Introduction
The tobacco/silver leaf whitefly, Bemisia tabaci Gennadius
(Hemiptera: Aleyrodidae) occurs in most parts of
the world; is an important agricultural
pest, and causing economic damage to crops (Palumbo et al. 2001). It has been listed as one of the world’s 100 worst
invasive alien species (Lowe et al.
2000) and infesting more than 600 host plant species (DeBarro et al. 2011; Li et al. 2011) including cassava,
cotton, sweet potatoes, tobacco, tomatoes (https://www.cabi.org/isc/datasheet/8927),
and cucurbits (Dennehy et al. 2010;
Cameron et al. 2014) . Adults and
nymphs of B. tabaci damage plants by sucking
nutrients and through the excretion of honeydew which reduces plant growth and yield by interfering photosynthesis (Jones
2003). B. tabaci also
transmits more than 100 different plant viruses during feeding (Hogenhout et al. 2008) including Tomato Yellow
Leaf Curl Virus (TYLCV)
in tomato (Berlinger 1986).
B. tabaci was reported as a serious
pest of tomato in 1997 from Oman (Azam et al. 1997) and was also
recorded from eggplant, cucumber and melon (Kaakeh et al. 2007). The TYLCV was isolated from tomato in 2008 (Khan et al.
2008). The infected plants my show vein/inter-vein or leaf yellowing, yellow
blotching or mosaic of leaves, leaf curling or crumpling, leaf vein thickening,
leaf enations, leaf cupping, stem twisting and plant stunting
(https://www.cabi.org/isc/datasheet/8927). B. tabaci is a cryptic
species complex with more than 40 morphologically indistinguishable species (Hu
et al. 2017). Within B. tabaci species complex, the
Mediterranean (MED or biotype Q) and Middle East-Asia Minor 1 (MEAM1 or biotype
B) species are highly invasive and cause substantial economic damage to crops
(Luo et al. 2002; Chu et al. 2006; Vassiliou et al. 2011).
B. tabaci has been usually controlled with carbamates, OPs and
pyrethroids representing 50 conventional insecticides (Horowitz et al. 2011). Resistance in B. tabaci
to insecticide has
developed due to the repeated applications of the same active ingredients and
their use in larger quantities (Denholm
et al. 1998; Horowitz et al. 2007). Repeated applications
of insecticides exert high selection pressure which increases the rate of
resistance development and also crop production cost (Naranjo and Ellsworth
2009). B. tabaci has tremendous potential to develop resistance to
different insecticides (Horowitz et al.
2007) and has been reported to develop resistance to 64 active ingredients of
different groups of insecticides (https://www.pesticideresistance.org/).
Deltamethrin (pyrethroid),
thiamethoxam (neonicotinoid) and pyriproxyfen (juvenile
hormone analog) have been used to control several insect pests including
B. tabaci (Dennehy and Williams 1997; Li et al. 2000; Dennehy et al. 2008; Tsagkarakou et al. 2009). These insecticides
have different modes of action. The pyrethroids target
voltage-gated sodium channels (VGSCs), neonicotinoids work on acetylcholine receptors in the insect nervous system and insect
juvenile hormone (JH) analog controls metamorphosis and development (Ishaaya
and Horowitz 1992; Cahill et al. 1995;
Dhadialla et al. 1998; Tomizawa and
Casida 2005). Both neonicotinoids and insect growth regulators (IGRs) have been
successful in controlling B. tabaci, which
also resulted in their excessive use. In a survey conducted in Oman, majority (95%) of the farmers used
insecticides consisting of 29 different active ingredients (Kaakeh et al. 2007). Deltamethrin and esfenvalerate (pyrethroids) have been
extensively used in Oman mostly in aerial sprays against dubas bug (550 tons
from 1993 to 2010) (Thacker et al.
2003; MAF 2014).
Resistance to deltamethrin,
thiamethoxam and pyriproxyfen in B. tabaci has been reported from other
regions (Toscano et al. 2001;
Horowitz et al. 2002; Nauen et al.
