Cotton Research
Institute
Chinese Academy of Agricultural Sciences
Anyang, Henan 455112????, China
(2 Current address:
National Agro-tech Extension & Service Center, Ministry of
Agriculture, No. 20 Maizidian Street, Beijing 100026, China)
ABSTRACT Resistance of
transgenic Bt plus CpTI cotton to H. armigera and its effects
on other insects were studied in laboratory, field-cage and
open-field from the view of bionomics, population ecology, community
ecology and integrated pest management. Transgenic Bt plus CpTI
cotton was highly resistant to cotton bollworms by feeding six
cotton-structures (leaf, square, petal, flower, bract and boll), and
it adversely affected their development, survival and reproductive
potential. The season-mean population numbers of sucking pests (A.
gossypii and T. cinnabarinus) on transgenic Bt plus CpTI
plants were slightly higher than those in non-transgenic control.
Abundance of predators (E. graminicolum and O.minutus)
in transgenic Bt plus CpTI cotton was increased compared with its
parental cultivar. Percentage of parasitization and adult emergence
of parasitoids (Microplitis sp. and C. chlorideae)
reared with transgenic Bt plus CpTI cotton-fed bollworm young larvae
(hosts) were all significantly decreased, compared with the
non-transgenic control-fed hosts. Insect communities of transgenic Bt
plus CpTI cotton were more stable and had better buffering action to
the changing from internal populations or the changing of environment
than those in non-transgenic control.
Key Words: Helicoverpa
armigera, transgenic Bt plus CpTI cotton, bionomics, population
ecology, community ecology, integrated pest management
China is the largest
cotton-producer in the World with about 4.5 million tons of lint
produced annually, which accounts for over 20% of the World’s
total production (Xia et al. 2001). Damage from pests is one
of the major limiting factors for cotton production in China, among
which cotton bollworm (Helicoverpa armigera Hübner) is a
key one (Fang et al. 1992). In the early 1990s, due to the
dramatic changes in cotton cropping systems, favorable weather
condition and rapid development of insecticide resistance, there had
been a serious bollworm outbreak in China, resulting in losses of
15-30% cotton lint (Xia, 1993, 1994, 1997). Cultivation of
insect-resistant cultivars proves an economical and feasible way for
bollworm control.
With the rapid development and
wide application of modern biotechnology, a great achievement has
been made in inserting insect-resistant genes from other organisms
into cotton. Scientists at Agracetus in USA were the first to
genetically engineer cotton plants expressing the δ-endotoxin
gene from Bacillus thruingiensis (Bt) var.kurstaki (Umbeck et
al. 1987). At the same time, scientists at Monsanto in USA
developed transgenic cotton plants containing Bt genes CryIA (b) from
bacterial strain HD-1 and CryIA (c) from HD-73 (Perlak et al.
1990). These transformed plants were effective in controlling
important lepidopterous cotton pests in laboratory, field-cage and
open-field evaluations (Benedict et al. 1993, 1996; Fitt et
al. 1994; Genkins et al. 1993; Halcomb et al. 1996;
Wilson et al. 1992).
Since the early 1990s, the Chinese
scientists have been working on genetically engineering cotton and
have successfully transformed the Bt gene cry1Ac into the
Chinese cotton plants (Cui and Guo, 1995; Ni et al. 1998; Xia,
1996; Xia et al. 1995; Xie et al. 1991). For the
resistance management of cotton bollworm to transgenic Bt cotton, the
Chinese scientists have also successfully inserted the Bt plus CpTI
(Cow pea Tripsin Inhibitor) gene into the Chinese cotton plants (Cui,
2003; Li et al. 2000, 2005).
So far, over 20 transgenic cultivars with gene
of Bt or Bt Plus CpTI have been bred and released in production,
demonstrating a high resistance to cotton bollworm (Cui and Guo,
1995; Ni et al.1998; Xia et al.1995b). Extension of
such transgenic cotton cultivars has brought about significant
economic, social and ecological benefits (Xia et al. 2006).
Xia et al. (2002) studied
in details the resistance of transgenic Bt cotton to H. armigera
and its effects on other insects in China. In the present paper, we
studied the resistance of transgenic Bt plus CpTI cotton to H.
armigera and its effects on other insects in China. All studies
were carried out in the China Cotton Research Institute (CCRI,
Anyang, Henan, China) during 1996-2006. The cotton cultivars were
CCRI 41 (transgenic Bt plus CpTI cotton) and CCRI 23 (non Bt cotton).
1 Resistance to Cotton
Bollworms
1.1 Variation in
resistance
The resistance of CCRI 41 to H.
armigera was studied in laboratory and field experiments. The
resistance was evaluated in terms of the bionomic responses to
feeding on various structures of host plants at different times of
the cropping season, and to various bollworm instars. Bollworms were
fed for 5 days in the laboratory with six structures of the
transgenic Bt plus CpTI and non-transgenic plants (leaves, bracts,
squares without bracts, petals, flowers without bracts and petals,
and small bolls without bracts) in June, July, August and September.
