全 文 ：第 51 卷 第 9 期
2 0 1 5 年 9 月
林 业 科 学
SCIENTIA SILVAE SINICAE
Vol. 51，No. 9
Sep．，2 0 1 5
doi:10．11707 / j．1001-7488．20150909
Ｒeceived date: 2014 － 02 － 28; Ｒevised date: 2014 － 08 － 28．
Fund project: The Natural Science Foundation of Hebei Province，China ( C2011204041) ; The Youth Science Foundation of Hebei Agricultural
University，China(QJ201211) ;Key Lab． of Forest Germplasm Ｒesource and Protection of Hebeiprovince．
应用白僵菌防治美国白蛾的潜力
李会平 黄秋娴 王 婧 李 雯
(河北农业大学林学院 保定 071000)
摘 要: 【目的】测定来自不同寄主和生境的白僵菌对美国白蛾的致病力，以明确白僵菌应用于美国白蛾
的生防潜力。【方法】以自土壤诱集的白僵菌 BS04，BS05，BS08 菌株和分离自美国白蛾幼虫和桑天牛幼虫的
BH01，BI05 为供试菌株，利用 POTTEＲ 喷雾塔对美国白蛾幼虫用1 × 10 8孢子·mL － 1的白僵菌孢子悬浮液进行
喷雾处理，逐日观察记载死亡率。对筛选出的高毒力菌株用 1 × 10 4，1 × 10 5，1 × 10 6，1 × 10 7 和 1 × 10 8孢子
·mL － 1系列浓度的白僵菌孢子悬浮液进行喷雾以测定其致死中浓度 LC50。对筛选出的高毒力菌株进行野外
田间试验，共设置白僵菌 BH01 的 8 × 10 8 孢子悬浮液，4. 5% 高效氯氰菊酯 2 000 倍液和清水对照 3 个处理，
用泰山 ft-796 型喷雾器进行喷雾，分别于处理后 3，5 和 7 天调查统计死亡率。【结果】BS08，BH01 和 BI05
菌株接种美国白蛾幼虫 8 天后，其死亡率为 70% ～ 85% ，而另外 2 个菌株的致死率仅为 32. 61% 和
30. 43% ，其致死中时 LT50值亦明显低于菌株 BS04 和 BS05。利用不同孢子浓度的悬浮液对美国白蛾幼虫进
行接种，进一步测定了上述 3 个菌株的致死中浓度，菌株 BH01 的 LC50值为 1. 39 × 10
6 孢子·mL － 1，明显低于
菌株 BS08 和 BI05(分别为 1. 34 × 10 7和 2. 11 × 10 7 孢子·mL － 1 )。田间试验表明，处理 7 天后，BH01 的防
治效果达 88. 84% ，与 4. 5% 高效氯氢菊酯无明显差异。【结论】白僵菌 BH01 菌株的 10 8 孢子·mL － 1孢子悬
浮液对美国白蛾幼虫具有较高的毒力，显示出用于防治美国白蛾幼虫的生防潜力。
关键词: 美国白蛾; 白僵菌; 生物防治; 筛选; 潜力
中图分类号: S763. 306 文献标识码: A 文章编号: 1001 － 7488(2015)09 － 0065 － 06
Potential of Entomopathogen Beauveria bassiana for Controlling Fall
Webworm Hyphantria cunea
Li Huiping Huang Qiuxian Wang Jing Li Wen
(Forestry College，Agricultural University of Hebei Baoding 071000)
Abstract: 【Objective】Hyphantria cunea (Drury) is a serious destructive insect pest with widespread distribution in
China． It usually lives and attacks fruit and ornamental trees，especially broad-leaved trees． The pest has become a big
problem to agriculture and forestry in northern China． Up to now，control strategies for H． cunea populations still depend
to a large extent on the use of insecticides． However，the resistance development to insecticides and the insecticide-caused
environmental pollution stimulate people to search for safely alternative methods to control the pests． Beauveria bassiana，
as one of the most common entomopathogenic fungi，has long been recognized as a potential biocontrol agent and actively
been developed to control various pest insects． However，there is significant difference in pathogenicity among different
strains of B． bassiana，and there exists obvious host specificity in different strains． Thus，it is feasible to enhance the
specialization and the pathogenicity of B． bassiana to some kind of pests through artificial orientation training． The
virulence of five B． bassiana isolates from different hosts or habitats to larvae of H． cunea was studied to exploit the
potentiality of B． bassiana for controlling H． cunea． ［Method］5-instar larvae of H． cunea were used to investigate the
effectiveness of five B． bassiana isolates，BS04，BS05 and BS08 from soil，BH01 from larvae of H． cunea，BI05 from
larvae of Apriona germari (Hope) ． The larvae of H． cunea were sprayed with 1 × 108 conidia·mL － 1 conidial suspension of
diferent B． bassiana isolates using POTTEＲ spray tower． Mortality was recorded daily for eight days． For the highly
virulent isolates identified in the above bioassay，larvae were sprayed with five serial concentrations of conidia (1 × 104，
林 业 科 学 51 卷
1 × 105，1 × 106，1 × 107 and 1 × 108 conidia· mL － 1 ) to determine the lethal concentration ( LC50 ) ． In the field
experiment，there were three treatments，including 8 × 108 conidia·mL － 1 of B． bassiana BH01，4． 5% β-cypermethrin
2000 times liquid and the water control． A Taishan ft-796 sprayer was used to routinely spray． The mortality was counted
in 3，5 and 7 d post experiment，respectively． ［Ｒesult］The isolates of BS08，BH01 and BI05 caused mortalities between