2002; Nauen and Denholm 2005). In Oman, B.
tabaci resistance has been reported to malathion and diazinon
(organophosphates) (Talukder et al.
2008). However, no baseline data on susceptibility to deltamethrin,
thiamethoxam and pyriproxyfen are available for B. tabaci populations in
Oman. This study was conducted to generate baseline data on susceptibility of B.
tabaci eggs, nymphs and adults to
deltamethrin, thiamethoxam and pyriproxyfen which are commonly used on
vegetables in Oman.
Materials and
Methods
Whiteflies collection and
rearing
Two separate colonies of B. tabaci adults (MEAM1) were collected from Agricultural
Experiment Station (AES) at the Sultan Qaboos University (SQU), Seeb (23.5910°
N, 58.1730° E) and the ‘Pairidaeza’ organic farm at Barka (Al-Batinah governorate)
(23.668854° N, 57.852961° E), Oman during March and April 2018. More than 100
adults were collected from infested tomato plants at each site using an
aspirator. The collected adults were transported in cool box with ice. At the
AES, different pesticides have been used in past while ‘Pairidaeza’ is a
certified organic farm and pesticides have not been used for last three years.
The SQU-1 (resistant) and Pairidaeza (susceptible) strains of B. tabaci colonies were reared
separately inside two walk-in glass cages (3 m × 4 m × 3 m with a mesh door) in
a secluded section of the glasshouse at AES. The colonies were maintained on
potted eggplants in a 48 cm3 cage which was placed inside each
walk-in glass cage with temperature and relative humidity (RH) set at 28 ± 2°C
and 65 ± 5%, respectively. Inside individual cages, three pots with 2–3 plants were placed
in 40 × 40 cm2 metal containers with 10 cm high edges. Pots were
replaced every two weeks. Plants were irrigated with a programmed automatic
drip system. Eggplant seedlings were grown in a growth chamber (25 ± 2°C and 65
± 5% RH) at the SQU and fresh plants at 3–4 leaf stage were regularly
provided to maintain the colonies.
Insecticides and
concentrations tested
The formulated insecticides used in bioassays were
bought from local market and included: deltamethrin 25 g L-1 (Delta
2.5 EC from Arab Pesticides and Veterinary Drugs Mfg. Co., Jordan),
thiamethoxam 240 g L-1 (Actara 240 SC from Syngenta, India) and
pyriproxyfen 100 g L-1 (Admiral 10 EC from Sumitomo Chemicals Co.,
Japan). Concentrations of each formulated insecticide were prepared with
deionized water, by 3X serial dilutions, and 1–2 concentrations above the field
recommended rates. The concentrations for deltamethrin were 0.74, 2.2, 6.7, 20,
60 and 180 µg/mL, for thiamethoxam
were 0.2, 0.56, 1.70, 5, 15, 45 and 135 µg/mL,
and for pyriproxyfen were 0.4, 1.2, 3.7, 11.1, 33.3 and 100 µg/mL.
Leaf-dip bioassay for adults
Six to seven concentrations of each insecticide that gave
15 to 85% mortality were selected for the bioassays (Heong et al. 2013). A leaf-dip bioassay method was adopted from Nauen et al. (2008). Leaf discs (45 mm) from
eggplant leaves were dipped for 15 s in an insecticide solution separately for
each concentration. Deionized water was used for control. Leaf discs were air
dried for 60 min on paper towel and placed upside down on a 1.5% agar already
poured in Petri dishes (55 mm). Petri-dish lids were ventilated with two rows
of small holes and lids were covered with fine mesh using glue to prevent
escaping of adults. B. tabaci adults were collected from the colonies
with an aspirator into small plastic vials and immobilized by immersing the
vials in the ice for 2–4 min. Working on a chilling pad, 20 B. tabaci adults (mixed sex) were transferred gently onto each
treated leaf disc. Each concentration was replicated three times and a total of
360 adults were used for deltamethrin and pyriproxyfen, and 480 adults for
thiamethoxam. Petri dishes were then covered with the already prepared lids and
sealed with parafilm. Petri dishes were placed upside down and kept at 24 ± 2°C
temperature, 60 ± 5% RH and a 12:12 h photoperiod in laboratory.