We also reared the 1st through 6th bollworm instars with six plant
structures for 5 days in the laboratory. The field experiment was
carried out in an insecticide-free field (2 ha) with Bt plus CpTI and
non-transgenic plants. Every 5 days from June to September, we
inspected the number of bollworm eggs and larvae from 10 randomly
selected plots (each with 10 plants).
Evaluation in the
laboratory indicated CCRI 41 was effective in killing H. armigera
young larvae, whereas the levels of resistance varied with the crop
stage, plant structure and larval age (size) (Table 1 and 2). The
mortality of bollworm young larvae fed six structures of the
transgenic plants was all significantly higher (P<0.05) than on
the respective controls. Thus, the corrected mortality of young
larvae fed each structure was computed for comparison, using the
formula of Abbott (1925). Clearly, the resistance of transgenic
plants to bollworm young larvae decreased with crop senescence, where
the mean-corrected mortality over six structures was 98.5% in June,
85.0% in July, 87.7% in August, and 80.4% in September (Table 1). The
season mean-corrected mortality of the young larvae was higher on
bracts and squares than on the leaves. Some researchers have observed
a decreasing level of H. armigera resistance in transformed Bt
cottons with crop senescence (Fitt et al. 1994; Xia et al.
1995b; Zhao et al. 1998a), and a low level of bollworm
resistance on petals and flowers in transformed Bt cottons (Dong et
al. 1997b; Zhao et al. 1998a).
The resistance of
transgenic cotton to bollworms decreased with larval age (Table 2).
Averaged over six structures, the mean-corrected mortality of the 1st
to 6th instars was approximately 85%, 80%, 70%, 60%, 30%,
and 10%, respectively. These results were consistent with those
observed in other transgenic Bt cultivars resistant to H.
armigera, H. Punctigera (Wallengren), H. zea
(Boddie) and H. virescens (Dong et al. 1997b；Fitt
et al. 1994; Halcomb et al. 1996; Xia et al. 1999;
Zhao et al. 1998b).
Evaluation in field
experiments showed that the transgenic Bt plus CpTI plants had little
influence on the number of bollworm eggs laid on them, but greatly
suppressed the larval populations in all three generations, thereby
reducing their damage from the insect. The season-mean number of eggs
laid on CCRI 41 in the field, over each sampling date, was only
slightly lower (0.27 per plant) than on the non-transgenic control
(0.32 per plant). The peak density of bollworm larvae on the
non-transgenic plants for the 1st to 3rd generation in the field cage
was significantly greater (1.21, 0.37 and 0.46 per plant,
respectively) than on the transgenic plants (0.14, 0.09 and 0.17 per
plant, respectively). Likewise, the season-mean number of larvae on
the non-transgenic plants in the field, over each sampling date, was
about 5 times that on the transgenic plants. The percentage of
injured terminals and squares plus boll on the non-transgenic control
in the field, averaged over three generations, was significantly
greater (46-91%) than on the transgenic plants (16-18%). Field
evaluations in USA and Australia demonstrated a similar efficacy of
transgenic Bt cottons in suppressing populations of H.virescens,
H. zea, H. armigera, H. punctigera and
PectinoPhora gossypiella (Saunders) (Benedict et al.1993;
Fitt et al. 1994; Sachs et al.1996; Wilson et
al.1992).
1.2 Effect on
bionomics
The resistance mechanism of CCRI
41 to H. armigera was studied with respect to effects on
insect bionomics. We continuously reared each larval instars until
death with the six plant structures in the laboratory, to determine
their effects on survival, growth and reproductive potential of H.
armigera.
Transgenic Bt plus CpTI cotton
adversely affect development, survival and reproductive potential of
H. armigera. The weight of larvae, larval duration, pupated
rate, weight of pupae, pupae duration, molting rate and lifespan of
adult of bollworms, fed various structures of Bt plus CpTI cotton,
were all decreased, compared with the non-transgenic control (Tables
3). No larvae of the 1st to 4th instars, fed
leaves, bracts, squares, petals and flowers of CCRI 41，could
survive to pupation. The duration of 6th instars on all
tested structures of the transgenic Bt plus CpTI cotton was
significantly longer than on the non-transgenic control. The weight
of 6th instars fed all structures of the transgenic Bt
plus CpTI cotton was less than that on the respective control.
It was commonly
observed that the 1st to 4th instars of H. armlgera, H. zea
and H. virescens larvae fed transgenic Bt cotton could not
survive to pupation (Halcomb et al. 1996; Zhao et al.
1998b). A decrease in development and survival rates of those
lepidopterous immatures has been reported in other transgenic Bt
cotton (Benedict et al.1992, 1993; Dong et al.1997b;
Fitt et al. 1994; Holcomb et al.1996; Jenkins et al.
