Crop Protection 21 (2002) 997–1002

Seasonal abundance of the mirids, Lygus lucorum and Adelphocoris

spp. (Hemiptera: Miridae) on Bt cotton in northern China
K. Wu*, W. Li, H. Feng, Y. Guo
Institute of Plant Protection, Chinese Academy of Agricultural Sciences, West Yuanmingyuan Road, Beijing 100094, China
Received 4 April 2002; accepted 14 May 2002

Abstract

Lygus lucorum Meyer-Dur, . Adelphocoris fasciaticollis Reuter and Adelphocoris lineolatus (Goeze) (Hemiptera: Miridae) are
important secondary insect pests in cotton fields in northern China. The seasonal dynamics of their mixed populations on a
transgenic variety expressing the insecticidal Bt protein Cry1A, and a cotton line expressing proteins of Cry1A and CpTI (cowpea
trypsin inhibitor gene) were compared to seasonal dynamics on similar but non-transgenic varieties from 1998 to 2001. No
significant differences were detected between population densities of these bugs on unsprayed normal cotton and unsprayed
transgenic cotton. However, mirid damage on unsprayed transgenic cotton was significantly higher due to a reduced number of
insecticide sprays against Helicoverpa armigera compared with the number of sprays in the normal cotton. This suggests that
the mirids have become key insect pests in transgenic cotton fields, and that their damage to cotton could increase further with
the expansion of the area planted to transgenic cotton if no additional control measures are adopted. r 2002 Elsevier Science Ltd.
All rights reserved.

Keywords: Transgenic Bt cotton; Population dynamics; Lygus lucorum; Adelphocoris spp.; China

1. Introduction pests on transgenic Bt plants in order to develop a

.
Helicoverpa armigera (Hubner) is a key pest of cotton,
Gossypium hirsutum L. in China (Guo, 1997), and
growers routinely use chemical insecticides for its
control. Since 1990, resistance to chemical insecticides
has been a serious problem, and is a major threat to
cotton production in China (Wu et al., 1997). Trans-
genic cotton, engineered to continuously express a d-
endotoxin from Bacillus thuringiensis Berliner (Bt),
holds great promise in controlling this insect pest. Bt
cotton began to be commercially planted in 1997 (ca.
10,000 ha.) and expanded rapidly to 1.067 million ha. in
2000 in northern China (ca. 90% cotton planting area in
the region) (Wang et al., 1997; Wu and Guo, 2000; Qu
et al., 2001).
There are numerous arthropods in cotton fields.
Because a comprehensive insect control strategy in
cotton also involves non-lepidopterous pests, it is
important to investigate the field abundance of all insect
*Corresponding author. Fax: +86-10-62894786.
E-mail address: kongmingwu@hotmail.com (K. Wu).
satisfactory IPM plan for Bt cotton (Wilson et al., 1992;
Riggin-Bucci and Gould, 1997; Pilcher et al., 1997).
While the Bt protein is only directly toxic to a narrow
spectrum of lepidopteran species, the dynamics of other
species may be indirectly affected. Effects on non-target
species may be positive, due to the removal of disruptive
pesticides, or negative due to the effective removal of a
lepidopterous host insect in the case of parasitoids or
prey in the case of predators (Fitt, 1994). The wide-
spread adoption of Bt cotton has drastically reduced the
need for insecticides for many key pest lepidopterans.
However, these insecticides previously afforded excellent
control of phytophagous plant bugs, and this reduction
in insecticide use has resulted in increased population
densities of plant bugs (Greene et al., 1999).
The important non-lepidopterous pests in cotton
fields in northern China include various mirids, cotton
aphid, Aphis gossypii Glover and carmine spider mite,
Tetranychus cinnabarinus (Boisduval) (Ting, 1963b;
Wu, 1989; Wu and Liu, 1992). Eighteen species of
mirids were recorded as cotton insect pests in China,
among which Lygus lucorum Meyer-Dur, . Adelphocoris

