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Archive of SID
J. Agric. Sci. Technol. (2008) Vol. 10: 165-171
165
Reproduction of the White Tip Nematode (Aphelenchoides
besseyi Christie, 1942) in Different Monoxenic Cultures
S. Jamali1, E. Pourjam2*, A. Alizadeh2 and F. Alinia3
ABSTRACT
The reproductive range of the Iranian population of white tip nematode in rice, Aphel-
enchoides besseyi, was investigated in vitro to find out a suitable medium as well as a fa-
vorable fungal host for monoxenic culturing this nematode. Studies were carried out on
rice seed associated fungi, pathogenic fungi and one mushroom (Agaricus bisporus)
grown on three culture media, RPA (rice polish agar), OMA (oat meal agar) and PDA
(potato dextrose agar). The nematode showed the greatest multiplication on Fusarium
verticillioides, F. proliferatum, Curvularia lunata and Magnaporthe salvini in OMA and
on Alternaria alternata, Bipolaris oryzae and Pyricularia oryzae in PDA. Among the fungi,
tested A. alternata, C. lunata, F. verticillioides, B. oryzae, M. salvini, F. proliferatum and P.
oryzae supported a high reproduction rate in the nematode in a descending rank. The
nematode failed to multiply on Aspergillus niger, Rhizoctonia solani and Agaricus bis-
porus grown on any of the three media. The highest sex ratio (F:M) was achieved on
OMA but the highest male percentage ratio was observed on PDA. The two pathogenic
fungi, B. oryzae and M. salvini are reported as new fungal hosts for monoxenic culturing
of this nematode.
Keywords: Aphelenchoides besseyi, Fungi, Host range, Monoxenic culture, Reproduction.
_____________________________________________________________________________
1. Department of Plant Pathology, College of Agriculture, Guilan University, Rasht, Islamic Republic of
Iran.
2. Department of Plant Pathology, College of Agriculture, Tarbiat Modares University, P. O. Box 14115-
336, Tehran, Islamic Republic of Iran.
3. Rice Research Institute, Rasht, Islamic Republic of Iran.
* Corresponding author, e-mail: pourjame@modares.ac.ir
INTRODUCTION
Nematodes are important for the decompo-
sition of and nutrient recycling in soil.
Nematode species have a wide range of food
preferences and knowledge of their feeding
habits is essential to understand their biol-
ogy and role in ecosystem processes. Fungus
feeding nematodes rear on many different
species of fungi, including saprophytic,
pathogenic and mycorrhyzal fungi (Freck-
man and Caswell, 1985; Giannakis and
Sanders, 1989; Ruess and Dighton, 1996).
Culturing of nematodes on fungal species
could provide a suitable means for obtaining
enough pure population for further investi-
gations.
Among the seed-borne pathogens of rice,
Aphelenchoides besseyi Christie, 1942 is
considered to be a major problem, causing
white tip disease which is widely distributed
throughout almost all the rice growing re-
gions of the world and results in low yields
and deteriorated seed quality (Rajan and
Mathur, 1990). This nematode is not only a
parasite of higher plants but it can also feed
on fungi. Many fungal species can support
the population growth of A. besseyi in vitro.
The feeding and reproduction of this nema-
tode on Fusarium solani (Huang et al.,
1973), Aureobasidium pullulans (Huang et
al., 1979), Alternaria tenuis (Todd and At-
kins, 1958) and Alternaria alternata (Rajan
et al., 1989) have already been reported. Rao
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________________________________________________________________________Jamali et al.
166
(1985) studied the population build up of
white tip nematode in different monoxenic
cultures and found that among various me-
dia examined, oat meal agar supported the
highest population increase in the nematode.
The population was highest on Fusarium
moniliforme, followed by Alternaria
padwickii, Helminthosporium oryzae and
Curvularia sp., but the nematode failed to
multiply on Pyricularia oryzae. In an other
investigation, populations of A. besseyi from
different hosts and various geographical ar-
eas were evaluated for their mode of repro-
duction and host range. It was determined
that different populations exhibited parthe-
nogenetic and amphimictic modes of repro-
duction (Gokte-Narkhedkar-Narkhedkar et
al., 2001).
