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Influence of abiotic factors on the infestation dynamics of whitefly, Bemisia


tabaci (Gennadius 1889) in cotton and its management strategies in North-
Western India

Article in International Journal of Tropical Insect Science · May 2020


DOI: 10.1007/s42690-020-00155-2

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Influence of abiotic factors on the
infestation dynamics of whitefly, Bemisia
tabaci (Gennadius 1889) in cotton and its
management strategies in North-Western
India
Mandeep Pathania, Arti Verma,
Manpreet Singh, Parshotam Kumar
Arora & Nirmaljeet Kaur

International Journal of Tropical


Insect Science

e-ISSN 1742-7592

Int J Trop Insect Sci


DOI 10.1007/s42690-020-00155-2

1 23
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Author's personal copy
International Journal of Tropical Insect Science
https://doi.org/10.1007/s42690-020-00155-2

Influence of abiotic factors on the infestation dynamics of whitefly,


Bemisia tabaci (Gennadius 1889) in cotton and its management
strategies in North-Western India
Mandeep Pathania 1 & Arti Verma 1 & Manpreet Singh 1 & Parshotam Kumar Arora 1 & Nirmaljeet Kaur 2

Received: 13 December 2019 / Accepted: 28 April 2020


# African Association of Insect Scientists 2020

Abstract
Bemisia tabaci is the most destructive insect of cotton worldwide. We analysed infestation dynamics of B. tabaci in cotton during
summers of 2015–2017, and predicted the factors influencing its abundance. The incidence of B. tabaci on cotton was excep-
tionally high in 2015 (25.91 ± 2.14 adults/3 leaves) as compared to 2016 (9.53 ± 1.23 adults/3 leaves) and 2017 (8.54 ± 1.12
adults/3 leaves). Minimum temperature, maximum-minimum relative humidity and rainfall influencing the B. tabaci population
build-up were predicted using PCRA technique with reasonable accuracy (R2 = 0.87). The results also showed that monitoring/
sampling of B. tabaci in cotton should be done before 10:00 h. Among different cotton cultivars, Ankur 3028 and Bioseed 6588
were most susceptible to B. tabaci infestation. Bemisia tabaci incidence in cotton interferes with the secondary metabolite
production in different cultivars. Pesticides tested for management of B. tabaci gave a maximum population reduction ranging
from 42.91 to 77.01% 7 days after spray. The efficacy of tested pesticides persisted up to 10 days after spray. Maximum control of
B. tabaci was achieved by flonicamid > clothianidin > diafenthiuron > dinotefuran > thiamethoxam, whereas, ethion was found
least effective. Pyriproxyfen have nymphicidal action and provided maximum reduction (68.62%) in whitefly population after
10 days of spray.

Keywords Cotton . whitefly . population dynamics . metabolites . management . insecticides

Introduction industrial production and 11% to total exports earnings


(Anonymous 2017a). India ranks first in cotton production
Cotton plays a significant role in India’s economy as the tex- with 38.41% and 26% of the total world production and area,
tile industry is primarily cotton based contributing around 5% respectively (Anonymous 2017b). In Punjab, cotton is grown
to the country’s gross domestic product (GDP), 14% to as a major cash crop in the summer season and because of
luxuriant growth, hot and humid weather prevalent during the
season, the crop is vulnerable to insects and diseases right
Highlights from germination till harvesting. During its growth period
• Abiotic factors played significant role in predicting the dynamics of
whitefly (Bemisia tabaci) to much extent.
cotton is infested by around 148 insect pests, out of which
• Monitoring of B. tabaci in cotton fields should be done before 10: 00 17 species are of major concern (Abbas 2001).
hours. Among these insects, whitefly, Bemisia tabaci (Hemiptera:
• Differences in crop conditions affect the biosynthesis of phenolic Aleyrodidae), occupied a significant place and caused severe
compounds and B. tabaci incidence in cotton cultivars.
• Flonicamid, clothianidin, diafenthiuron, dinotefuran and pyriproxyfen
damage to the cotton crop, especially in North-western India
are effective in controlling B. tabaci. during the last 4–5 years. There are two different genetic
groups of B. tabaci reported to occur in Indian Punjab, viz.
* Mandeep Pathania B. tabaci Asia I and Asia II-1 (Naveen et al. 2017). However,
mpathania@pau.edu B. tabaci Asia II-1 was more predominant in cotton (Ellango
et al. 2015). Initially, B. tabaci was not considered as a serious
1
Regional Research Station, Punjab Agricultural University, pest of cotton. However, in 2015, it became so prominent and
Abohar, Punjab 152116, India its severity was so high that it became the major pest of cotton
2
Department of Botany, Punjab Agricultural University, in north-western India (Dhillon and Sidhu 2016). In Punjab
Ludhiana, Punjab 141004, India alone, it severely damaged 60% of the cotton crop leading to a
Author's personal copy
Int J Trop Insect Sci

