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Crop Protection 23 (2004) 463–467

Seasonal pattern of infestation by pink bollworm Pectinophora


gossypiella (Saunders) in field plots of Bt transgenic cotton in the
Yangtze River valley of China
P. Wana,b, K. Wua,*, M. Huangb, J. Wub
a
Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100094, China
b
Institute of Plant Protection and Soil Fertilize, Hubei Academy of Agricultural Sciences, Wuhan 430064, China
Received 2 September 2003; received in revised form 29 September 2003; accepted 30 September 2003

Abstract

Two transgenic cotton lines (BG1560 and GK19) carrying a Cry1A gene from Bacillus thuringiensis subsp. kurstaki (Berliner),
developed, respectively, by Monsanto Co. and Biotechnology Research Institute, Chinese Academy of Agricultural Sciences, were
evaluated for resistance to pink bollworm Pectinophora gossypiella (Saunders) in field plots in Tianmen County of Hubei Province,
located in the Yangtze River valley of China during 2001 and 2002. The results showed that there were no significant differences in
egg density among the two Bt cotton lines and a conventional cotton line, but larval densities on both Bt lines were significantly
lower than on the conventional line in both years. In comparison with the larval density on a conventional line without chemical
control, the control efficacy in different growth stages of cotton in several treatments were 89–100% for BG1560, 73–100% for
GK19, and 54–88% for chemically treated conventional cotton, where insecticides were sprayed 9 times in 2001 and 11 times in 2002
for control of pink bollworm. We conclude that Bt cotton planting in the Yangtze River region possesses a high potential for control
of pink bollworm.
r 2003 Elsevier Ltd. All rights reserved.

Keywords: Bt transgenic cotton; Pink bollworm; Control efficiency; China

1. Introduction pink bollworm Pectinophora gossypiella (Saunders) and


cotton bollworm Helicoverpa armigera (Hubner), . are
Cotton planting in China is grouped geographically major pests in the region, particularly in middle and late
into 3 major regions: the Yangtze River Region, the season under dry conditions (Cao and Shu, 1986; Liu
Yellow River Region, and the Northwestern Region et al., 1986; Shu and Cao, 1987). Traditionally, chemical
(Guo, 1997). The climate in these different regions varies control is the major method for protecting cotton from
greatly in amount of rainfall and length of growing pink bollworm damage, but the efficacy of these
season. The Yellow River Region is located between insecticides has declined quickly due to the evolution
33 N and 41 N. Influenced by the highland dry of resistance to insecticides in pink bollworm (Yuan and
monsoon, the annual average rainfall is 500–700 mm Wu, 1986; Wang et al., 1998; Yang et al., 2000).
concentrated in June, July and August. Damage from Transgenic lines of cotton that carry a gene coding for
cotton bollworm is a major factor in this region’s cotton an insecticidal protein derived from Bacillus thuringien-
production (Guo, 1997). The Yangtze River Region is sis have high levels of insecticidal efficacy against larvae
located between 25 N and 33 N where the annual of cotton bollworm, pink bollworm and other lepidop-
rainfall is between 800 and 1500 mm. Due to the longer teran pests (Wilson et al., 1992; Flint et al., 1995, 1996;
period for cotton development, cotton is cultured in a Flint and Parks, 1999; Wu et al., 2000). In China, Bt
density less than 35,000 plants per hectare; the plants cotton was first commercially planted to combat H.
attaining a height above 160 mm after mid-season. Both armigera in the Yellow River Region in 1997 and
expanded rapidly to 2 million ha in 2001 in the region
*Corresponding author. Tel.: +86-1062815929; fax: +86-1062894786. (ca. 95% of the cotton planting area in the region)
E-mail address: wkm@caascose.net.cn (K. Wu). (Qu et al., 2001). The practice of Bt cotton planting in

0261-2194/$ - see front matter r 2003 Elsevier Ltd. All rights reserved.
doi:10.1016/j.cropro.2003.09.017
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464 P. Wan et al. / Crop Protection 23 (2004) 463–467