There is no information available on the
reproduction of this nematode on RPA (rice
polish agar) medium, a new substrate for
monoxenic culturing; RPA contains rice pol-
ish as a natural substrate of the host in con-
trast to PDA (potato dextrose agar) and
OMA (oat meal agar). Present attempt was
made to study population build up of adults,
juveniles and sex ratio of white tip nematode
on different monoxenic cultures including
rice seed associated fungi, pathogenic fungi
and a mushroom, using OMA, RPA and
PDA as media.
MATERIALS AND METHODS
Preparation of Fungal Isolates
Rice seeds were collected from rice fields
in Guilan, Mazandaran and Golestan Prov-
inces and were cultured on PDA medium.
Five fungal species i.e. Fusarium verticil-
lioides, F. proliferatum, Alternaria alter-
nata, Curvularia lunata and Aspergillus ni-
ger were isolated and purified. The fungi
were originally recovered from the same
sites where the nematode was present. They
were frequently found associated with paddy
seeds sampled from different regions during
cultural practices. In addition, four patho-
genic fungi, Bipolaris oryzae (Brown Spot),
Magnaporthe salvini (Stem Rot), Pyricu-
laria oryzae (Blast) and Rhizoctonia solani
(Sheath Blight) recovered from infected
plants and one isolate of Agaricus bisporus
obtained from the culture collections of the
Plant Pathology Department of Tarbiat Mo-
dares University, were used in this study.
Preparation of Nematodes
Aphelenchoides besseyi was isolated from
infected seeds collected from rice fields in
Guilan Province, northern Iran. Nematodes
were extracted following Coolen and
D'Herde's method (Coolen and D'Herde,
1972), sterilized in a 1,000 ppm streptomy-
cin sulfate solution for five minutes and then
rinsed with sterilized water several times
(Moore et al., 1985).
Experiments
Twenty pairs (female and male) of nema-
tode were transferred to each Petri dish con-
taining Purified fungus. The nematodes were
released onto the Petri dish when 1/3 surface
of the plate was colonized by the fungus
mycelium. The plates were sealed with
parafilm, kept in plastic bags and incubated
at 28ºC in darkness (Rao, 1985). The nema-
todes were harvested four weeks after inocu-
lation and the population recorded. For this
purpose, each Petri dish lid was initially re-
moved and the colony surface was thor-
oughly washed into a container then the me-
dium was sliced and processed by a modi-
fied Baermann funnel technique (Hooper,
1990) for 48 hours. Total populations of
nematodes in this water suspension were
then counted in a counting dish under a ste-
reomicroscope.
To examine the sex ratio of the nematode
in the culture media, only the adults were
counted and recorded. The multiplication
factor of nematodes (Final nematode popula-
tion/Initial inoculum level) was calculated
for each host fungus.
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Reproduction of White Tip Nematode ___________________________________________
167
The experiment was conducted in a com-
pletely randomized design with two factors,
three media and ten fungi, using four repli-
cates and repeated twice. Transformed data
on nematode numbers (mean of eight repli-
cates derived from two experiments) were
analyzed and the means were compared us-
ing Duncan's multiple range and LSD tests.
RESULTS
In total, ten different fungal species were
tested for their capability to support the
population build up of the fungal feeder
nematode, A. besseyi, using three culture
media. Four weeks after incubation, nema-
tode mass cultures were established on A.
alternata, F. verticillioides, C. lunata, B.
oryzae, M. salvini, F. proliferatum and P.
oryzae. Infrequent or no survival of nema-
todes was observed on A. niger, A. bisporus
and R. solani (Table 2 and Figure 1). The
highest reproduction rate was observed on A.
alternata with 16,737 nematodes/plate. The
lowest population was obtained from P.
oryzae grown on OMA (27) and the remain-
ing ranged from 11,137 to 274 nema-
todes/plate. Figure 1 shows the clusters of
nematode rearing on A. alternata in the
plate. The results indicated a varying degree
of reproduction of A. besseyi rearing on dif-
ferent fungal species (Table 2). A. alternata,
C. lunata, F. verticillioides, B. oryzae, M.
salvini, F. proliferatum and P. oryzae had
the highest average of nematode numbers in
descending order (Table 2). A summary of
mean comparison of nematode populations
reared on various fungi and different culture
media using Duncan's multiple range tests is
presented in Table 2. Differences between
Table 1. Analysis of variance (ANOVA) of population growth of Aphelenchoides besseyi.