1993; Zhao et al. 1998b) and Bt diets (Could et al. 1991),
though little has been known about their effects on the insect
reproductive potential.
2 Effects on Other
Herbivores
2.1 Effects on
other lepidopterous pests
Except for the main
target, H. armigera, there are several other lepidopterous
pests frequently causing damage to cotton, such as cut worm (Agrotis
ipsilon Hüfnagel), corn borer (Ostrinia furnacalis
Hübner) and small looper (Anomis flava Fabricius) (Fang
et al. 1992). We evaluated the resistance of CCRI 41 to A.
ipsilon in the laboratory, by feeding their neonates until death
with the young leaves from field-grown transgenic Bt plus CpTI and
non-transgenic plants.
Laboratory evaluation
revealed detrimental effects of CCRI 41 on the survival and growth of
cutworms (Table 4). The percentage of cutworm larvae surviving to
pupation and then to the adults (25.6%) on the transgenic Bt plus
CpTI (30.0% and 32.2%, respectively) was significantly lower than on
non-transgenic control (85.0% and 75.0%, respectively). Compared with
the non-transgenic control, the cutworm larval weight (at day 6) and
pupa weight at day 6 on the transgenic plants was decreased. These
results are consistent with those in transgenic Bt cotton (Cui et
al. 2002; Xia et al. 2001).
2.2
Effects on non-lepidopterous pests
Besides the
lepidopterous pests, there are several sucking pests injurious to
cotton, such as cotton aphid (Aphis gossypiii Glover), red
spider mite (Tetranychus cinnabarinus Boisduval) and thrips
(Thrips tabaci Lindeman). We sampled A. gossypii and
T. cinnabarinus on each phenotypic cotton from randomly selected
10 plots (each with 10 plants) in an unsprayed field (1.5 ha), every
5 days from April to September.
Compared to the non-transgenic
control, abundance of cotton aphid (Fig.1) and red spider mite
(Fig.2) was increased on transgenic Bt plus CpTI plants. The
season-mean population numbers of these two pests on the Bt plus CpTI
plants, were increased by 21.6% and 158.3% at a higher peak density,
respectively. These sucking pests have been also observed more
abundant on transgenic Bt plants in single cotton and cotton / wheat
intercropping systems (Cui, 1998; Cui and Xia, 1998; Xia et al.
1999). Wilson et al.（1992）
reported
higher populations of Bemisia tabaci (Gennadius) on the
transgenic Bt plants than on the non-transgenic control. An increased
abundance of sucking pests on transgenic Bt plus CpTI cottons may
have been a consequence of reduced leaf feeding damage by
lepidopterous insects rather than increased susceptibility of
transformed plants to those pests (Cui, 1998; Cui and Xia, 1998;
Wilson et al. 1992).
3 Effects on Major
Predators
3.1 Effects on
functional response
Several predators
have been recorded to attack H. armigera larvae, such as
Propylaea japonica Goeze, Coccinella septempunctata
L.，Orius
minutus L.and Erigonidium graminicolum Sundevall. We
determined the effects of CCRI 41 on the functional responses of
these four predators to H. armigera in the laboratory by
rearing the field-collected adult predators (2-5 days old) with
transgenic Bt plus CpTI cotton-fed and non-transgenic cotton-fed
young larvae (prey), and then fitting the data with Holling's (1959)
typeⅡ predation equation. For all predators tested, the prey
density levels were 20, 40, 60, 80 and 120, each with 5 replicates.
Laboratory evaluation
indicated an increase in maximum predation （Na）and
search rates ( a ) but a decrease in handling time （Th）for
all tested predators preying on the transgenic Bt plus CpTI cotton
fed-prey in comparison with the Bt-free prey (Table 5). The handling
time of P. japonica preying on the Bt plus CpTI cotton
fed-larvae was decreased by over 3.8%, though it was decreased by
less than 29.2 % for the non-transgenic cotton predators. The search
rate of E. graminicolum preying on the transgenic Bt plus CpTI
cotton-fed larvae was decreased on the Bt-free prey, while it was
increased by 27.1 % for the non-transgenic cotton predators. P.
Japonica was more effective in preying on the Bt plus CpTI
cotton-fed bollworm larvae than the other predators because its
maximum predation rate was more that on the control. Increased
predation rate of those predators could be due to the smaller size
and less vigor of the transgenic Bt plus CpTI cotton-fed prey. A
similar trend has been also observed in transgenic Bt cotton (Cui, et
al. 2005; Xia et al. 2001).
3.2 Effects on
predator population dynamics
The population
dynamics of E. graminicolum and P. japonica on
transgenic Bt plus CpTI cotton was studied in field experiments.
Every 5 days from April to September, the population numbers of these
two predatory species on each phenotypic cotton were inspected from
randomly selected 10 plots (each with 10 plants) in an insecticide
free-field.