the Yellow River Region indicated that the Bt lines sprayed as needed to control pink bollworm. In 2002,
expressed insecticidal protein at a high level in early the experimental design was the same as in 2001 except
season and presented a high level of resistance to the that Simian3 replaced HB3517. In the chemical applica-
second generation of cotton bollworm, but decreased in tion treatment, the timing of spraying was decided
toxin content in the middle and late stages of cotton according to the control threshold for pink bollworm
growth causing efficacy to decline late in the season described by Cao and Shu (1986). Insecticides were
(Zhang et al., 2001). Given the high risk of damage and applied with a sprayer held 0.3–0.5 m above cotton
overwintering from both pink bollworm and H. plants. The sprayer was a ‘‘Gongnong-16’’ knapsack
armigera in middle and late season (if Bt protein sprayer with a tank capacity of 16 l and a spray lance
concentrations decline in this way), the potential value length of 0.8 m (Handan Sprayers Ltd., Handan,
of Bt cotton deployment in the Yangtze River Region China). Spray volumes were 600 l/ha. before July 10
has been debated for several years (Huang et al., 2002). and 900 l/ha after July 15. Insecticide application details
Therefore, it is important to understand the efficacy of for the two years are shown in Table 1.
Bt cotton against lepidopteran pests in middle and late To estimate pink bollworm egg density, each plot in
season. Here we report the results of studies of seasonal the field was sampled once every 5 d from early June to
efficacy of Bt cotton against damage from pink boll- late September. Each sampling used 5 random sites
worm conducted in Hubei Province in the middle of the within each plot and evaluated a total of 100 cotton
Yangtze River Region during 2001 and 2002. plants. For each sampled plant, a thorough whole-plant
survey was made. Five sites with a total of 50 cotton
plants in each plot were selected for surveying the
2. Materials and methods damage from first generation pink bollworm. Flowers
infested with pink bollworm were collected for counting
2.1. Cotton lines larvae every day from July 1 to July 31. In general, one
larva could be found in each infested flower. On August
There were four cotton lines in the experiment. Two 15, August 30 and September 15, 5 random sites within
transgenic cotton varieties, GK19 containing a Cry1A each plot with a total of 50 cotton plants were sampled,
gene and BG1560 expressing a Cry1Ac gene, were and exit holes in infested bolls were counted. One
supplied by the Biotechnology Research Institute, hundred pre-mature bolls were sampled randomly from
Chinese Academy of Agricultural Sciences (Beijing, each plot on October 10 and October 25. They were kept
China), and Monsanto Co. (St. Louis, USA), respec- in a 30  40 cm2 bag and left in the sun for two weeks to
tively. Two conventional cultivars, Simian3 (GK19’s
parental line) and HB3517 (a major planting variety in Table 1
Hubei Province), were obtained from Hubei Academy Insecticide sprays for control of pink bollworm on conventional cotton
lines in 2001 and 2002
of Agricultural Sciences (Wuhan, China).
Year Insecticide formulation Dose Spray date
2.2. Field experiments (l/ha (product))

2001 50% Acephate ECa 1.8 June 14


Experiments were conducted in 2001 and 2002 in 4.5% Cypermethrin ECb 1.5 July 19
Tianmen County, Hubei Province, in the middle of the 50% Parathion methyl ECa 1.5 July 28
4.5% Cypermethrin ECb 1.5 August 5
Yangtze River valley, where there is an intensive
4.5% Cypermethrin ECb 1.5 August 12
planting area of cotton. The test cotton lines in 2001 4.5% Cypermethrin ECb 1.5 August 22
were GK19, BG1560 and HB3517. HB3517 was 4.5% Cypermethrin ECb 1.5 September 5
replaced with Simian3 in 2002. The experimental design 4.5% Cypermethrin ECb 1.5 September 15
was a randomized complete block and replicated three 4.5% Cypermethrin ECb 1.5 September 25
times. A 1.5 m space was left between plots to decrease
2002 4.5% Cypermethrin ECb 1.5 June 20
the possibility of pink bollworm larval movement 4.5% Cypermethrin ECb 1.5 July 20
among treatments. Each plot was about 0.033 ha and 4.5% Cypermethrin ECb 1.5 July 27
was seeded at a rate expected to produce 30,000 plants 50% Parathion methyl ECa 1.8 August 10
per hectare. The cottonseeds were sown in a seedling bed 50% Acephate ECa 1.8 August 16
50% Parathion methyl ECa 1.8 August 22
in the glasshouse in early April. After the seedlings grew
4.5% Cypermethrin ECb 1.5 August 28
to the two-leaf stage, they were transplanted to the field 4.5% Cypermethrin ECb 1.5 September 5
between May 10 and May 15, and maintained using 4.5% Cypermethrin ECb 1.5 September 12
standard agronomic practices for the Province. 4.5% Cypermethrin ECb 1.5 September 18
In 2001, the trial consisted of four treatments: GK19, 4.5% Cypermethrin ECb 1.5 September 25
BG1560 and HB3517 plots without insecticide use, and a
Shalongda Co. Ltd.
b
HB3517 chemical control plots where insecticides were Hongtaiyang Co. Ltd.
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P. Wan et al. / Crop Protection 23 (2004) 463–467 465