SOURCE DF SS MS F Value
Fungus 9 297005.73 33000.63 2629.7**
Medium 2 9421.74 4710.87 375.39**
Fungus × Medium 18 24504.78 1361.37 108.48**
Error 210 2635.32 12.54
Total 239 333567.58
C.V.= 9.19 %
** indicating significant differences (P= 0.01).
Table 2. The ranges of population increase of Aphelenchoides besseyi reared on different fungal
species grown in three culture media.
Fungal species OMA PDA RPA Total mean
Alternaria alternata 105.53 a a 129.37 a 92.08 a 109 a
Curvularia lunata 75.54 b 64.12 b 52.97 b 64.21 b
Fusarium verticillioides 104.7 a 46.97 d 36.57 c 62.75 b
Bipolaris oryzae 58.49 d 62.05 b 55.45 b 58.66 c
Magnaporthe salvini 66.52 c 54.12 c 51.36 b 57.33 c
F. proliferatum 34.69 e 27.77 e 11.29 d 24.58 d
Pyricularia oryzae 5.24 f 16.56 f 0.7 e 7.5 e
Agaricus bisporus 0.7 g 0.7 g 0.7 e 0.7 f
Aspergillus niger 0.7 g 0.7 g 0.7 e 0.7 f
Rhizoctonia solani 0.7 g 0.7 g 0.7 e 0.7 f
CDb to compare populations of the nematode at 1% level= 4.54
CD to compare populations of the nematode at 5% level= 3.46
a Data are transformed ( 5.0+X) means of eight replicates.
Figures in each column with the same letter are not significantly different (P= 0.01).
b
C
ri
t
i
ca
l
d
iff
e
r
e
n
ce
betwee
n
tw
o
popu
l
at
i
o
n
s
o
f
t
h
e
n
e
m
atodes.
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________________________________________________________________________Jamali et al.
168
the two nematode populations can also be
compared with CD at both levels of prob-
ability (Table 2) and was found to be sig-
nificant if was greater than CD in the LSD
test. The results for the sex ratio of adults of
A. besseyi reared on fungal hosts grown on
RPA, OMA and PDA and the calculated
multiplication factor are summarized in Ta-
ble 3. According to the ANOVA test, there
was significant difference in reproduction
rate among the ten fungal species and three
culture media. Furthermore, the results indi-
cated a significant interaction between fun-
gus and medium (Table 1).
The results revealed that the nematode
showed greatest multiplication on Fusarium
verticillioides, F. proliferatum, Curvularia
lunata and Magnaporthe salvini in OMA
and on Alternaria alternata, Bipolaris oryzae
and Pyricularia oryzae in PDA. Among the
culture media examined, the lowest popula-
tion of adults and juveniles was observed on
RPA (Table 2). P. oryzae, as an important
pathogenic fungus of rice, exhibited variable
results in supporting the nematode popula-
tion on various media. While the nematode
supported population growth on PDA, it was
able to survive on OMA, as indicated by the
presence of adults, but it failed to multiply
on RPA.
The highest multiplication factor (418
times) was obtained on A. alternata grown
in PDA and the lowest (0.7 time) on P.
oryzae grown in OMA, respectively (Table
3). The female population in the harvested
nematodes was highest on OMA, whereas
the highest male ratio was observed on PDA
(Table 3).
Figure 1. (a and b) Alternaria alternata plates without and with nematode (Darker); (c) Conidiophores
and conidia of A. alternate and (d and e) Aphelenchoides besseyi growing on A. alternata.
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Reproduction of White Tip Nematode ___________________________________________
169
DISCUSSION
This study showed that the food source has
an important impact on population growth in
the nematode. The feeding preference of A.
besseyi could be evaluated on the basis of
the adult nematode population recovered
from different fungal colonies. A clear influ-
ence of fungal species on the multiplication
rate of A. besseyi was discernible (Table 2).
