-Cry1Ab maize addition, the leaf damage rating on conventional maize
A was also significantly higher than on Bt-Cry1Ab maize at
**
70 all stages (3-leaf: t=10.105, df=4, P=0.001; 5-leaf: t=8.708,
No. of egg masses per 100 plants

df=4, P=0.001; 6-leaf: t=18.911, df=4, P<0.001; 7-leaf:

60 t=12.780, df=4, P<0.001; 8-leaf: t=13.308, df=4, P<0.001;
50
10-leaf: t=15.839, df=4, P<0.001; tasseling: t=14.762, df=4,
30 P<0.001; silking: t=23.213, df=4, P<0.001; Fig. 3-C).
ns **
20
** ** ** 3.4. Oviposition, feeding preference and damage by
10 * *
ns S. frugiperda on crops in the field
0
g Host plant species greatly affected the oviposition and

g
af

af

af

af

af

af

lin

in
le

le

le

le

le

-le

lk feeding preference of S. frugiperda (Fig. 4). In October,

se
3-

5-

6-

7-

8-

10

Si
s
Ta

B
**
1–29 days after sowing when plants were at the seedling
1 000 stage, the number of egg masses per 100 plants on Bt-
No. of larvae per 100 plants

800 (Cry1Ab+Vip3Aa) and conventional maize was significantly

higher than those on wheat, sorghum, foxtail millet,
600
peanut and soybean (F6, 14=39.870, P<0.001, Fig. 4-A).
300 **
Conventional maize had the most egg masses per 100
** **
200 **
**
**
plants. It also had significantly more larvae per 100 plants
**
100 (F6, 14=38.256, P<0.001, Fig. 4-B) and more damaged
*
plants (F6, 14=144.211, P<0.001, Fig. 4-C) compared with
0
Bt-(Cry1Ab+Vip3Aa) maize and the other five hosts.
g

g
af

af

af

af

af

af

lin

in
le

le

le

le

le

-le

In general, in November, 30–59 days after sowing

lk
se
3-

5-

6-

7-

8-

10

Si
s
Ta

C 10
when plants were in the vegetative growth phase, Bt-
** **
(Cry1Ab+Vip3Aa) maize had the most egg masses per
**
8 100 plants, which was significantly higher than those on
Leaf damage rating

**
**
conventional maize, wheat, sorghum, foxtail millet, peanut
6 **
and soybean (F6, 14=129.222, P<0.001, Fig. 4-A). The
4
** number of larvae per 100 plants (F6, 14=77.404, P<0.001,
Fig. 4-B) and percentage of damaged plants (F6, 14=404.531,
2 ** P<0.001, Fig. 4-C) were significantly higher for conventional
maize than for Bt-(Cry1Ab+Vip3Aa) maize and the other
0
five hosts.
g