70% and 85% in eight days post-inoculation while the other two isolates only caused mortalities of 32． 61% and 30． 43%，
respectively． The LT50 values of BH01，BS08 and BI05 were shorter significantly than that of the other two isolates． The
LC50 values of BH01 (1． 39 × 10
6 conidia·mL － 1 ) was lower than that of BS08 and BI05 (1． 34 × 107 and2． 11 × 107
conidia·mL － 1 ) ． The field experiment showed that in seven days after treatment the control effect of BH01 (88． 84% )
had no significant difference with that of 4． 5% β-cypermethrin． ［Conclusion］This study demonstrates that a suspension
containing 108 conidia·mL － 1 of a B． bassiana strain BH01 is highly virulent and has excellent potential for biological
control of H． cunea．
Key words: Hyphantria cunea; Beauveria bassiana; biological control; screening; potential
Hyphantria cunea ( Drury ) is a serious invasive
defoliator pest in China． It originally distributed in North
America，ranging from Canada to Mexico，and was one of
the few insect pests introduced from North America into
other continents． Introduced to what was formerly
Yugoslavia in the 1940s ( firstly recorded in 1949 )
(Wagner，2005; Douce，2003 )， it now has occupied
probably its entire range in Europe from France to the
Caspian Sea in the east，as well as penetrated into Central
Asia: Turkmenistan ( from 1990—1993 )， Uzbekistan
(Fergana Valley from 1996—1997 )，Kyrghyzstan，and
southeastern Kazakhstan． It was also introduced into Japan
in 1945，and has adjusted its number of generations per
year since its arrival (Gomi et al．，1996) ．
It was firstly discovered in 1979 at Dandong City，
Liaoning Province ( FAO，2007; Zhang，2008 ) ． Since
then，H． cunea began to spread into Northern China． At
present，it had spread to Liaoning，Shandong，Henan，
Shaanxi，Hebei， Tianjin， Beijing and other provinces
(Liu et al．，2008; Liu et al．，2005; Takeda，2005; Yang
et al．，2008) ． Frequent outbreaks occurred in these areas
and great economic losses have been caused subsequently．
As an important invasive pest，it usually lives and attacks
cultivated plants，particularly the ornamentals，man-made
forests and fruit trees around residential areas，towns and
cities ( Yang et al．，2007; Sullivan et al．，2011 ) ． The
pest has become a big problem to the planting projects in
northern China．
To date， insecticide use was still the most widely
practiced management method and played an important
role in the control of H． cunea． Although some effects had
been achieved，insecticides also caused the pollution of
the environment， killed a large number of natural
enemies．
Under the increasing concern over pesticide efficacy
and safety to humans and the environment， alternative
control options need to be fully evaluated． Under natural
conditions， fungi are frequent and important mortality
factors in the insect populations． Entomopathogenic fungi
have shown their great potential to control insect pests both
in the field and under greenhouse conditions ( Inglis et al．，
2001; Franci et al．，2012; Butt et al．，2001) ． Beauveria
bassiana is one of the most common pathogens infecting
insects． It has long been recognized as a potential
biocontrol agent and was actively being developed to
control various pest insects ( Zibaee et al．，2013; Edison
et al．，2006; zdikmen et al．，2004; Aurelien et al．，
2004; Eken et al．，2006; Liu et al．，2007; Lu et al．，
2008; Wang et al．，2007; Qin et al．，2012; Liu et al．，
2013; Bextine et al．，2002) ．
There was significant difference in the mortality
between the different strains of B． bassiana． And an
obvious host specificity exited in different strains． So It
was feasible to enhance the specialization and the
pathogenicity of B． bassiana to some kind of pest through
artificial orientation training (Guo et al．，2010) ． In this