Field evaluation
revealed an increased abundance of E. graminicolum (Fig.3) but
a decreased abundance of P.japonica (Fig.4) on transgenic Bt
plus CpTI cotton, compared with its parental cultivar. The
season-mean numbers of E. graminicolum on transgenic Bt plus
CpTI plants, compared with the transgenic Bt control, were increased
by 4.5% with the highest peak density increased by 9.5%. The
season-mean number of P. japonica on the transgenic plants was
increased by by 7.5 % with its highest peak density increased by
8.9%, compared with the non-transgenic control. An increased
abundance of E. graminicolum on the transgenic plants may have
resulted from the increased populations of some sucking insects
(prey), noticeably cotton aphid (Fig. 1). Reduced P. japonica
populations on the transgenic plants may be ascribed to the dramatic
decrease in bollworm larval populations ( Fig.4 ) which this predator
actively consumes (Table 5). Helbeck et al.（1998a,
b ）
showed
that the mean total immature mortality for Chrysoperla carnea
Stephens, raised on the transgenic Bt corn-fed Ostrinia nubilalis
(Hübner) and Spodoptera Iittoralis (Boisduval), was
significantly higher than those raised on the Bt-free prey, and their
development time was longer than that in control. They further
observed that the cryIA (b) was toxic to C. carnea at 100 ug /
ml of the encapsulated artificial diets.
4 Effects on Major
Parasitoids
4.1 Effects on
parasitism
More than 10
parasitoid Species have been known to attack the different life
stages of lepidopterous pests in cotton (Fang et al. 1992).
Two of them, Microplitis sp. and Campoletis chlorideae
Uchida, are often found to parasitize H.armigera larvae with
parasitization ranging from 2-36 % (Cui, 1998; Fang et al .1992).
The effect of CCRI 41 on parasitism of these two parasitoids was
evaluated in the laboratory, by rearing them with transgenic Bt plus
CpTI cotton-fed and non-Bt fed bollworm young larvae (hosts).
Transgenic Bt plus
CpTI cotton affected the survival and growth of Microplitis
sp. and C.chlorideae. The percentage of parasitization and
adult emergence, as well as the weight of cocoons and adults of both
parasitoids reared with Bt plus CpTI cotton-fed bollworm young
larvae, were all significantly decreased compared with the
non-ransgenic control-fed hosts (Table 6). The mechanism for
transgenic plants to affect parasitism of both larval parasitoids is
similar to that of commercial Bt products as observed by (Salama et
al. 1982; Qing, et al. 2004).
4.2
Effects on parasitoid population dynamics
Population dynamics
of Microplitis sp in transgenic Bt plus CpTI cotton was
studied in the field experiments. Its population numbers in each
phenotypic cotton were observed from randomly selected 10 plots (each
with 10 plants) in an insecticide-free field (2 ha), every 5 days
from June to September.
Field observation showed a
significantly reduced abundance of Microplitis sp. on CCRI 41,
compared with the non-transgenic control (Fig. 5), as there were
fewer larvae to parasitize. Thus, the season-mean number of
Microplitis sp. on the non-transgenic control was 7-11 times that
on the transgenic Bt plus CpTI plants. This evidence further
indicates that transgenic plants exert a similar impact on bollworm
larval parasitoids as commercial Bt products (see also Johnson and
Gould, 1992).
5 Effects on
Arthropod Community
5.1 effects on
species composition
We evaluated the
effect of transgenic Bt plus CpTI plants on arthropod com-mutinies in
an unsprayed field, using the method described by Xia et al.
(1995a). Field evaluation revealed no adverse effect of CCRI 41 on
species composition of arthropod communities. The number of arthropod
species on the transgenic Bt plus CpTI plants was 50 (from 14 Orders
and 37 Families), comprised of 27 pest and 23 beneficial species. How
about on non-transgenic control?????. The same pattern has also been
observed in transgenic Bt cotton (Xia et al. 2001).
5.2 Effects on
characteristic indices
As shown in Table 7,
the dominance indices of three major sucking pests (A. gossypii,
T. cinnabarinus and T. tabaci) and three major
predators (E. graminicolum, O. minutus and C.
septempunctata) on the transgenic Bt plus CpTI cotton were
slightly increased, compared with the non-transgenic control. These
results were consistent with those observed from the field-population
dynamics of those pests (Fig 1and 2) and predatory species (Figs 3
and 4). However, the dominance indices of H. armigera and its
larval parasitoids were significantly decreased compared with the
non-transgenic control (Table 7). Interestingly, the dominance index
of A. gossypii parasitoid complex on the transgenic plants was
decreased by over 30 % compared with the non-transgenic control in
laboratory experiments, which was not coupled with the increased
abundance of A. gossypii on the transgenic plants (Fig.1).