Leaf-dip (3-leaf whole plant)
bioassay for eggs and nymphs
A leaf-dip (3-leaf
whole plant) bioassay method was adopted from Bielza et al. (2019). An eggplant with three
leaves each trimmed into a small rectangle (4 cm × 6 cm) were placed in the
SQU-1 and Pairidaeza rearing cages for 24 h for egg laying to allow
synchronization of each developing stage. For eggs and nymphs, separate
bioassays were done. In egg-bioassay, after 24 h each
leaf (with ~50 eggs) was completely merged in the insecticide solution for 20 sec.
A single plant was used for each
concentration, with each of the three infested leaves counted as three
replicates. In bioassay for nymphs, the 3-leaf plants were inspected for the
presence of 2nd instar nymphs 15 days after egg laying, and then
treated by dipping individual leaves. Eggs and the immobile 2nd
instar nymphs were counted on each leaf under stereomicroscope and a total of
900–1400 eggs and 600–1050 nymphs were used in these bioassays.
Data recording and analysis
Mortality
of adults was assessed after 48 h for deltamethrin and after 72 h for
thiamethoxam and pyriproxyfen. Adults not moving after gentle touch by a needle
were considered dead. Number of eggs and hatched
alive nymphs were recorded 7 days after treatment in the egg bioassay. In the bioassays for nymph, the number of dead
nymphs and pupae were recorded 5 days
after treatment. Percent mortality was computed following Abbott (1925). Lethal
concentration values of each of the insecticide for
the eggs, nymphs and adult stages were calculated separately using Polo
Plus Version 2.0 (LeOra 1987). Resistance
factors (RF) were calculated by dividing LC50 of SQU-1 strain
(resistant) by LC50 of Pairidaeza strain
(susceptible). An RF of <2 means no resistance while 2–10 is
considered as very low, 11–20 as low, 21–50 as moderate, 51–100 as high and
>100 as very high resistance (Saleem et
al. 2008). Percent
corrected mortality caused by the three insecticides
applied at label recommended rate against eggs, nymphs and adults of B. tabaci were analyzed by
single factor ANOVA (analysis of variance) using S.P.S.S. V19.0 and means were
separated at LSD0.05.
Results
Susceptibility of adults to insecticides
The acute
contact LC50 for deltamethrin was 55.09 µg/mL and 12.69 µg/mL for
adults of SQU-1 and Pairidaeza strains, respectively. A low level
of resistance (RF = 4.3) to deltamethrin was detected in SQU-1 adults compared
to Pairidaeza. SQU-1 and Pairidaeza populations LC50s
for thiamethoxam were 4.10 and 1.85 µg/mL,
respectively. The SQU-1 population was 2.2-and 1.3-fold resistant to
thiamethoxam and pyriproxyfen, respectively suggesting very low to no
resistance against these insecticides (Table 1).
Susceptibility of nymphs and eggs to insecticides
LC50 of
deltamethrin for nymphs of SQU-1 and Pairidaeza strains were 28.73 µg/mL and 8.37 µg/mL, respectively and nymphs
of SQU-1 strain exhibited RF value 2.7-fold as compared to Pairidaeza strain. A
very high LC50 of 7837 µg/mL was determined for SQU-1 strain while
LC50 for Pairidaeza strain could not be determined because of the
concentration range used. Therefore, RF for eggs against deltamethrin could not
be calculated. LC50 for thiamethoxam was 7.21 and 2.59 µg/mL for nymphs of SQU-1 and Pairidaeza
strains with RF of 2.7 for former strain while RF for eggs was
2.3-fold. LC50 for pyriproxyfen was 5.29 and 4.67 µg/mL against nymphs of SQU-1 and Pairidaeza
strains with RF 1.1. LC50 for pyriproxyfen was 3.39
and 2.18 µg/mL for eggs of SQU-1 and
Pairidaeza strains,
respectively. The RF for eggs against pyriproxyfen was 1.6 (Table 2).