experiment， the pathogenicity of some isolates from
different hosts or habitats to larvae of H． cunea was
studied，and a high virulent strain was screened through
laboratory and field experiments．
1 Materials and methods
1. 1 Insects
The eggs of H． cunea were collected in June of 2012
from the field in Baoding，Hebei． Larvae hatched from the
eggs in the laboratory were bred in the artificial climate
66
第 9 期 李会平等: 应用白僵菌防治美国白蛾的潜力
chamber at a fluctuating temperature of 25 to 28 ℃，
humidity 80% － 85% and a photoperiod of L∶ D(12 ∶ 12)
to 5-instar larvae with leaves of Populus tomentosa which
had been surface sterilized．
1. 2 Fungi
Fungi used in the experiments ( Tab. 1 ) were
obtained from the Forest Pathology Laboratory of Hebei
Agricultural University． BH01 was isolated from larva’s
cadaver of H． cunea obtained from Qinhuangdao of Hebei
province． Cadavers of H． cunea seemed to be fungal
diseases were washed in a solution of 1% sodium
hypochlorite for one minute and twice in sterile distilled
water，for one minute each time． Then they were dried on
sterile filter paper． After drying，they were transferred to
PDA plates and incubated at 25 ℃ ． The fungi were
identified by microscopically inspecting of the sporulating
structures and conidial morphology． BI05 was isolated
from a larva’s cadaver of Apriona germari from Dingzhou
County，Baoding City，Hebei，China ( Li et al．，2007) ．
BS04，BS05 and BS08 were bated from soil used the old
larvae of Tenebrio molitor as bate insects(Li et al．，2006) ．
Tab. 1 Isolates of B． bassiana for the experiments
Isolates Host species or habitats Locality Collect date Viability(% ) (mean ± SE)
BS04 Soil Yixian，Baoding 2005 － 06 90. 39 ± 3. 21
BS05 Soil Baoding 2005 － 06 96. 10 ± 1. 89
BS08 Soil Yixian，Baoding 2005 － 06 95. 29 ± 1. 78
BH01 H． cunea Qinhuangdao 2010 － 09 95. 23 ± 2. 91
BI05 A． germari Dingzhou，Baoding 2003 － 07 91. 09 ± 2. 99
1. 3 Preparation of conidial suspension
The fungi were grown on PDA plates in Petri dishes
and maintained at 25 ℃ ． Conidia were harvested from 10
days old surface cultures directly by scraping． Spore
suspensions were made by suspending conidia in 20 mL
sterile distilled water in little beaker containing 0. 05%
Tween-80． Beakers were agitated on a vibrant shaker for
10 min to produce a homogenous conidial suspension． The
spore concentrations were then adjusted to defined
concentrations using a Neubauer hemocytometer． Viability
of the conidia was checked by a germination test prior to
the experiment and assured to be ＞ 90% for all isolates．
1. 4 Pathogenicities of B． bassiana isolates to
H． cunea
The mortalities of larvae inoculated with the B．
bassiana isolates showed in Tab. 1 were compared at 1 ×
108 conidia·mL － 1 ． Larvae of H． cunea were sprayed with
conidial suspension using POTTEＲ spray tower，drained of
excess suspension by filter paper． The sterile distilled
water containing 0. 05% Tween-80 was used as the
control．
After treatment，insects were transferred individually
into a transparent plastic vial and fed on leaves of Pinus
tomentosa which had been surface sterilized． The leaves
were changed daily． Mortality was recorded daily for eight
days． Dead insects were surface sterilized and transferred
into a Petri dish lined with moistened filter paper． The
mortality due to fungi was confirmed by microscopic
examination of hyphae and spores on the surface of the
dead insect． All test insects were maintained in the
artificial climate chamber as described above． For one
treatment，50 insects and 3 mL conidial suspension were
used． There were four replicates for one isolates．
Data from the experiment were subjected to variance
analysis (ANOVA)，and differences are presented by the
results of LSD multiple range test． The LT50 value was
calculated using the probit procedure of the SPSS
statistical package．