This may be an indication that some metabolic changes in transgenic
cotton plants (e.g. changes in content of some secondary compounds)
could exert certain adverse effects on A. gossypii parasitoids
attacking the transgenic Bt plus CpTI cotton-fed hosts.
Three characteristic
indices (diversity, evenness and dominance concentration) are
considered important indicators of stability for an arthropod
community. In general, an arthropod community is more stable when it
is higher in diversity and evenness but lower in dominance
concentration and complexity (Cui, 1998; Xia et al. 1995a,
1998). The index of diversity and evenness on the transgenic Bt plus
CpTI plants was decreased compared with the non-transgenic control
(Table 7). Presumably, the arthropod community on transgenic plants
might be more stable than that on the non-transgenic control.
6. General
Discussions and Future Research
6.1 Insect
Resistance
Transgenic Bt plus
CpTI cottons demonstrated a high efficacy to control H.armigera
in laboratory, and in field experiments, though their resistance
levels varied with the crop stage and plant structure. The
spatiotemporal dynamics of insect resistance in the transgenic cotton
could be mainly attributed to the variation in Bt expression with
crop age (Sachs et al. 1998) and among plant structures
(Benedict et al.1996; Sims et al. 1996). Spatiotemporal
changes in Bt expression might be caused by genetic and environmental
factors such as site of insertion, gene construct, background
genotype, epitasis, somaclonal mutations, metabolism associated with
plant growth and reproduction, temperature, nitrogen and soil water
(Benedict et al. 1993, 1996; Sachs et al. 1998). The
spatiotemporal variation in Bt expression of current transgenic Bt
plus CpTI cottons would provide an ideal environment for selection of
endotoxin resistance by insects, thus challenging the high-dosage
strategy for endotoxin resistance management (Fitt et al.
1994; Forrester, 1994; Xia et al.1999). Variation in Bt
expression could also pose a question on how to control H.
armigera at the late crop stage if population numbers would be
above the recommended action threshold for conventional cultivars.
Two main mechanisms
are involved in the resistance of transgenic Bt cottons to target
pests: ( 1 ) by poisoning and killing the target pests at the
specific stage (larvae), and (2) by reducing reproductive potential
of the infested pests (Benedict et al. 1992, 1993; Dong et
al. 1997a；Xia
et al. 1999). Decreased reproductive potential of Bt plus CpTI
cotton-infested H. armigera would increase, to some extent,
the effectiveness of control, the significance of which needs to be
further examined and understood.
6.2 Ecological
Impacts
There are a number of
potential ecological impacts of transgenic Bt plus CpTI cottons in
cotton production systems, among which, three should be taken in to
consideration from the entomological point of view.
Impact on pest
species. Transgenic Bt plus CPTI cottons prove effective for
controlling a variety of lepidopterous pests, Helicovepa spp.，
H.
virescens, P. gossypiella and A. ipsilon. All these
species may pose some risk of evolving resistance to the Bt endotoxin
(Fitt et al. 1994 ; Forrester, 1994; Roush, 1994). It has been
observed that some non-target sucking pests, such as A. gossypii,
and T. cinnabarinus are more abundant on transgenic Bt plus
CpTI cottons than on the non-transgenic cultivars. Reduced chemical
use for controlling the main target bollworms on transgenic Bt plus
CpTI cottons may favor some minor pests such as Empoasca biguttula
Shiraki, Creontiades dilutus Stal, Campylomma livida
Reuter and Lygus luconum Meyer-dur (Cui, 1998; Cui and Xia,
1998; Fitt et al.1994). These sucking insects may, in turn, be
so important that pesticides may become a critical management option,
thereby devaluing the gains from the transgenic expression system.
Population dynamics of major non-target sucking pests should be well
understood for effective integrated pest management in transgenic Bt
plus CpTI cottons.
Impact on natural
enemies. Potential impact of transgenic cottons on beneficial
arthropods is derived from removal of lepidopterous eggs, larvae and
pupae as food source for predators or as hosts for parasitoids. The
significance of this impact depends largely on the importance of the
lepidopterous life stage on cotton in maintaining local beneficial
populations, and also on their feeding ecology. Clearly, transgenic
Bt plus CpTI cottons impose a greater impact on the specialized
parasitoids than on the generalist predators. Predators closely
associated with lepidopterous pests (e.g. P. japonica) suffer
a greater adverse effect compared with the more generalist ones (see
also Helbeck et al. 1998a, b). Trichogramma spp., the
important bollworm egg parasitoids, may also be influenced due to the
deterioration of eggs laid by Bt plus CpTI cotton-infested adults.
The effect of transgenic Bt plus CpTI cottons on the bionomics and
feeding ecology of these important beneficial species should be
further investigated.