force diapausing pink bollworm larvae to exit the bolls. 14, and 576 eggs per hundred plants in the third
The larvae were then counted. generation in HB3517 (chemical treatment) on Septem-
ber 9, respectively. However, there were no significant
2.3. Statistical analysis differences in egg densities among the treatments on the
peak dates for three generations (df ¼ 3; 6; F ¼ 0:817;
All data on population densities and infestations of P ¼ 0:520; df ¼ 3; 6; F ¼ 0:375; P ¼ 0:773; df ¼ 3; 6;
pink bollworm in different treatments in 2001 and 2002 F ¼ 0:503; P ¼ 0:690). The larval density in flowers
were analyzed using analysis of variance (ANOVA) and ranged from 0.38 per hundred flowers in BG1560 to 5.54
means were compared using the protected least sig- per hundred flowers in HB3517 without insecticide use.
nificant difference (LSD) test (SAS Institute, 1988). Larval densities in HB3517 were significantly higher in
HB3517 without insecticide use than in other treatments
(df ¼ 3; 6; F ¼ 79:482; Po0:001) (Table 2). The exit
3. Results holes in August were 0.08 per hundred plants in BG1560
and 0.31 per hundred plants in GK19; both of these
3.1. Pink bollworm infestation in 2001 were significantly less than in HB3517 with or without
insecticide use (df ¼ 3; 6; F ¼ 38:746; Po0:001). In
Curves of pink bollworm egg density in the different September, the exit holes in HB3517 increased drasti-
treatments in 2001 are presented in Fig. 1. These cally to 23.26 from 11.95 per hundred bolls in August,
indicate that there are three generations of pink and significantly higher than those in other treatments
bollworm in cotton fields during the cotton season. (df ¼3, 6; F ¼ 150:473; Po0:001). There were also
The maximum numbers of eggs in different generations significant differences in larval densities in bolls among
were 86 eggs per hundred plants in the first generation in treatments (df ¼ 3; 6; F ¼ 123:781; Po0:001), which
HB3517 sampled on June 19, 266 eggs per hundred reached 87.50 individuals per hundred bolls in HB3517
plants in the second generation in BG1560 on August compared with less than 10 larvae per hundred bolls in
both Bt cotton varieties.
700
BG1560 (Bt)
600 GK19 (Bt)
3.2. Pink bollworm infestation in 2002
Eggs per hundred plant

HB3517
500
HB3517 (chemical)
400 Fig. 2 shows egg density dynamics of pink bollworm
300 in different treatments in 2002. As in 2001, the
200 population densities increased generation by generation.
100
The number of eggs increased from 94 eggs per hundred
plants for the first generation on Simian3 on June 24 to
0
30-May 14-Jun 29-Jun 14-Jul 29-Jul 13-Aug 28-Aug 12-Sep 27-Sep
504 eggs per hundred plants for the third generation on
Date GK19 on September 9. There were no significant
differences in egg densities on peak dates for three
Fig. 1. Egg density of pink bollworm on different cotton lines in 2001.
Values shown are means71 standard error. ANOVA indicates no generations among the treatments (df ¼ 3; 6; F ¼ 1:375;
significant differences in egg density among varieties on each sampled P ¼ 0:318; df ¼ 3; 6; F ¼ 0:317; P ¼ 0:813; df ¼ 3; 6;
date (P > 0:05). F ¼ 0:623; P ¼ 0:620). The larval density in BG1560

Table 2
Infestation of pink bollworm on different cotton lines in Tianmen, Hubei Province during 2001 and 2002

Year July Aug Sept Oct

Flowers Larvae per Bolls Exit holes per Bolls Exit holes per Bolls Larvae per
sampled hundred flowers sampled hundred bolls sampled hundred bolls sampled hundred bolls

2001 GK19 3294 1.0970.23b 1834 0.3170.18c 2173 0.7070.30b 600 9.1771.36b
BG1560 3318 0.3870.15b 1947 0.0870.08c 1964 1.4170.41b 600 3.0071.32b
HB3517 2376 5.5470.46a 1265 11.9571.75a 1738 23.2671.60a 600 87.5078.08a
HB3517 (chemical) 2578 1.2670.22b 1874 1.9970.44b 1756 2.8370.56b 600 13.1771.17b