0261-2194/02/$ - see front matter r 2002 Elsevier Science Ltd. All rights reserved.
PII: S 0 2 6 1 - 2 1 9 4 ( 0 2 ) 0 0 0 8 0 - 7
998 K. Wu et al. / Crop Protection 21 (2002) 997–1002
fasciaticollis Reuter and Adelphocoris lineolatus (Goeze)
are considered as the most important pests in cotton
production in northern China (Chu and Meng, 1958;
Ting, 1963a; Li et al., 1994a). They prefer to feed on
flower buds causing them to abscise from the plant, and
therefore may reduce cotton yields (Ting, 1964, 1965; Li
et al., 1994a ,b). In this paper, we report on the results of
investigations into the dynamics of mirids on transgenic
cotton varieties in northern China.
2. Materials and methods
2.1. Cotton lines
Two transgenic cotton varieties, GK12 and SGK321,
developed by the Biotechnology Research Institute,
Chinese Academy of Agricultural Sciences, and their
parental lines (Shimian3 and Shiyuan321), were used in
this study (Guo, 1995). GK12 is a Bt cotton variety
expressing Cry1A toxic protein, and SGK321 is a cotton
variety expressing proteins of Cry1A and CpTI (cowpea
trypsin inhibitor gene). Both transgenic varieties have
been commercially planted in northern China. All
cotton lines were supplied by the Biotechnology
Research Institute, Chinese Academy of Agricultural
Sciences.
2.2. Field experiments
Experiments were conducted from 1998 to 2001 at
Langfang Experimental Station of Chinese Academy of
Agricultural Sciences, located in Hebei Province of
northern China. The test cotton lines were GK12 and
Shimian3 from 1998 to 2000, however, SGK321 and
Shiyuan321 were used in 2001 due to the rapid increase
in the planting area of SGK321 in 2000. The field
experimental designs were a randomized complete
block, replicated three times. A 3 m space was set up
between plots to decrease possibility of mirids dispersion
among treatments. Each plot was about 0.033 ha and
was seeded at a rate expected to produce 45,000 plants
per planted hectare. Cotton was planted between May
1st and 5th every year, and maintained using the
standard agronomic practices in northern China.
In 1998, the trial consisted of two treatments, GK12
plots and Shimian3 plots, in which no insecticides were
used in the whole season. After 1998, the experiment
was designed with three treatments, namely, a transgenic
cotton treatment and its control variety (normal
parental line), with no insecticide treatment and an
insecticide (mainly pyrethroid) treatment of non-Bt
cotton (Shimian3). In the chemical treatment, sprays
were applied against cotton bollworm, according to the
control threshold described by Guo et al. (1985), with a
nozzle held 0.3–0.5 m above cotton plants. A ‘‘Gong-
nong-18’’ knapsack sprayer with a tank capacity of 16 l
and a spray lance length of 0.8 m (Handan Sprayers
Ltd., Handan, China) was used to apply 600 l/ha before
10th July and 900 l/ha after 15th July (Table 1).
Sampling was undertaken once every 3–4 d from mid-
June to early-September. Five sites were randomly
chosen from every plot on each occasion with a total
number of 100 cotton plants per plot. For each sampled
plant, a thorough whole-plant survey was conducted in
which adults and nymphs of the mirids were counted in
the field.
2.3. Statistical analysis
A paired t-test was used to compare the means of
mirid population densities between the plots of GK12
and Shimian3 in 1998. All data on population densities
of the mirids from different treatments in 1999, 2000 and
2001 were analyzed using analysis of variance and
means were separated using the protected least sig-
nificant difference (LSD) test (SAS Institute 1988).
3. Results
There were no significant differences in mirid density
on GK12 (Bt cotton) and its parental line (Shimian3) in
1998 from the middle of June to early September
(p > 0:05) (Fig. 1). In comparison to 53 individuals per
hundred cotton plants on Shimian3 on August 13th, the
highest density on GK12 was 70 on August 23rd.
In 1999, mirid densities in all treatments were low
before early August, but they increased rapidly, and
reached their peaks in mid-August. Due to insecticide
use for control of H. armigera, mirid densities in
insecticide treatment of conventional cotton on August
13th, 17th, 21st and 25th were significantly lower than
those in the plots of GK12 and Shimian3 which had no
insecticide applications (po0:05) (Fig. 2). As in 1998,
there were no significant differences in mirid densities
between GK12 and its parental variety (Shimian3)
(p > 0:05).
In 2000, mirid density in all treatments was again very
low before August, but rapidly increased and remained
high up till late September, reaching 323 per hundred
plants on August 21st on GK12 and 370 per hundred
plants on August 25th on Shimian2 cotton without
insecticide use. Mirid density was not significantly
different (p > 0:05) on the unsprayed plots, but where
insecticide had been applied on non-Bt cotton, mirid
density was lower than those on GK12 and Shimian3
(without insecticide use) (Fig. 3).
Due to a higher density of H. armigera in July 2001
non-Bt cotton fields were sprayed with a pyrethroid
insecticide, b-cypermethrin 16 times (Table 1). After the
first spray on June 18th, mirid densities in the insecticide
 K. Wu et al. / Crop Protection 21 (2002) 997–1002 999