huge reduction in lint yield from 574 kg-ha in 2014 – 15 to University Regional Research Station, Abohar, India located
197 kg-ha in 2015 – 16 (Dhillon and Sidhu 2016). Moreover, at 30°08’N; 74°12′E with an altitude of 185.78 m above sea
due to the fear of B. tabaci among farmers, the cotton area in level. The study area is characterized as semi-arid, hot and dry.
Punjab dropped to 2.57 lakh hectares in 2016 – 17 from 3.39 This type of climate was symbolized as BWh according to
lakh hectares in 2015 – 16 (Anonymous 2017c). Bemisia Köppen-Geiger classification system (Geiger 1954). The
tabaci causes severe damage to cotton and other crops by study area receives an annual rainfall ranging between 75
sucking sap from the ventral leaf surface, secreting honeydew and 300 mm which mostly occurs from July to September.
on which black sooty mould grows, resulting in reduced pho- During experimental period (SMW 19 to SMW 43), the mean
tosynthetic activities and transmitting viral diseases (Jose and weekly temperatures ranged between 23.0 °C – 31.5 °C,
Usha 2003; Jones 2003; Atwal and Dhaliwal 2007; Nelson 24.9 °C – 31.8 °C and 24.6 °C – 32.7 °C during 2015, 2016
et al. 1998). Both nymphs and adults of whitefly suck the cell and 2017, respectively (Fig. 1a). Automatic Weather Station
sap from different plant parts resulting in loss of plant vigour (Model No. DCPAW502, BioScientific Limited, UK) was
and yield (Attique et al. 2003; Aslam et al. 2004). installed in the study area to record daily weather data (Fig.
Globally, the climate is changing, and abiotic factors like 1a, b and c).
temperature, relative humidity, rainfall, wind speed, wind di-
rection and radiation have a strong impact on the rise and fall Incidence of Bemisia tabaci in cotton
of insect numbers, their survival, growth, multiplicative po-
tential and tritrophic interactions as well (Bale et al. To study the population dynamics of B. tabaci, cotton (variety
2002; Tomar 2010). Complete physiology and development F2228) was sown in April, 25 – 30 during 2015 – 2017 on a
of living organisms experience unforeseen swings at certain plot size of 250 m2. The crop was grown and maintained as
threshold values (Allen and Breshears 1998; Easterling et al. per recommended agronomical practices of Punjab
2000a; Easterling et al. 2000b). Existing studies suggest that Agricultural University, Ludhiana (Anonymous 2015) except
direct effects of temperature are likely to be larger and more for insecticide spray. No insecticide was applied for any of the
important for the growth and development of an organism insect-pest during the period of the experiment. Data on white-
(Bayhan et al. 2005; Pathania et al. 2019). The population of fly incidence was recorded at weekly interval from SMW
whitefly varies in different seasons of the year. Atmospheric 19 – 43. The number of whiteflies was counted from 15 ran-
humidity, temperature and rainfall influence the whitefly pop- domly selected plants. From each plant, 3 leaves were selected
ulation dynamics (Horowitz et al. 1984; Horowitz 1986). The (one leaf from the upper canopy, the 2nd leaf from the middle
use of chemicals is a widely adopted method for the manage- canopy and 3rd leaf from lower canopy of the plant) for taking
ment of B. tabaci (Kaur et al. 2015; Muhammad et al. 2009; adult counts of whitefly.
Tariq et al. 2016; Zamora et al. 2004). However, due to heavy
pest incidence, sole dependence on chemicals and their in- Determination of best timing for whitefly data
creased applications has led to development of resistance collection
(Naveen et al. 2017) or resurgence in insects as well as caused
several ecological and physiological problems for humans, Cotton (variety F2228) sown during last week of April 2016
animals, and beneficial insects thereby affecting the ecological was used for the experiment. Plot size taken was 500 m2. After
balance. Also, as both the insects and their natural enemies 15 days of sowing, the incidence of B. tabaci was monitored
belong to the same class, insecticides usually cause mortality on an hourly basis on randomly selected 15 plants for 60 days
in both (Croft 1990; Naveen et al. 2017; Pathania et al. 2019). on every alternate day. The number of B. tabaci adults was
The present study aimed at investigating the infestation of counted on upper fully opened 3 leaves. The data collected
B. tabaci in cotton, to develop a prediction system for was used to find out the best time for observing whitefly
B. tabaci population based on different weather parameters, incidence in cotton, which could be helpful for decision mak-
and to test the new chemistry with novel mode of action for its ing in developing pest management strategies.
management through better monitoring and timing under field
conditions. Screening of cotton varieties to Bemisia tabaci