Impact on
endotoxin resistance. The development of insect resistance to Bt
proteins is, currently, of the greatest concern to the scientists and
public (Benedict et al. 1993; Fitt et al. 1994;
Forrester, 1994; Kennedy and Whalon, 1995. With the ecology of H.
armigera and its historical development of insecticide resistance
taken into consideration, it seems that this insect is likely to
develop resistance to transgenic Bt cotton, as there is a persistent
expression of Bt proteins in them. The persistent Bt expression in
host plants may lead to the potential for continuous selection for
resistance. Even the transgenic Bt plus CpTI cotton possesses two
genes, its risk for development of endotoxin resistance should be
carefully evaluated.
6.3 Management
prospects
The development, evaluation and
implementation of resistance management strategies for transgenic Bt
plus CpTI cotton may be a major factor for their commercialization in
China cotton region because of the lesson from H. armigera
outbreaks, mainly attributed to pyrethroid resistance (Xia, 1993,
1994). Several resistance management strategies for transgenic Bt
cottons have been developed and evaluated, such as a mixture of
transgenic with non-transgenic seeds, cultivation of refugia, and
high dose exposure (Mcgaughey and Whalon, 1992; Roush, 1994; Xia et
al. 2003). The seed mixture would cause severe damage to the
crops as old bollworm larvae could disperse from non-transgenic to
the transgenic plants (Dong et al.1998b; Xia et al.
1995b). The refuge strategy would be not necessary (provided that
there is no simultaneous cultivation of other transgenic Bt crops),
as there exist diversified multi-cropping patterns for bollworm
hosts, and also, bollworm adults are highly mobile (Xia, 1994; Zhao
et al. 1998b). The high dosage strategy appears to be more
applicable and feasible, though it still faces some challenges, such
as a lower Bt-expression in flowers of the current transgenic Bt
lines, and later in the crop season. Thus, more efforts should be
made on time-specific or tissue-specific expression of Bt endotoxins
in transgenic plants, and to pyramid, in the same plants, the Bt
endotoxin with other foreign insecticidal genes or with the native
insect resistance traits (e.g. nectariless, okra leaf and high
terpenoid content) (Benedict et al.1993; Cui and Guo, 1995;
Sachs et al. 1996, 1998; Wilson et al.1992; Xia, 1996).
It should be remembered that
management of Bt-endotoxin resistance is only one component in
integrated cotton pest management system. As current transgenic Bt
plus CPTI cotton prove effective only for controlling some
lepidopterous pests, there is a need for developing a more
comprehensive transgenic cotton-based system for integrated pest
management on cotton. For these reasons, the seasonal pattern of
arthropod communities and population ecology of some key insects at
different trophic levels on transgenic cottons should be well
understood. Our findings from these preliminary studies showed
evidence of alterations in structures of arthropod communities and in
population dynamics of some important insect species at different
trophic levels on transgenic Bt plus CpTI cotton. Because of such
changes, some conventional pest control tactics should be adopted
accordingly. Thus, application of selective pesticides should be
highlighted to optimize natural controls. Economic thresholds of
important pests (e.g. A. gossypii, T. cinnabari, and H.
armigera at late season) may have to be re-determined due to the
changes in pest status and beneficial insect abundance. Further
research on all these aspects, accompanied with a better
understanding of the ecological impacts of transgenic Bt cottons on
arthropod communities at each of three trophic levels, would greatly
assist in scientifically utilizing modern transgenic cotton crops.
Acknowledgements
We are grateful to C. Y. Wang, C. H. Li and
Q. Zhao for their assistance with the experiments.
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Table 1 Effect of
transgenic Bt plus CpTI cotton on mortality of cotton bollworm larvae
Month | Varieties | Mortality of cotton bollworm larvae (%) |
Leaf | Square | Petal | Flower | Bract | Boll |
| Jun. | Bt+CpTI | 98.2±1.53a | 98.9±1.85a | --- | --- | 98.5±3.41a | --- |
| Non-Bt | | | | | | |
Jul. | Bt+CpTI | 64.3±2.12a | 94.1±3.33a | 92.9±0.98a | 70.3±7.26a | 94.3±4.12a | 94.3±4.12a |
| Non-Bt | | | | | | |
Aug. | Bt+CpTI | 65.7±12.76a | 87.6±14.07a | 96.9±0.69a | 87.8±12.16a | 100±0.0a | 88.4±7.24a |
| Non-Bt | | | | | | |
Sept. | Bt+CpTI | 35.2±14.72a | 97.1±0.46a | 97.0±2.63a | 81.5±2.98a | 85.6±1.96a | 86.0±3.00a |
| Non-Bt | | | | | | |
The same letter indicates the
difference is not significant, and the different letter indicates the
difference is significant (p<0.05 or p<0.01).