Table 1
Insecticide sprays for control of H. armigera on conventional cotton plants from 1999 to 2001 to control H. armigera

Year Insecticide Dose (l/ha (product)) Spray date

1999 2.5% Cyhalothrin (ICI Ltd., Britain) 0.60 June 24th

2.5% Cyhalothrin (ICI Ltd., Britain) 0.60 June 29th
20% Fenvalerate (Sumitomo Chemical Co. Ltd.) 0.90 July 2nd
20% Fenvalerate (Sumitomo Chemical Co. Ltd.) 0.90 July 7th
10% Imidacloprid (Shijiazhuang Chemical Co.)a 0.45 July 23rd

2000 4.5% b-cypermethrin (Tianjin Pesticide Co.) 0.60 June 20th

0.60 June 23rd
0.60 June 29th
0.90 July 3rd
0.90 July 15th
0.90 July 19th
0.90 July 23rd
0.90 July 27th

2001 4.5% b-cypermethrin (Tianjin Pesticide Co.) 0.60 June 18th

0.60 June 20th
0.60 June 22nd
0.60 June 24th
0.60 June 26th
0.60 June 28th
0.60 June 30th
0.90 July 2nd
0.90 July 4th
0.90 July 15th
0.90 July 17th
0.90 July 20th
0.90 July 22nd
0.90 July 26th
0.90 July 28th
0.90 July 30th
a
This spray was directed at A. gossypii.

100
Gk12
Population density (individuals per hundred

90
Shimian3
80

70
cotton plants)

60

50
40
30

20
10

0
15-Jun 27-Jun 9-Jul 21-Jul 2-Aug 14-Aug 26-Aug
Date

Fig. 1. Mirid population dynamics in GK12 and Shimian3 fields, 1998, Hebei Province. Values shown are means71 standard error. Paired t-test
indicates no significant difference between GK12 and Shimian3 (p > 0:05).

treatment of non-transgenic cotton was lower than those 4. Discussion

on SGK321 and its parental line Shiyuan321 (without
insecticide use) until September 24th. There were also In our experiments, in cotton/soybean systems, the
significant differences among different treatments on major mirid species were identified as L. lucorum, A.
August 4th and 16th (df=2,4; F ¼ 9:23; p ¼ 0:0317; and fasciaticollis and A. lineolatus although their proportion
df=2,4; F ¼ 16:84; p ¼ 0:0113) (Fig. 4). varied among years. A. fasiaticollis overwinters in its
1000 K. Wu et al. / Crop Protection 21 (2002) 997–1002

60

Population density (individuals per hundred

Gk12
a
50 Shimian3
a

40 Shimian3(chemical control)

plants)
a
a
30 a
a
a
a
20
a

10 ab
b
b b
b b
0
6-Jul 16-Jul 26-Jul 5-Aug 15-Aug 25-Aug 4-Sep
Date
Fig. 2. Mirid population dynamics in GK12 and Shimian3 fields, 1999, Hebei Province. Means from the same evaluation date followed by the same
letter were not statistically different (po0:05; LSD test). Evaluation dates with means not followed by letters were not significantly different among
treatments.

450
Gk12
Population density (individuals per hundred

400
Shimian3 a a
350
a
300 Shimian3(chemical control) a a
cotton plants)

250 a ab
a
200

150 b
b
100 b
50 b

0
19-Jun 29-Jun 9-Jul 19-Jul 29-Jul 8-Aug 18-Aug 28-Aug
Date

Fig. 3. Mirid population dynamics in GK12 and Shimian3 fields, 2000, Hebei Province. Means from the same evaluation date followed by the same
letter were not statistically different (po0:05; LSD test). Evaluation date with means not followed by letters were not significantly different among
treatments.
Population density (individuals per hundred cotton