Four Bt cotton hybrids viz., RCH 650 (Tolerant), NCS 855,


Materials and methods Ankur 3028 (Susceptible), Bioseed 6588, and five Non-Bt
cotton varieties viz. F1378, F1861, LH2108, F 2228 and
Study site F2383 were sown at Research Farm of Regional Research
Station, Abohar, India during 2016 and 2017 to evaluate their
The present work was carried out during summers of 2015 to resistance against B. tabaci. Plants were maintained as per
2017, at the research farm of the Punjab Agricultural recommended practices of Punjab Agricultural University,
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Int J Trop Insect Sci

Fig. 1 a Weekly maximum and a


minimum temperature (°C) 46 2015 Tmax 2015 Tmin 2016 Tmax
during the study period i.e. 43 2016 Tmin 2017 Tmax 2017 Tmin
2015 – 2017. b Weekly maximum
and minimum relative humidity 40
(%) during the study period i.e. 37

Temperature (°C)
2015 – 2017. c Weekly 34
distribution of rainfall (%) during
the study period i.e. 2015 – 2017 31
28
25
22
19
16
13
19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43
Standard Meteorological Week

b 110 2015 RHmax 2015 RHmin 2016 RHmax


2016 RHmin 2017 RHmax 2017 RHmin
100
90
Relative Humidity (%)

80
70
60
50
40
30
20
10
19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43
Standard Meteorological Week

c 160
150
2017 2016 2015
140
130
120
110
Rainfall (mm)

100
90
80
70
60
50
40
30
20
10
0
19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 43
Standard Meteorological Week

Ludhiana (Anonymous 2015). Each cultivar was maintained plants from each treatment. From each plant, 3 leaves were
on 100 m2 area. The experiment was designed in Randomized selected (one leaf from the upper canopy, the 2nd leaf from the
Block Design (RBD) with nine treatments (varieties) and three middle canopy and 3rd leaf from the lower canopy of the plant)
replicates. Data on whitefly incidence was recorded at weekly for taking adult counts of whitefly. Two sets of the experiment
interval starting from SMW 23 – 44 (22 weeks). The number were planned simultaneously. In the first experiment, the cot-
of whitefly adults was counted from 15 randomly selected ton varieties were grown in open field while in the other set of
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Int J Trop Insect Sci

experiment cotton varieties were grown under shade nets (Hostathion 40% EC, Bayer Crop Science), thiacloprid
which were opened from both sides to allow the whitefly (Splendour 21.7% SC, Cheminova India Ltd.), Verticillium
infestation for 2 months when the crop was 1 month old. lecanii (Bio-Catch 1.15% WP, T Stanes & Company
Seed cotton yield from the different treatment plots were re- Limited), azadirachtin (Neembicidine 300 ppm, T Stanes &
corded and converted to hectare basis. The phytochemical Company Limited) and azadirachtin (Achook1500 ppm,
properties of these cotton varieties i.e. total soluble sugars Organix India Pvt. Ltd.) were used. Based on preliminary
(Dubois et al. 1951; Nelson 1944; Malhotra and Sarkar trials, different concentrations of each pesticide were prepared
1979), total phenols (Singleton and Rossi 1965; Singleton with distilled water and sprayed on the crop to study their
et al. 1999; Chandler and Dodds 1983) and flavonoids efficacy against whiteflies.
(Waage and Hedin 1984) were worked out as per standard
protocols during the season 2016. Statistical analysis