Table 2 Efficacy of transgenic
Bt plus CpTI cotton to different instar larvae of cotton bollworm in
the 6th day
Structures | Cultivars | Mortality of different instar larvae of cotton bollworm (%) |
1st | 2sd | 3rd | 4th | 5th | 6th |
Leaf | Bt+CpTI | 98.7±1.2A | 98.9±1.9A | 96.7±3.4A | 86.8±10.0A | 50.0±8.8A | 21.1±5.10A |
Non-Bt | 28.0±5.3B | 30.0±3.3B | 7.8±3.8B | 15.5±3.8B | 5.5±3.9B | 5.5±3.8B |
Square | Bt+CpTI | 99.3±1.2A | 84.4±7.6A | 85.6±5.1aA | 55.6±8.4A | 35.6±5.1A | 35.6±15.4A |
Non Bt | 44.0±5.3B | 6.7±3.4B | 28.4±8.8B | 18.9±11.7B | 4.4±5.1B | 16.7±6.6B |
Flower | Bt+CpTI | 91.1±2.0aA | 97.8±1.9aA | 81.1±15.8aA | 81.1±1.9A | 30.0±7.6A | 17.8±6.9A |
Non Bt | 40.0±20.2B | 39.4±1.9B | 23.3±10.0B | 20.0±8.8C | 5.6±5.1B | 5.6±1.9B |
petal | Bt+CpTI | 96.1±1.0aA | 100±0.0A | 93.3±3.4aA | 54.4±11.7A | 36.7±9.0A | 21.2±8.4A |
Non Bt | 45.0±5.7B | 38.3±8.6B | 21.1±5.1B | 23.3±6.7B | 7.8±5.1B | 0.0±0.0B |
Bract | Bt+CpTI | 100±0.0A | 96.7±3.4A | 87.8±7.7A | 53.3±4.4A | 40.0±6.7A | 22.2±10.2A |
Non Bt | 28.9±3.5C | 18.9±10.2C | 17.8±3.8B | 15.5±2.5B | 17.8±1.9B | 4.5±3.9B |
Boll | Bt+CpTI | 96.7±1.6A | 75.0±6.7aA | 68.9±1.9A | 48.9±1.9aA | 26.7±8.8a | 16.7±3.4a |
Non Bt | 67.3±4.1B | 25.5±6.9B | 27.8±5.1B | 13.3±6.7B | 4.5±3.8b | 1.1±1.9b |
The same letter indicates the
difference is not significant, and the different letter indicates the
difference is significant (p<0.05 or p<0.01).
Table 3 Effect of transgenic Bt
plus CpTI cotton on the development of 6th instar larvae of cotton
bollworm
Items | Treatments | Leaf | Square | Flower | Petal | Bract | Boll |
Weight of larvae (mg) | Bt+CpTI | 261.5±72.9a | 181.1±21.4a | 252.0±19.7a | 244.8±10.8a | 179.5±14.0a | 238.2±9.6a |
Non-Bt | 373.5±16.2c | 290.1±32.5c | 319.7±23.1c | 312.7±15.2c | 284.5±6.4c | 338.9±45.6c |
Larval duration (d) | Bt+CpTI | 3.2±0.2a | 4.5±0.2a | 4.0±0.2a | 4.2±0.8a | 5.1±0.3a | 4.0±0.1a |
Non-Bt | 2.1±0.1b | 3.6±0.5b | 3.3±0.6b | 4.2±0.3a | 5.1±0.1a | 3.3±0.6b |
Pupated rate (%) | Bt+CpTI | 25.6±12.6aA | 44.4±2.0aA | 53.3±3.4aA | 55.5±6.9A | 25.5±15.4A | 58.9±13.4A |
Non-Bt | 87.2±6.1B | 82.2±8.4B | 77.8±5.1B | 83.3±3.2C | 75.6±2.0bB | 90.0±3.4B |
Weight of pupae (mg) | Bt+CpTI | 144.7±15.3a | 168.5±20.3a | 203.9±10.2a | 181.6±6.0a | 131.4±1.3a | 207.8±17.0a |
Non-Bt | 220.4±27.6c | 242.3±34.0c | 262.0±8.5c | 205.7±3.0c | 211.8±12.8c | 257.3±7.1c |
Pupae duration (d) | Bt+CpTI | 11.5±0.7a | 10.0±1.0a | 9.7±0.6a | 9.4±0.5a | 9.8±1.1a | 10.3±1.2a |
Non;Bt | 9.0±0.0b | 10.2±0.3a | 10.0±0.0a | 9.0±0.0a | 10.0±0.0a | 9.7±1.2a |
Molting rate (%) | Bt+CpTI | 25.6±12.6A | 36.7±3.4A | 27.8±8.4aA | 32.3±1.9A | 5.6±5.1A | 45.5±10.7a |
Non;Bt | 82.2±6.9B | 72.2±3.9B | 62.9±8.4B | 78.9±2.0C | 63.3±11.6B | 61.1±5.1a |
Lifespan of adult(d) | Bt+CpTI | 5.3±0.6a | 6.0±0.9a | 9.8±0.3a | 8.0±1.0a | 9.5±1.4a | 10.3±0.3a |
Non;Bt | 8.8±1.0b | 7.8±0.8a | 10.0±0.0a | 10.0±1.0a | 8.7±1.2a | 10.3±0.6a |
The same letter indicates the difference is
not significant, and the different letter indicates the difference is
significant (p<0.05 or p<0.01).