1. 5 Dose-response test
For the highly virulent isolates identified in the above
bioassay， a further investigation was designed． To
determine the lethal concentration (LC50) of the selected
highly virulent isolates， larvae were sprayed with five
concentrations of conidia(1 × 104，1 × 105，1 × 106，1 ×
107 and 1 × 108 conidia·mL － 1 ) ． The control was the same
solution without the fungus． For each conidial
concentration，50 larvae were used． The insects were
inoculated and reared as described in 2. 4， and dead
insects were treated as described above to confirm the
cause of death． The LC50 was calculated using of the
probit procedure of the SPSS statistical package．
1. 6 Evaluation of field trial
The field experiments were carried out in October of
2012 and 2013，respectively in Baoding． At this time，H．
cunea was at the mature larval stage and would crawl down
from the tree to pupate． Three treatments，including 8 ×
76
林 业 科 学 51 卷
108 conidia·mL － 1 of B． bassiana BH01， 4. 5% β-
cypermethrin 2 000 times liquid and the water control were
arranged in the experiment． There were 4 replicates for
each treatment，and 3 trees for one replicate． In this test，
Taishan ft-796 sprayer was used to routinely spray． A thin
film was laid under the tree to catch the drops of dead H．
cunea ． The dead and live insects on the tree and film were
counted at 3，5 and 7 d post experiment respectively． The
control effect was calculated using the following formula:
Control effect(% ) = (Mortality in the treatment area － Mortality in the contrast area)
(1 － Mortality in the contrast area)
× 100% ．
2 Ｒesults
2. 1 Pathogenicities of B． bassiana isolates to
H． cunea
Mortalities and LT50 of H． cunea larvae inoculated
with the tested isolates were shown in Tab. 2．
All tested isolates were significantly different in their
virulence against H． cunea． The isolate BH01 was the
most virulent towards H． cunea， causing approximately
84. 78% mortality eight days post-infection． This isolate
was followed by isolates BS08 and BI05 that resulted in
71. 74% and 71. 75 mortality． And BS04 and BS05
caused only 32. 61% ，30. 43% mortality，respectively．
For the control，cumulative larval mortality was 8% after
eight days， and no fungi were observed on the dead
larvae．
Tab. 2 Mortalities and LT50 of H． cunea larvae treated with various isolates of B． bassiana in the laboratory
①
Isolates
tested
Percent mortality( corrected) /%
1 2 3 4 5 6 7 8
LT50
(95% fiducial limits) / d
BS04 0 0 0 0 10. 42 14. 89 25. 53 32. 61c 8. 524(7. 830 － 9. 654) a
BS05 0 2 0 8. 33 14. 58 21. 28 23. 40 30. 43c 8. 80(7. 926 － 10. 279) a
BS08 0 4 8. 16 22. 92 31. 25 55. 32 65. 96 71. 74b 5. 939(5. 582 － 6. 342) b
BH01 0 8 12. 24 33. 33 56. 25 76. 60 80. 85 84. 78a 4. 94(4. 627 － 5. 259) c
BI05 0 4 12. 24 43. 75 50. 00 57. 45 70. 21 71. 75b 5. 44(4. 67 － 6. 36) bc
CK 0 0 2 4 4 6 6 8
①Values followed by the same letter in the same column are not significantly different by LSD(P = 0. 05) ． The same below．
LT50 values differed significantly among the isolates
when applied at a concentration of 1 × 108 conidia·mL － 1
(Tab． 2) ． The LT50 values of B． bassiana BH01，BS08
and BI05 were 4. 94 d， 5. 939 d and 5. 44 d，
respectively，and shorter significantly than that of the
other two isolates．
2. 2 The lethal concentration of isolates to H． cunea
Based on the above bioassays， the isolates BH01，
BS08 and BI05 were selected to determine the LC50 value．
By dose-mortality analyses， the mortality of H． cunea
larvae differed significantly when inoculated with different
concentration of B． bassiana． The LC50 values of three
isolates were shown in Tab. 3．
The LC50 value for isolate BH01 was 1. 39 × 106
conidia·mL － 1，proved to be the most virulent against 5-
instar H． cunea． The LC50 values of the other two isolates
BS08 and BI05 were higher than that of isolate BH01