The data generated were subjected to analysis of variance. The


Efficacy of different pesticides in the management of percentage data of adult’s mortality was arcsine transformed
Bemisia tabaci
for statistical analyses. To evaluate the treatment effects, the
means of adult’s mortality were separated using Least
Cotton (cv. RCH 650 BG II) sown during last week of April
Significant Difference (LSD) at 5% probability. Pearson’s cor-
was raised for conducting the experiment. After 75 – 80 days
relation was used to correlate the effect of abiotic factors on
of sowing, when the natural infestation of B. tabaci at its peak
the population build-up of B. tabaci. Paired‘t’ test was used to
the experiment was conducted. The experiment was conduct-
differentiate the incidence of B. tabaci in open field grown and
ed in RBD with three replicates of during 2017 growing sea-
shade grown cotton cultivars. The seed cotton yield data gen-
son. Each experimental unit measured 100 m2. Power operat-
erated were subjected to analysis of variance and means were
ed knapsack sprayer (Mohindra GA-914) of 25 l capacity
separated at LSD 5%. Principal Component Analysis (PCA)
equipped with hollow cone nozzle was used to spray the plot
and development of regression equation for prediction of
at the dose of 100 l of spray solution per acre. Crop in control
B. tabaci population were done using SPSS (Version 20,
treatment was sprayed with water only. Bemisia tabaci
SPSS, Inc. Chicago, Il, USA).
sampling/ population counts were done on each treatment
1 day before and 3, 7, 10 and 14 days after the spray. Five
plants were randomly selected per replication and the number
Results
of B. tabaci living adults on three leaves/ plant (one leaf each
from upper, middle and lower canopy) was counted. The ex-
Incidence of Bemisia tabaci in cotton
periment was conducted twice during the season and the re-
sults were pooled. The corrected per cent mortality was cal-
The data on the population dynamics of B. tabaci in cotton
culated as per Henderson and Tilton’s (1955):
(cv. F2228) for the years 2015 to 2017 are presented on Fig. 2.
Corrected Mortality% B. tabaci infestation on cotton started immediately after ger-
N in control before spray−N in treatment after spray mination of the cotyledons in the first week of May. Both
¼ 1−
N in control after spray−N in treatment before spray nymphs and adults of B. tabaci suck the sap from the leaves
of cotton from early May to end of October (Fig. 2). The
 100
population of B. tabaci adults on cotton ranged from
Where: N = number of whitefly adults / 3 leaves; 0.00 – 70.74 ± 2.62, 1.20 ± 0.59 – 19.65 ± 1.23 and 1.20 ±
For conducting this experiment commercial formulation of 0.15 – 20.88 ± 1.45/ 3 leaves (mean ± SE; N = 15), during
acetamprid (Pride 20% SP, Dow Agro Sciences), buprofezin 2015, 2016 and 2017, respectively (Fig. 2). B. tabaci popula-
(Applaud 25% SC), chlorpyriphos (Dursban 20% EC, Dow tion peaked on 31st (70.74 ± 2.61 adults / 3 leaves), 27th
AgroSciences), clothianidin (Dantotsu 50% WDG, Sumitoma (19.65 ± 1.12 adults / 3 leaves) and 32nd (20.88 ± 0.99 adults
India Pvt. Ltd.), diafenthiuron (Polo 50% WP, Syngenta Crop / 3 leaves) SMW’s during 2015, 2016 and 2017, respectively.
Protection), dinotefuran (Osheen 20% SG, PI Industries Pvt. The incidence of B. tabaci on cotton was significantly higher
Ltd.), ethion (Fosmite 50% EC, PI Industries Pvt. Ltd.), in 2015 (Fig. 2; average: 25.91 ± 2.14 adults / 3 leaves) as
fipronil (Regent 5% SC, Bayer Crop Science), flonicamid compared to 2016 (average: 9.53 ± 1.23 adults / 3 leaves)
(Ulala 50% WG, United Phosphorus Limited), profenophos and 2017 (average: 8.54 ± 1.12 adults / 3 leaves).There were
(Curacron 50% EC, Syngenta Crop Protection), pyriproxyfen two peaks of B. tabaci incidence observed during the study
(Lano 10% EC, Sumitoma India Pvt. Ltd.), spiromesifen period each year. In 2015, the first peak (range: 4.41 ±
(oberon 22.9% SC, Bayer crop Science), thiamethoxam 0.98 – 70.74 ± 2.61) of B. tabaci was observed from 23rd to
(Actara 25% WG, Syngenta Crop Protection), triazophos 31st SMW and second (range: 18.69 ± 1.13–39.60 ± 1.98)
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Int J Trop Insect Sci