Alternaria alternata was the most favorable
fungus, supporting a higher nematode popu-
lation. The results on population growth of
the nematode reared on A. alternata grown
on different media, revealed that PDA was a
suitable substrate for the fungus. Multiplica-
tion of this nematode has been recorded on
different fungi, but none has provided as
high as a 418 times increase in the number
of adults and juveniles as noted in the pre-
sent investigation. In previous studies, the
highest record of the population increase
was 354 times (Rao, 1985). Therefore, this
host (A. alternata on PDA) can be a good
alternative for mass production of the nema-
tode in the laboratory for biological, eco-
logical, epidemiological and molecular stud-
ies. Aureobasidium pullulans, A. tenuis, A.
alternata and F. solani have previously been
used for mass production of the nematode
(De Waele, 2002). In this study Aspergillus
niger, A. bisporus and R. solani were found
to be non-hosts for the nematode. It can be
assumed that A. niger, despite being a cos-
mopolitan saprophytic fungus, plays no sig-
nificant role on the reproduction and sur-
vival of this nematode in nature. On the
other hand, A. besseyi is not considered to be
a pest for A. bisporus in mushroom cultiva-
tions. The causal agent of blast disease, P.
oryzae, supported a very low population,
whereas multiplication of the nematode on
the other fungi in this study was intermedi-
ate.
B. oryzae and M. salvini supported a rela-
tively good multiplication of the A. besseyi
population and are reported as new hosts.
The three fungi species, P. oryzae, B. oryzae
and M. salvini could be used to study the
interaction between the nematode and rice
pathogenic fungi. Differences between
populations of the nematode on each fungus
when compared on three culture media ex-
hibited varying reproduction rates which
were clearly influenced by the fungal cul-
tures as well as by the type of culture media
used. Similar findings were reported by
Gokte-Narkhedkar-Narkhedkar and Mathur
(1989). In another investigation using differ-
ent culture media and fungal species, the
Table 3. Sex ratio and multiplication factor of Aphelenchoides besseyi reared on different fungal species
grown in three culture media.
PDA OMA RPA
Fungal species Sex ratio
(F:M)a Multiplica-
tion factor Sex ratio
(F:M) Multiplica-
tion factor Sex ratio
(F:M) Multiplica-
tion factor
Alternaria alter-
nata 4.1:1 418 8.5:1 278 7.1:1 212
Bipolaris oryzae 4.0:1 96 8.2:1 86 6.8:1 77
Curvularia lunata 4.4:1 103 8.6:1 143 7.0:1 70
Fusarium verticil-
lioides 3.9:1 55 8.1:1 274 7.3:1 33
F. proliferatum 3.9:1 19 8.3:1 30 7.2:1 3
Magnaporthe
salvini 4.4:1 73 8.3:1 11 7.0:1 66
Pyricularia oryzae 4.7:1 7 8.0:1 0.7
-b -
Agaricus bisporus - - - - - -
Aspergillus niger - - - - - -
Rhizoctonia solani - - - - - -
a F= Female, M= Male, b No multiplication and survival.
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________________________________________________________________________Jamali et al.
170
highest multiplication rate of this nematode
was achieved when A. besseyi was grown on
2% OMA and F. moniliforme (Rao, 1985). It
seems that the effectiveness of a monoxenic
host fungus on population increase is de-
pendent on the type of culture medium used.
In our studies, OMA was proven to be a bet-
ter substrate for multiplication of the nema-
tode on F. verticillioides than on RPA and
PDA (Table 2). The results of our study are
in agreement with those of Rao (1985) and
Gokte-Narkhedkar-Narkhedkar and Mathur
(1989).
In this work, the culture media showed
definite effects on the sex ratio of the nema-
tode as recorded on these fungal cultures.
According to our data, the sex ratio ranges
were highest on OMA (8-8.6) and lowest on
PDA (3.9-4.7) (Table 3). The multiplication
factor can also be used as a good index of
potential reproduction of the nematode in
different cultures (Table 3).