significantly．
2. 3 Evaluation of field trials
The results in the field test ( Tab. 4 ) showed that
4. 5% β-cypermethrin could kill the larvae of H． cunea
quickly． The control effect of 4. 5% β-cypermethrin to H．
cunea reached to 89. 43% 3 d after treatment，which has
no significant difference with that at 5 d and 7 d，94. 14%
and 93. 29% respectively． To BH01，the rate of control
H． cunea was noticeably slower than that of 4. 5% β-
cypermethrin，and the control effect increased gradually
with time． The control effect to H． cunea were 38. 21%
and 56. 98% respectively at 3 d and 5 d post control，
which were significantly lower than that of 4. 5% β-
cypermethrin． But till seven days after control，the control
effect of BH01 increased to 88. 84%， which was no
significant different with 4. 5% β-cypermethrin．
Tab. 3 LC50 values of isolates tested against larvae H． cunea eight days after treatment in laboratory experiment
Isolates tested
LC50
(95% fiducial limits) /( conidia·mL － 1 )
Dose regression equation
( correlation coefficient)
BS08 1. 34 × 107 (5. 26 × 106 － 4. 86 × 107 ) b Y = － 3. 203 + 0. 450X(0. 942 4)
BH01 1. 39 × 106 (7. 58 × 105 － 2. 55 × 106 ) c Y = － 4. 377 + 7. 13X(0. 927 8)
BI05 2. 11 × 107 (7. 23 × 106 － 1. 06 × 108 ) a Y = － 2. 940 + 0. 401X(0. 952 1)
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第 9 期 李会平等: 应用白僵菌防治美国白蛾的潜力
Tab. 4 The control effect in field experiment
of B． bassiana BH01①
Control effect(% )
3d 5d 7d
4. 5% β-cypermethrin 89. 43a 94. 14a 93. 29a
BH01 38. 21a 56. 98b 88. 84c
① Values followed by the same letter in the same line are not
significantly different by LSD(P = 0. 05) ．
3 Conclusions and discussions
In conclusion，our laboratory and field experiments
suggest that B． bassiana BH01 can provide an effective
and acceptable level of control against larvae of H． cunea
at concentration of 108 conidia·mL － 1 ． But the control
effect to egg，pupa and adult are needed because of the
generation overlap in the life cycle of H． cunea． And
before the use in the field，other fungal characteristics
such as spore production， germination， hyphal growth
rates and effects varying environmental conditions must
also be evaluated． Further research is currently being
conducted along these lines．
In the bioassay，the common method was immersion
and spraying． But H． cunea was difficult to soak by water
because of the overabundance of chaeta． And the amount
of spore suspension remained among the chaeta after
immersion was uncontrollable， which made inter-
individual difference of inoculum． So in the test，a spray
tower was used to lower this difference．
In northern China， the weather was very dry． H．
cunea，a sun-loving insect，occurred mainly in the space
where there was good light． The space was unfavourable to
the survival and germination of spores of B． bassiana
because of the dry，hot and intense ultraviolet． So H．
cunea in the leaf feeding period can not be infected easily
by B． bassiana． Furthermore，H． cunea in the high crown
was often difficult to contact with B． bassiana limited by
spraying equipment． The mature larvae of H． cunea would
crawl down from the tree to search pupation site which
mainly occurred under such surface coverage as rubble
masonry， plant litter and surface deposit， etc． This
process provides a big advantage for contact of B． bassiana
with H． cunea． So control H． cunea using B． bassiana in
mature larvae stage was more feasibility than in the other
stages．
The mature larvae of H． cunea were selected as the
test insects in this study． The results showed that
controlling mature larvae of H． cunea using B． bassiana
was a feasible control approach． But to avoid the effect of
hot，dry and ultraviolet on the B． bassiana，it was better
to spray at the peak of pupation．
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