2002 GK19 2774 2.6470.11bc 1257 0.0070.00c 1708 1.4770.46b 600 11.8371.17b
BG1560 2152 1.0470.14c 1211 0.0070.00c 1937 0.7070.52b 600 1.5070.50b
Simian3 1654 9.8371.14a 1015 13.6170.96a 1593 25.7273.27a 600 108.17711.13a
Simian3 (chemical) 1932 4.4970.48ab 1409 2.8270.40b 1894 3.9671.40b 600 15.0072.78b

Values with different letter(s), within a column in same year, are significantly different (Po0:05; LSD).
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466 P. Wan et al. / Crop Protection 23 (2004) 463–467

700
BG1560 (Bt)
season (Zhang et al., 2001). This study on pink
600 GK19 (Bt) bollworm also indicates that a few larvae can develop
Eggs per hundred plants

Simaian3 normally in the Bt cotton lines in September and


500 Simian3 (chemical)
October. However, the high efficacy in early season
400 would effectively decrease the risk that the pest would
300 have an outbreak in late season. Furthermore, long-term
studies indicate that Bt cotton use in Arizona has caused
200
regional suppression of pink bollworm, further con-
100 tributing to a reduced need for insecticide sprays
0 (Carriere et al., 2003). In any case, these late season
30-May 13-Jun 27-Jun 11-Jul 25-Jul 08-Aug 22-Aug 05-Sep 19-Sep larvae also do relatively little economic damage.
Date However, survival of pink bollworm on Bt cotton late
Fig. 2. Egg density of pink bollworm on different cotton lines in 2002. in the season may contribute to selection for resistance
Values shown are means71 standard error. ANOVA indicates no (Gould, 1998). Monocultures of lines that express Bt
significant differences in egg density among varieties on each sampled toxins continuously are likely to select intensively for
date (P > 0:05). resistance. Simulation studies and some experimental
data have shown that, without refuge populations, pest
flowers infested by pink bollworm in July was signifi- resistance to Bt cotton could appear rapidly with
cantly lower than in Simian3 with or without insecticide widespread use (Gould, 1998). Thus it is important to
use (df ¼ 3; 6; F ¼ 37:241; Po0:001) (Table 2). There consider how to delay the evolution of pink bollworm
were no exit holes to be found in the bolls sampled in resistance to Bt transgenic cultivars as the Mid-
August for either Bt cotton line, compared with 13.61 Changjiang River Valley opens to Bt cotton. Resistance
and 2.82 per hundred bolls in the Simian3 without and management strategies for Bt cotton and pink bollworm
with chemical control, respectively. In September, exit have been developed for the southwestern United States,
holes in the four treatments increased to 0.70 per including analyses of refuge design (Tabashnik et al.,
hundred bolls in BG1560, 1.47 per hundred bolls in 1997). In addition, resistance monitoring for this pest
GK19, 3.96 per hundred bolls in Simian3 with chemical has been conducted since 1996 in Arizona (Tabashnik
sprays, and 25.72 per hundred bolls in Simian3 without et al., 2000). However, the lower efficacy of Bt cotton
chemical use. The larval density in the Simian3 without against pink bollworm in our study than that in Arizona
chemical control in October was 108.17 individuals per indicates that further studies of Bt cotton deployment
hundred bolls, which was significantly higher than in and resistance management strategies in the Yangtze
any other treatment (df ¼ 3; 6; F ¼ 74:154; Po0:001) River Region are necessary.
Further area-wide planting of Bt cotton would
severely limit the numbers of immigant PBW to produce
4. Discussion late season infestationsy. In the USA re-Simulation
models, as far as the reviewer knows, have shown little
Our studies indicated that infestations of pink boll- or no resistance over several years of Bt planting in
worm in the Bt cotton lines developed by Monsanto Co. Arizona—a surprise.
and Biotechnology Research Institute of CAAS were
significantly lower than in the conventional lines in both
years of work. Compared with the larval density in the Acknowledgements
conventional lines without chemical control, the control
efficiencies were 89.42–100% for BG1560, 73.14–100% We thank Dr. Graham Head (Monsanto Company,
for GK19, and 54.32–87.83% for the chemical treatment St. Louis, USA) for critical review and discussion of the
of conventional cotton, where insecticides were sprayed manuscript. This research was supported by 973 Projects
9 times in 2001 and 11 times in 2002 for control of pink Grant (G001CB109004) and 863 Projects Grant
bollworm. We conclude that Bt cotton planted in the (2001AA212261) from the Ministry of Science and
Yangtze River Region possesses a high potential for Technology of China, and a Project from Monsanto
control of pink bollworm and would benefit the Company.
management of this pest in the region, though the
efficacy of Bt cotton against pink bollworm is lower
than that observed in Arizona (Flint and Parks, 1999).
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