RPA medium as a substrate containing
natural compounds of rice, showed a low
multiplication rate and was a poor substrate
for nematode reproduction. It may suggested
that the influence of the fungi on the devel-
opment and reproduction of nematodes ap-
pears to be more important than the type of
media used (Tables 1 and 3). The nematode
failed to multiply and survive on P. oryzae
when grown on RPA, because this medium
induced more sporulation in the fungus and
it seems that the nematode prefers mycelia
for feeding rather than conidia. Our findings
proved the previous results (Rao, 1985;
Gokte-Narkhedkar-Narkhedkar and Mathur,
1989; Rajan and Mathur, 1990; Gokte-
Narkhedkar-Narkedkar et al., 2001) that the
fungus species has an important function
and must be taken into consideration in de-
termining the reproduction rate of A. bes-
seyi.
ACKNOWLEDGMENTS
The authors would like to thank the Rice
Research Institute, Eng. Moosanejad for
providing the necessary facilities and Dr.
Mohammadi Goltapeh for providing mush-
room isolate.
REFERENCES
1. Coolen, W. A. and D’Herde, C. J. 1972. A
Method for the Quantitative Extraction of
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2. De Waele, D. 2002. Foliar Nematodes:
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tance to Parasitic Nematodes. Starr, J. L.,
Cook, R. and Bridge, J. (Eds). CAB Interna-
tional Publishing, UK, pp. 141-151.
3. Freckman, D. W. and Caswell, E. P. 1985.
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tems. Ann. Revi. of Phytopathol., 23: 275-
296.
4. Giannakis, N. and Sanders, F. E. 1989. Inter-
actions between Mycophagous Nematodes,
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5. Gokte-Narkhedkar-Narkhedkar, N. and
Mathur, V. K. 1989. Reproduction and De-
velopment of Aphelenchoides besseyi. Phy-
toparasitica, 17: 263-267.
6. Gokte-Narkhedkar-Narkhedkar, N., Mathur,
V. K., Ramasundaram, P. and Sabesh, M.
2001. Reproductive Variations in Aphelen-
choides besseyi Populations. Indian J. Nema-
tology, 31: 115-119.