Table 4 Survival
and growth of A. ipsilon fed transgenic Bt plus CpTI cotton
leaves in laboratory
Items | Bt+CpTI | Non-Bt |
Larval weight (g) at day 6 | 0.0031±0.0004bA | 0.0040±0.0010cA |
% larval survival to pupation | 30.0±3.3aA | 85.0±5.0bA |
Larval duration (d) | 30.7±2.08aAB | 28.4±1.115bB |
Pupa weight (g) at day 6 | 0.3224±0.0454aA | 0.4040±0.0446bA |
% pupal survival to adults | 25.56±5.09aA | 75.0±0.00bB |
Pupal duration (d) | 13.1±0.31bA | 11.3±0.10aB |
The same letter indicates the difference is
not significant, and the different letter indicates the difference is
significant (p<0.05 or p<0.01).
Table 5. Maximum
Predation rate (Na，d
–1), search rate (a, d d –1) and
handling time (Th, h) of four major predators preying on
H. armigera young larvae, fed transgenic Bt plus CpTI and
non-transgeic cotton leaves in laboratory, based on type Ⅱ
functional response of Holling (1959)
| Predator | Treatment | Na | a | Th |
| p.japonica | Bt+CpTI | 125.1 | 1.1213 | 0.0080 |
| | Non- Bt | 88.9 | 1.1774 | 0..113 |
| C.septempunctata | Bt+CpTI | 243.0 | 0.7263 | 0.0041 |
| | Non- Bt | 97.1 | 1.1419 | 0.0103 |
| O.minutus | Bt+CpTI | 84.9 | 0.4994 | 0.0118 |
| | Non- Bt | 69.0 | 0.4421 | 0.0143 |
| E.graminicolum | Bt+CpTI | 49.2 | 0.7309 | 0.2030 |
| | Non- Bt | 35.9 | 1.3740 | 0.2785 |
The same letter indicates the difference is
not significant, and the different letter indicates the difference is
significant (p<0.05 or p<0.01).
Table 6. Survival and growth of Microplitis sp.
and C. chlorideae parasitizing H. armigera young larvae
(n=50), fed transgenic Bt plus CpTI and non-transgenic cotton leaves
in laboratory
| Parameter | Treatment | C.chlorideae | Microplitis sp. |
| %larvae parasitized | Bt+CpTI | 43.3 aA | 21.6 aAB |
| | Non- Bt | 80.6Ac | 32.6 aAC |
| Cocoon wt at day 3(g) | Bt+CpTI | 0.0067 aA | 0.0038aA |
| | Non- Bt | 0.0087cB | 0.0051 cC |
| %adult emergence | Bt+CpTI | 73.6 aA | 47.7aA |
| | Non- Bt | 100cC | 100 cC |
| Adult wt at emergence(g) | Bt+CpTI | 0.0008 aA | 0.0006aA |
| | Non- Bt | 0.0009bA | 0.0007 bA |
The same letter indicates the difference is
not significant, and the different letter indicates the difference is
significant (p<0.05 or p<0.01).
Table 7 Comparison of
characteristic indexes of arthropod communities on transgenic Bt plus
CpTI and non-transgenic cotton plants in an unsprayed field
| Parameter | Bt+CpTI | Non- Bt |
| Dominance index | | |
| A.gossypii | 0.8817 | 0.8067 |
| T.tabaci | 0.0233 | - |
| H.armigera | - | 0.0137 |
| E.graminicolum | 0.3559 | 0.2150 |
| C.septempunctata | 0.0717 | 0.0811 |
| P.japonica | 0.2629 | 0.1923 |
| O.minutus | 0.0186 | 0.571 |
| Diversity index | 1.2157±0.1933aA | 1.1185±0.1533 abA |
| Evenness index | 0.3109±0.0538 aA | 0.2857±0.0335 aA |
| Dominance concentration index | 0.5731±0.073 abA | 0.6183±0.0536 abA |
The same letter indicates the difference is
not significant, and the different letter indicates the difference is
significant (p<0.05 or p<0.01).
Fig.1.
Population dynamics of A. gossypii in transgenic Bt plus CpTI
cotton
Fig
2 Population dynamics of T. cinnabarinus in Bt plus CpTI
cotton
Fig.3
Population dynamics of E. gramicicolum in transgenic Bt plus
CpTI cotton
Fig.4
Population dynamics of P. japonica) in transgenic Bt plus CpTI
cotton
Fig.
5. Population dynamics of Microplitis sp. n transgenic Bt plus
CpTI cotton