Mortality by field application rate
The field
application rate of deltamethrin caused 47.0 ± 6.3 and 59.6 ± 6.5% mortality in
adults and nymphs of SQU-1 strain, respectively, at dose of 20 µg a.i/mL, however, egg mortality was
only 14.0 ± 3.1% (Table 3). Thiamethoxam caused 82.0 ± 9.4, 86.7 ± 8.5 and 17.3
± 4.2% mortality in adults, nymphs and eggs of SQU-1 strain, respectively, at
dose of 100 µg a.i/mL. Pyriproxyfen
the field application rate at the dose of 75 µg a.i/mL caused 82.3 ± 9.8, 92.3 ± 10.5 and 82.0 ± 9.9% mortality
in adults, nymphs and eggs, respectively. Pyriproxyfen in SQU-1 strain which was not
significantly different than the Pairidaeza strain. Mortality in
adults and nymphs caused by thiamethoxam and pyriproxyfen in both strains was
significantly higher (F= 109, df = 2, P <
0.001; F = 54, df = 2, P < 0.001)
than deltamethrin. Mortality in eggs of both strains
caused by pyriproxyfen was significantly higher (F= 247, df =
2, P < 0.001) than deltamethrin and thiamethoxam. There was
no significant difference in adult (F= 1.3, df =
1, P=0.27), nymph (F = 0.33, df =
1, P=0.57) and eggs (F = 0.89, df,
1, P = 0.1) mortality
between the SQU-1 and Pairidaeza strains.
Discussion
Deltamethrin, thiamethoxam and pyriproxyfen are currently used in
the management of B. tabaci in
different horticultural crops in Oman. Resistance in B. tabaci has developed as a result of the intensive use of these
insecticides (Li et al. 2000; Dennehy
et al. 2008; Tsagkarakou et al. 2009). A very low
resistance to deltamethrin Table 1: Toxicity of three insecticides against adults of two B.
tabaci strains using
leaf-dip bioassay
Insecticides |
Strains |
Total
number tested |
LC10
(µg/mL) (95% FL) |
LC50
(µg/mL) (95% FL) |
LC90
(µg/mL) (95% FL) |
Slope
(± SE) |
heta |
RFb |
Deltamethrin
|
SQU-1 |
360 |
0.66 (0.15-1.62) |
55.09 (24.92-112.18) |
1256.9
(389.1-4226.9) |
0.81
± 0.17 |
0.47 |
4.3 |
|
Pairidaeza |
360 |
0.46 (0.26-1.74) |
12.69
(5.42-39.35) |
526.7
(181.2-1229.5) |
0.66
± 0.15 |
0.15 |
|
Thiamethoxam |
SQU-1 |
480 |
0.27
(0.01-1.41) |
4.10
(0.98-15.30) |
135.64
(42.3-7141.4) |
0.95
± 0.13 |
1.85 |
2.2 |
|
Pairidaeza |
480 |
0.12
(0.09-1.62) |
1.85
(0.08-5.20) |
85.63
(22.3-1421.5) |
0.64
± 0.12 |
0.67 |
|
Pyriproxyfen |
SQU-1 |
360 |
0.32
(0.07-0.76) |
8.39
(5.28-12.86) |
218.2
(100.5-811.9) |
0.91
± 0.13 |
0.41 |
1.3 |
|
Pairidaeza |
360 |
0.27
(0.06-0.67) |
6.59
(4.27-11.38) |
182.4
(84.7-567.4) |
0.84
± 0.14 |
0.32 |
|
LC10,
LC50 and LC90 are the concentrations (µg/mL) that will
kill 10, 50 and 90% of the B. tabaci
adults, respectively
60 adults used in
control
aA value lower than 1 indicates that homogeneity and
linearity of dose-mortality response were rejected
bResistance factor (RF) = LC50 of SQU-1 strain
divided by LC50 of Pairidaeza strain
Table 2: Toxicity of insecticides against nymphs and eggs of two B.