g
af

af

af

af
a

in

in

Generally, in December, 60–90 days after sowing

le

le

le

le

le

-le

el

lk
3-

5-

6-

7-

8-

10

Si
ss

when plants were in the reproductive growth phase, the

Ta

Stage
number of egg masses did not differ significantly (F6, 14=
1.576, P=0.226, Fig. 4-A) among the different hosts. The
Fig. 3 Number of egg masses (A) and larvae (per 100 plants)
(B) of Spodoptera frugiperda on conventional and Bt-Cry1Ab number of larvae (F6, 14=101.903, P<0.001, Fig. 4-B) and
maize in the field and the damage level of maize leaves (C) at percentage of damaged plants (F6, 14=1254.051, P<0.001,
different growing stages. Bar is SE (n=3). *, P<0.05; **, P<0.01; Fig. 4-C) were significantly higher on conventional maize
ns, non-significant differences (P>0.05) (Student’s t-test).
than on Bt-(Cry1Ab+Vip3Aa) maize and the other five host
plants.
P=0.001, Fig. 3-A). Overall, the numbers of egg masses per 100 plants on Bt-
The number of S. frugiperda larvae per 100 plants on (Cry1Ab+Vip3Aa) and conventional maize were significantly
conventional maize was significantly higher than on Bt- higher than those on wheat, sorghum, foxtail millet, peanut
Cry1Ab maize at all stages in the field (3-leaf: t=13.788, df=4, and soybean (F6, 14=54.997, P<0.001, Fig. 4-A), and Bt-
P<0.001; 5-leaf: t=5.596, df=4, P=0.005; 6-leaf: t=9.172, (Cry1Ab+Vip3Aa) maize had the most egg masses per
df=4, P=0.001; 7-leaf: t=18.179, df=4, P<0.001; 8-leaf: 100 plants. Conventional maize had the most larvae per
t=12.594, df=4, P<0.001; 10-leaf: t=12.363, df=4, P<0.001; 100 plants (F6, 14=361.381, P<0.001, Fig. 4-B) and the most
tasseling: t=4.354, df=4, P=0.012; silking: t=10.339, df=4, damaged plants (F6, 14=1337.852, P<0.001, Fig. 4-C), both
P<0.001; total: t=13.555, df=4, P<0.001; Fig. 3-B). In significantly higher than those on Bt-(Cry1Ab+Vip3Aa) maize
 810

C
B
Bt Bt Bt
-(C C -(C C -(C C
ry onv ry onv ry onv
1A e Dameged plants (%) 1A e No. of larvae per 100 plants 1A e
b+ ntio b+ ntio b+ ntio No. of egg masses per 100 plants
Vi na Vi na Vi na

0
30
60
90
120
0
100
200
400
600
0
10
20
30
p3 l p3 l p3 l
Aa ma Aa ma Aa ma
) m ize ) m ize ) m ize

a
a

a
a a a
W ize W ize W ize

a
S
Fo or ea h S
Fo or ea h S
Fo or ea h

b b
b

cd cd
xt gh t xt gh t xt gh t
ai um ai um ai um

b
lm lm lm
Bt Bt Bt
Pe ille Pe ille Pe ille

b b
-(C C -(C C -(C C
ry onv So an t ry onv So an t ry onv So an t
Seedling stage

Seedling stage

Seedling stage
b b b
1A e y ut 1A e y ut 1A e y ut
b+ ntio bea b+ ntio bea b+ ntio bea

one-way ANOVA followed by Tukey’s HSD.

n n n

b
b b

cd d bc
Vi na Vi na Vi na
p3 l p3 l p3 l
Aa ma Aa ma Aa ma
) m ize ) m ize ) m ize

a
a
b

a a a
W ize W ize W ize
a

S
Fo or ea h S
Fo or ea h S
Fo or ea h

b b

c cd
xt gh t xt gh t xt gh t
ai um ai um ai um

b
b b

lm lm lm
Bt Bt Bt

b b
-(C C Pe ille -(C C Pe ille -(C C Pe ille
ry onv So an t ry onv So an t ry onv So an t

b
b b

1A e
n y ut 1A e
n y ut 1A e
n y ut
Vegetative growth

Vegetative growth

Vegetative growth
b+ tio bea b+ tio bea b+ tio bea
n n n

b
b

d cd cd
Vi na Vi na Vi na
p3 l p3 l p3 l
Aa ma Aa ma Aa ma

a
) m ize ) m ize ) m ize

a
a a a
W ize W ize W ize
a a

S
Fo or ea h S
Fo or ea h S
Fo or ea h
xt gh t xt gh t xt gh t
ai um ai um ai um
lm lm lm
Bt Bt Bt
-(C C Pe ille -(C C Pe ille -(C C Pe ille
o
ry nv So an t o
ry nv So an t o
ry nv So an t

b b b b b
1A e
n y u 1A e
n y u 1A e
n y u
b+ tio be t b+ tio be t b+ tio be t
Reproductive growth

Reproductive growth

Reproductive growth

bc d b d cd d
b
a a a a a

Vi na an Vi na an Vi na an
p3 l p3 l p3 l
Aa ma Aa ma Aa ma
HE Li-mei et al. Journal of Integrative Agriculture 2021, 20(3): 804–814