7. Hooper, D. J. 1990. Extraction and Process-
ing of Plant and Soil Nematodes. In: Plant
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Tropical Agriculture. Luc, M., Sikora, R. A.
and Bridge, J. (Eds). CAB International Pub-
lishing, UK, pp. 45-68.
8. Huang, C. S., Huang, S. P. and Chiang, Y. C.
1979. Mode of Reproduction and Sex Ratio
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1973. The Effect of Temperature on Devel-
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12. Rajan, A., L., Mathur, V. K. and Lal, A.
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ﻔﺳ كﻮﻧ ﺪﺗﺎﻤﻧ ﺮﻴﺜﻜﺗﻴﺪي ﺞﻧﺮﺑ گﺮﺑ (Aphelenchoides besseyi Christie, 1942) يور ﺮﺑ
ﺤﻣﻴﻂ ﺺﻟﺎﺧ يﺎﻫ
س .ﻟﺎﻤﺟﻲا ، .ع ،ﻢﺟرﻮﭘ .ﻠﻋﻴف و هداﺰ .ﻠﻋﻲﻧ ﻴﺎ
هﺪﻴﻜﭼ
روآدازيﻌﻤﺟ ﻴ ﺖAphelenchoides besseyi اﺮﺷ ﺖﺤﺗ ،رﻮﺸﻛ لﺎﻤﺷ زا هﺪﺷاﺪﺟﻳﺎﻣزآ ﻂﻳ ـﺳرﺮﺑ هﺎﮕﺸﻲ
ﺤﻣ و ﺪﺷﻴ اﺮﺑ ﺐﺳﺎﻨﻣ چرﺎﻗ و ﺖﺸﻛ ﻂي ﻟﻮﺗ ﻴ ا هﻮﺒﻧا ﺪﻳ ﺖـﻓﺮﮔ راﺮﻗ ﻪﻌﻟﺎﻄﻣ درﻮﻣ ﺪﺗﺎﻤﻧ ﻦ . ور ﺮـﺑ ﻪـﻌﻟﺎﻄﻣي هد
چرﺎــﻗ ﻞﻣﺎــﺷ چرﺎــﻗﺎــﻫي ﺎــﻫ چرﺎــﻗ ،رﺬــﺑ زا هﺪــﺷ اﺪــﺟ يﺑ ﻢــﻬﻣ ﻴرﺎــﻤﻳ و اﺰــﻳ ﻛارﻮــﺧ چرﺎــﻗ ﻪــﻧﻮﮔ ﻚﻲ
(Agaricus bisporus) ﺤﻣ ﻪﺳ زا هدﺎﻔﺘﺳا ﺎﺑﻴ ﺖﺸﻛ ﻂRPA ،OMA و PDA ﺖﻓﺮﮔ ترﻮﺻ .ﺎﺘﻧ سﺎﺳا ﺮﺑﻳ ﺞ
ـﺤﻣ ،هﺪـﻣآ ﺖﺳد ﻪﺑﻴ ﺖﺸـﻛ ﻂOMAﺑ ﺮـﺘﻬﻳ ـﺤﻣ ﻦﻴ اﺮـﺑ ﻂيﺜﻜﺗ ـﻴ ﺪـﺗﺎﻤﻧ ﺮA. besseyi ور ﺮـﺑي چرﺎـﻗ ﺎـﻫي
, Curvularia lunata
Fusarium verticillioides
F. proliferatum , و
Magnaporthe salvini
ﻲﻣ ﺪﺷﺎﺑ .ﻟﺎﺣردﻴﺮﺘﺒﺳﺎﻨﻣ ﻪﻜﻳﺤﻣ ﻦﻴاﺮﺑ ﻂيﻟﻮﺗ ﻴا ﻞﺜﻣ ﺪﻳور ﺮﺑ ﺪﺗﺎﻤﻧ ﻦي چرﺎـﻗ ﺎـﻫي Alternaria alternata
Bipolaris oryzae ,
و
Pyricularia oryzae
ﺤﻣﻴ ﻂPDA ﺖﺳا .ﺑ ردﻴچرﺎﻗ ﻦﺎﻫيﺳرﺮﺑ درﻮﻣ ﻲﻦﻳﺮﺘﺸﻴﺑ ،
ﻟﻮﺗ ناﺰـﻴﻣ ـﻴ ﻞـﺜﻣ ﺪA. besseyi ﺮـﺑ ﺐـﻴﺗﺮﺗ ﻪـﺑ يور A. alternata
,
, C. lunata
F. verticillioides
,
B.
oryzae
,
M. salvini
,
F. proliferatum
و P. oryzaeﺪــﺷ هﺪﻫﺎﺸــﻣ .اــ ﻳورﺮــﺑ ﺪــﺗﺎﻤﻧ ﻦيﺎــﻗ ﺎــﻫ چري
Aspergillus niger, Rhizoctonia solani و Agaricus bisporus
ـﺤﻣ ﻲﻣﺎـﻤﺗ ردﻴﻂ ﺪـﻗﺎﻓ ،ﺖﺸـﻛ يﺎـﻫ
ﺜﻜﺗ ترﺪﻗﻴ دﻮﺑ ﺮ .ﺮﺗﻻﺎﺑﻳ ﺴﻨﺟ ﺖﺒﺴﻧ ﻦﻲ) ﺮﻧ ﻪﺑ هدﺎﻣ( ﺤﻣ ﻪﺑ ﻖﻠﻌﺘﻣ ،ﻴ ﻂ
OMA ﺑ و ﻴﺮﺘﺸﻳ ﺮـﺑ ﺮـﻧ ﺪـﺗﺎﻤﻧ ﺪـﺻرد ﻦ
وريﺤﻣ ﻴﻂ
PDA دﺮﮔ هﺪﻫﺎﺸﻣ ﻳﺪ .ﺑ چرﺎﻗ ودﻴ ،ﺞﻧﺮﺑ ﺮﮔرﺎﻤB. oryzae و M. salvini ﻣ ناﻮـﻨﻋ ﻪـﺑﻴ يﺎـﻬﻧﺎﺑﺰ
ﭼرﺎﻗﻲﺪﺟ ﻳ ﺪﺗﺎﻤﻧ ﺪA. besseyi ﻣ شراﺰﮔﻲﺪﻧﻮﺷ.
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