35
SGK321 Shiyuan321 Shiyuan321(chemical control)

30

25

20
plants)

a aa
15

10

b
5 b
b
0
16-Jun 26-Jun 6-Jul 16-Jul 26-Jul 5-Aug 15-Aug 25-Aug
Date

Fig. 4. Mirid population dynamics in SGK321 and Shiyuan321 fields, 2001, Hebei Province. Means from the same evaluation date followed by the
same letter were not statistically different (po0:05; LSD test). Evaluation dates with means not followed by letters were not significantly different
among treatments.
 K. Wu et al. / Crop Protection 21 (2002) 997–1002
egg-stage in scars of tree trunks. Hatching begins in
early May, and the nymphs leave the tree and move to
weeds in adjacent areas or directly to the cotton field. A.
lineolatus and L. lucorum lay eggs in the tissues of alfalfa
and other weeds. They hatch in early April and
subsequent generations attack cotton plants for a long
period, from late May to the end of cotton growing
season. Overlapping generations frequently occur since
the adult stage of the mirids may last more than one
month (Chu and Meng, 1958; Li et al., 1994a). Plant
bugs prefer shady and moist environments and it is
reported that the level of rainfall and quality of host
plants are key factors which regulate the seasonal
population dynamics of mirids (Ting, 1963a, 1964).
The growth form of the mixed populations of cotton
mirids may be influenced by the amounts and temporal
distribution of rain-fall from June to August. Consistent
with periods of rainfall, the peaks of population density
may present four types in the seasonal dynamics of the
mirids, i.e., pre-peak, post-peak, mid-peak and bi-peak
(Ting, 1964). A similar conclusion may be drawn from
our present experimental results. High rainfall in mid-
season in 1998 and 2001 coincided with serious
populations of the mirids at the flowering stage. High
rainfall late in the 1999 and 2000 seasons resulted in a
rapid increase of the mirid population during the boll
stage of cotton growth.
It is reported that there are no adverse effects of Bt
cotton on several beneficial insects including (Coccinella
septempunctata (Linnaeus), Leis axyridis (Pallas) and
Propylaea japonica (Thunberg)), lacewing (Chrysopa
sinica (Tjeder), Chrysopa septempunctata (Wesmael),
Chrysopa shansiensis (Kawa) and Chrysopa formosa
(Brauer)), spiders (Erigonidium graminicolum (Sunde-
vall) and Misumenopos tricuspidata (Fabricius)) and
Orius similis (Zheng) (Wu, 2001). Population densities of
sweetpotato whitefly, Bemisia tabaci (Gennadius) on Bt
cotton are higher than on the control cultivars as a
consequence of reduced leaf feeding damage by lepi-
dopterous insects (Wilson et al., 1992). A study on the
influences of Bt cotton plantings on the population
dynamics of the cotton aphid, A. gossypii Glover,
indicated that, in comparison with non-Bt varieties,
where pesticides are applied against cotton bollworm,
the aphid populations in Bt cotton plots were sup-
pressed efficiently by natural enemies. It was suggested
that Bt cotton could not only play an important role in
control of cotton bollworm, but also could efficiently
prevent cotton aphids from resurgence caused by
insecticidal application against cotton bollworm (Wu,
2001).
In Australia, the mirid bugs (Creontiades dilutus,
Campylomma livida) in Bt cotton fields showed resur-
gence pattern (Fitt, 1994). Our results indicate that there
was no significant difference in the density of popula-
tions of the mirids between unsprayed conventional
1001
cotton and unsprayed Bt cotton. However, perhaps due
to the decrease in insecticidal applications against cotton
bollworm, the damage of the mirids on Bt cotton was
more serious than that in sprayed conventional cotton
fields, suggesting that the mirids have become key insect
pests in Bt cotton fields. Therefore their damage to
cotton would further increase with the enlargement of
Bt cotton area, if no additional control measures were
adopted. If the published thresholds for mirid control
had been followed, (5 bugs per hundred plants in the
seedling stage and 10 bugs per hundred plants in the
mid-period of cotton growth) (Zhang et al., 1986), plant
bugs in Bt cotton fields would have required control
based on our studies from 1998 to 2001.
Li et al. (1994a) indicated that there are significant
differences in developmental duration, survival and
average body weight of nymphs, and in the fecundity
and longevity of adult A. lineolatus which develop on
alfalfa, cotton, kidney bean and sesame; and that an
alfalfa/cotton system can result in major outbreaks of
the pest in cotton fields. It is important to avoid Bt
cotton planting in fields adjacent to alfalfa and other
host plants mirids prefer.
Acknowledgements
We thank Dr. Derek Russell (NRI, UK), Dr. Fred
Gould (North Carolina State University, USA) and
Dr. Fengming Yan (Peking University, China) for
critical review and discussion of the manuscript. This
research was supported by Projects Grant No. 863
(2001AA212271) and Projects Grant No. 973
(G2000016208) of the Ministry of Science and Technol-
ogy of China.
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