) m ize ) m ize ) m ize

a
a
a

a a a
W ize W ize W ize
a

S
Fo or ea h S
Fo or ea h S
Fo or ea h
b

c de
xt gh t xt gh t xt gh t
ai um ai um ai um
Total

Total

Total

b
lm lm lm
Pe ille Pe ille Pe ille
b b

So an t So an t So an t
b b b b b

yb ut yb ut yb ut
ea ea ea
n n n
b b

e cde cd

sampling on November 3 and November 22; Reproductive growth, sampling on December 5 and December 20; Total, the sum of
in the field and percentage of damaged plants (C) of each host. Seedling stage, sampling on Octobor 20; Vegetative growth,

and larvae per 100 plants among different hosts and percentage of damaged plants among different hosts at P<0.05 level in a
five times for sampling. Bar is SE (n=3). Different lowercase letters indicate a significant difference in the number of egg masses
Fig. 4 Number of egg masses (A) and larvae (B) per 100 plants of Spodoptera frugiperda on seven hosts at different growth stages
 HE Li-mei et al. Journal of Integrative Agriculture 2021, 20(3): 804–814
and the other five hosts.
4. Discussion
Trap cropping is a promising, environmentally sound
approach to manage pests in agricultural and forest systems
through exploiting insect preferences for certain host plants
(Hokkanen 1991; Shelton and Badenes-Perez 2006; Cook
et al. 2007). In a wide range of cropping systems, trap
cropping greatly reduces damage, disease and insecticide
use on the main crops, and thus increases the yield of the
main crop (Mitchell et al. 2000; Boucher et al. 2003; Wu et al.
2008). Our laboratory results showed that FAW adults laid
eggs on all tested host plants, but preferred maize. These
findings are similar to those of Xu et al. (2019), Li D Y et al.
(2019) and Ba et al. (2020), but differs with the results
reported in Pitre et al. (1983), in which FAW adults also lay
eggs on grasses such as wheat and sorghum, in addition
to maize. These differences are likely due to different
environmental conditions, methods and insect populations.
In our study, the most eggs were recorded on conventional
maize, but there was no significant difference among the
conventional and two Bt maize plants. Thus, conventional
and Bt maize may be used to trap FAW and protect other
crops from this pest.
When plants are damaged by phytophagous insects, the
composition change of the plant volatiles will directly affect
feeding, oviposition and other behaviors of herbivorous
insects. Such herbivore-induced plant volatiles can alter
relationships among plants, herbivores, their natural
enemies and defense against the herbivorous attackers.
Volatiles released by Phaseolus vulgaris (Linn.) after
serious damage by Tetranychus urticae (Koch) can repel
T. urticae (Dicke et al. 1990). Injured leaves of maize also
can repel S. exigua (Turlings and Tumlinson 1991). In
the present study, when conventional maize, Bt-Cry1Ab
maize and Bt-(Cry1Ab+Vip3Aa) maize were damaged by
FAW larvae, the number of egg masses on Bt-Cry1Ab and
Bt-(Cry1Ab+Vip3Aa) maize was significantly higher than
that on conventional maize. Conventional maize plants
were seriously damaged, but Bt maize plants were less
damaged, perhaps due to the protection conferred by Bt,
and this varying degree of damage could have altered
the composition of the volatile components. These plant
volatiles in turn might act as a direct defense against
oviposition by FAW; thus FAW adults preferred to oviposit on
the less-damaged Bt maize plants. This preference of adults
to oviposit on healthy and undamaged or less-damaged
host plants has also been found for Chilo suppressalis,
Manduca quinquemaculata, and Xanthogaleruca luteola
Müller (Kessler and Baldwin 2001; Meiners et al. 2005;
Jiao et al. 2018). For oviposition, C. suppressalis adults
811
preferred Bt rice over neighboring non-Bt rice, which had
significantly greater caterpillar damage; consequently,
Bt rice plants may protect neighboring non-Bt rice plants
against C. suppressalis (Jiao et al. 2018). However, we
still need to determine which volatile components changed