tabaci strains using leaf-dip
(3-leaf whole plant) bioassays
Insecticides |
Strains |
Life
stage |
Total
number tested |
LC10
(µg/mL) |
LC50
(µg/mL) |
LC90
(µg/mL) |
Slope
(± SE) |
heta |
RFb |
Deltamethrin |
SQU-1 |
Nymphs Eggs |
600 900 |
0.82 (0.29-1.87) 15.87 (4.38-37.01) |
28.73
(7.12-63.36) 7837
(3832-18936) |
697.8
(283.2-1963.5) -- |
1.08
± 0.13 0.68
± 0.13 |
1.30 0.07 |
2.7 -- |
Thiamethoxam |
SQU-1 |
Nymphs Eggs |
1050 1400 |
0.91
(0.27-2.25) 11.62
(3.75-22.95) |
7.21
(3.27-12.71) 3319.5
(889.4-54602.0) |
157.89
(49.7-2210.9) -- |
1.42
± 0.19 0.52
± 0.10 |
0.78 1.01 |
2.7 2.3 |
|
Pairidaeza |
Nymphs Eggs |
1050 1400 |
0.63
(0.15-1.52) 3.56
(1.57-12.32) |
2.59
(0.24-11.24) 1419.5
(693.4-21361.1) |
102.8
(29.7-710.9) -- |
1.51
± 0.28 0.66
± 0.19 |
0.27 0.58 |
|
Pyriproxyfen |
SQU-1 |
Nymphs Eggs |
600 900 |
0.29
(0.06-0.74) 0.13
(0.04-0.28) |
5.29
(2.59-8.38) 3.39
(2.29-4.98) |
93.7
(49.6-267.1) 86.18
(42.5-262.3) |
1.03
± 0.16 0.91
± 0.07 |
0.69 0.27 |
1.1 1.6 |
|
Pairidaeza |
Nymphs Eggs |
600 900 |
0.33
(0.08-0.98) 0.11
(0.05-0.53) |
4.67
(2.24-7.27) 2.18
(0.94-4.47) |
87.6
(36.4-187.9) 68.58
(35.8-182.6) |
1.11
± 0.12 0.73
± 0.09 |
0.36 0.14 |
|
LC10,
LC50 and LC90 are the concentrations (µg/mL) that will
kill 10, 50 and 90% of the B. tabaci
nymphs or eggs, respectively
aA value lower than 1 indicates that homogeneity and
linearity of dose-mortality response were rejected
bResistance factor (RF) = LC50 of SQU-1 strain
divided by LC50 of Pairidaeza strain
Table 3: Efficacy of the three commonly used insecticides against
B. tabaci applied at label recommended rate
Insecticides |
Label rate |
a.i. (µg/mL) |
Strain |
Percent corrected mortality |
||
|
|
|
|
Adults |
Nymphs |
Eggs |
Deltamethrin |
80 mL per 100 L water |
20 |
SQU-1 Pairidaeza |
47.0 ± 6.3a 62.7 ± 4.3a |
59.6 ±6.5a 67.4 ± 7.3a |
14.0 ± 3.1a 16.1 ± 3.4a |
Thiamethoxam |
8 g per 20 L water |
100 |
SQU-1 Pairidaeza |
82.0 ± 9.4b 94.3 ± 11.6b |
86.7 ± 8.5b 87.6 ± 8.3b |
17.3 ± 4.2a 25.0 ± 4.6a |
Pyriproxyfen |
150 mL per 200 L water |
75 |
SQU-1 Pairidaeza |
82.3 ± 9.9b 93.7 ± 10.1b |
92.3 ± 10.5b 94.4 ± 11.3b |
82.0 ± 9.9b 87.6 ± 8.7b |
Values sharing same letters in column don’t
differ significantly (P > 0.05)
was detected in adults (4.3-fold) and nymphs (2.7-fold)
of SQU-1 strain with reduced mortalities in both stages of the tested strains
at field application rate. Houndete et al. (2010), while establishing
baseline susceptibility, recorded a very low 1.6–4.7-fold resistance to deltamethrin in B. tabaci collected from cotton fields. The same populations,
however, showed reduced susceptibility (RF = 44) to another pyrethroid, bifenthrin.