and the extent of their change in the damaged maize plants.
Such studies will help us better understand the interaction
between plants and herbivorous insects and thus enhance
the efficacy of integrated pest control.
Density-dependent oviposition is a common strategy
for many insects to reduce larval competition, and females
usually spread out their eggs during oviposition, thus
minimizing conspecific density (Roitberg and Prokopy 1987).
For example, some frugivorous tephritid flies and seed-
feeding beetles have reduced larval survival when multiple
larvae develop on a single plant organ, and accordingly,
females avoid organs with previous oviposition (Prokopy
1972; Mitchell 1975). Our field investigation verified the
results of the laboratory trials and indicated that FAW
females had density-dependent oviposition behavior. In
the early stage, 1–29 days after sowing when plants were
less damaged, S. frugiperda adults laid a similar number of
egg masses on Bt-Cry1Ab or Bt-(Cry1Ab+Vip3Aa) maize
and conventional maize. When plants were at vegetative
growth phase (5- to 10-leaf stage) and the leaf damage
rating was more than 3 or the percentage of damaged plants
on conventional maize was more than 90%, oviposition
decreased on conventional maize and increased on Bt-
Cry1Ab or Bt-(Cry1Ab+Vip3Aa) maize. In general, FAW
adults preferred to lay eggs on less-damaged conventional
maize and on Bt-Cry1Aa or Bt-(Cry1Ab+Vip3Aa) maize; the
number of egg masses on Bt-Cry1Ab or Bt-(Cry1Ab+Vip3Aa)
maize were higher than that on conventional maize.
However, conventional maize had the most FAW larvae
and most damaged plants or leaf damage rating. The
decrease of leaf area and high density of FAW population in
the field also may contribute to the decrease of oviposition
on conventional maize. These findings indicate that maize
is a highly preferred and suitable host for larval feeding
and ovipositing by females, consistent with the level of
damage in the field and previous research results (Kebede
and Shimalis 2018; Jiang et al. 2019; Li D Y et al. 2019;
Ba et al. 2020). Therefore, we can take advantage of this
strong oviposition preference for Bt over non-Bt maize in
FAW females to effectively reduce the population density
of FAW in the field by planting Bt maize as a trap crop and
keep the population of FAW within the economic threshold.
At present, planting insect-resistant transgenic crops is one
of the main strategies to control and manage lepidopteran
pests such as H. armigera, P. gossypiella and S. frugiperda
around the world (Chitkowski et al. 2003; Olsen et al. 2005;
Siebert et al. 2008a, b; Wu et al. 2008; Tindall et al. 2009;
812 HE Li-mei et al. Journal of Integrative Agriculture 2021, 20(3): 804–814
Hardke et al. 2011). Here, FAW adults mainly laid eggs on
Bt maize, while the number of larvae per 100 plants and
leaf damage rating or percentage of damaged plants were
significantly lower than on conventional maize. In other
words, the control efficacy of Bt-(Cry1Ab+Vip3Aa) is high
against S. frugiperda in Yunnan, consistent with the results
of Zhang and Wu (2019). Cultivation of Bt maize may thus
be used commercially to control S. frugiperda in China.
5. Conclusion
Maize is a preferred host for the invasive population of
FAW in China and Bt maize takes a high efficacy against
the pest. After conventional maize was damaged by FAW
larvae, the transgenic one could attract more female moth to
oviposit and killed larvae hatched late. Therefore, Bt maize
holds promise as trap crop for the commercial control and
management of S. frugiperda on the agricultural system that
consists of different crops in China.
Acknowledgements
This work was supported by the Key Project for Breeding
Genetically Modified Organisms, China (2019ZX08012004)
and the National Key Research and Development Program
of China (2019YFD0300102).
Declaration of competing interest
The authors declare that they have no conflict of interest.
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