Resistance factor for eggs treated with deltamethrin could not be calculated
because LC50 was not determined for the susceptible strain. A very
low level of resistance was observed for thiamethoxam in adults (2.2-fold) and
nymphs (2.7-fold) of SQU-1 strain, while no resistance (<2 fold) was
detected in egg stage. Adults of SQU-1 strain treated with thiamethoxam had
slightly reduced but non-significant mortality at the field application rate.
Pyriproxyfen treated eggs, nymphs and adults did not show any resistance. Eggs
of SQU-1 strain treated with field application rate of pyriproxyfen did not
show reduction in susceptibility.
Findings of
very low resistance ratios to deltamethrin in the SQU-1 strain may be due to
its cautious use at the experimental station. B. tabaci from other commercial farms where deltamethrin is
repeatedly used may show reduced susceptibility levels. Very low resistance
ratios to thiamethoxam and lack of resistance to pyriproxyfen show that B.
tabaci has retained a general level of susceptibility to these
insecticides. These two insecticides are relatively new to Oman. It is unlikely
that they may cause any resistance problem and their effectiveness is expected
to be maintained in near future. Another reason for the very levels of
resistance is because of the presence of B biotype in Oman. One strain of B. tabaci representing the B biotype had
resistance factors between 1–8 showing
very low to no resistance to imidacloprid, thiamethoxam and acetamiprid (Qiong et al. 2012). The Q biotype of B.
tabaci has shown stronger resistance to neonicotinoid insecticides than B
biotype (Ma et al. 2007; Luo et al. 2010; Rao et al. 2011; Qiong et al.
2012).
Monitoring field populations for their
susceptibility to the most used insecticide classes is crucial for early
detection of resistance development (Roush and Miller 1986). While developing resistance management strategies for an
insect pest, it is important to establish the baseline susceptibility levels
(Prabhaker et al. 2008). Baseline
susceptibility data provide a reference point to which subsequent
susceptibility data can be compared with. Any shift in the susceptibility to a
particular insecticide from the reference would detect resistance in its early
stages.
The determined baseline susceptibility levels of B. tabaci adults, nymphs and eggs
against deltamethrin, thiamethoxam and
pyriproxyfen can be used for continuous monitoring of B. tabaci populations. Natural variations in responses to
insecticides in populations collected from various geographic regions in Oman
should be expected. B. tabaci
populations should also be tested at different time of the year, for example
September to December, that could help explain the causes of variability in
insecticide susceptibility. Any change in the susceptibility levels indicates
development of resistance in B.
tabaci. Once resistance is detected, resistance management strategies must
be initiated and implemented before control failures occur. An extensive survey
and toxicological work with several strains collected from different regions in
Oman, with different history of insecticide applications, is underway which
will help in broadening the susceptibility baseline data of B. tabaci.
Our results provide a baseline for
future comparisons of the sensitivity of B.
tabaci to three insecticides that represent the primary classes being used
to control this pest, each with a different mode of action. The range of
concentrations across which these populations responded will allow baseline
sensitivity studies in other governorates in Oman to test the active range of
response for these insecticides. Insecticide resistance management (IRM) is a
crucial component of a successful IPM program (Foster et al. 2002). Preventative approaches should be implemented instead
of relying on only insecticides (Timmeren et al. 2018). IRM strategies should include rotation of insecticides (based on IRAC
classification with different modes/site of action). Thiamethoxam and pyriproxyfen
did not show any reduction in susceptibility and should be included in rotation. Use of insecticides should be integrated with cultural and biological pest
management tools that will provide effective management of B. tabaci in Oman.
Acknowledgements
The authors
acknowledge the financial support provided by Sultan Qaboos University, Oman
through internal grant ‘IG/AGR/CROP/18/02’.
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