Fig. 2 Population dynamics of 80


B. tabaci on cotton (cv. F2228) in 2015 2016 2017
relation to climatic factors during 70

No. of whitefly adults / 3 leaves


2015–2017
60

50

40

30

20

10

0
19 20 21 22 23 24 25 26 27 28 29 30 34 32 33 34 35 36 37 38 39 40 41 42 43
Standard Meteorological Week

from 35th to 38th SMW. However, in 2016 and 2017 the first co-relationship existed between Ta and Tm, Ta and Tmn, Ta
peak of B. tabaci population was observed from 21st to 27th and Ws, Ta and Rd., Tm and Rd., Tm and Ws, Tmn and
and 28th to 33rd SMW (Fig. 2), respectively. B. tabaci popu- RHmn, Tmn and Rd., RHaand RHm, RHa and RHmn,
lation followed a gradually decreasing trend after 39th SMW RHm and RHmn and Ws and Rd. (Table 1).
in all the 3 years of study. Principal component regression analysis (PCRA) was per-
formed using the 10 variables (Table 2) in order to cluster the
Prediction of Bemisia tabaci population correlated weather variables to the smallest possible subsets
expressing the majority of variation. The first 3 PCs (Principal
The degree of linear relationship of B. tabaci population in Components) explained 87.34% variability of data set and
cotton with weather-based observations (Ta: average temper- were, therefore, considered for further analysis. The variables
ature; Tm: maximum temperature; Tmn: minimum tempera- from PC-1 (Tm, Tmn, Ta, Ws, and Rd), PC-2 (RHm, RHmn
ture; RHa: average relative humidity; RHmn: minimum rela- and RHa) and PC-3 (Wd and Rf) having Eigen values >1 were
tive humidity; RHm: maximum relative humidity; Wd: wind taken for explanation. The variation explained by PC-1, 2 and
direction, Ws: wind speed, Rf: rainfall and Rd.: radiations) is 3 was found to be 40.62, 33.02 and 13.70%, respectively
presented through correlation matrix (Table 1). Bemisia tabaci (Table 2). Due to the non-significant correlation of Ta, Tm,
population was observed to be highly correlated with Tmn, Ws, and Rd. with whitefly adult population, Ta, Tm, Ws, and
RHa, RHmn, RHmand Rf. It was also observed that a better Rd. were not considered by PC-1 to develop principal

Table 1 Correlation matrix (Pearson’s) for weather-based observations with B. tabaci population during 2015–2017

Variables Wf Ta Tm Tmn RHa RHm RHmn Rf Wd Ws

Ta NS
Tm NS 0.79**
Tmn 0.50* 0.81** 0.31**
RHa 0.70** 0.55** 0.90** NS
RHm 0.47* 0.68** 0.87** NS 0.95**
RHmn 0.92** NS 0.69** 0.44** 0.87** 0.70**
Rf 0.32** NS 0.22** NS 0.22 NS 0.37**
Wd NS NS NS 0.27* 0.35** 0.28* 0.36** NS
Ws NS 0.74** 0.46** 0.72** 0.38** 0.56** NS NS NS
Rd NS 0.81** 0.66** 0.69** 0.50** 0.55** 0.20 NS NS 0.88**

Wf: whitefly adult population / 3 leaves; Ta: average temperature (°C); Tm: maximum temperature (°C); Tmn: minimum temperature (°C); RHa: average
relative humidity (%); RHmn: minimum relative humidity (%); RHm: maximum relative humidity (%); Rf: rainfall (mm); Wd: wind direction (°); Ws:
wind speed (m-s ) and Rd.: radiation (W/m2 ). Bold digits in the table indicate the “–” correlation data; data followed by ‘*’ indicates their significant
correlation at P < 0.05 and data followed by ‘**’ indicate their significant correlation at P < 0.01; NS: not significant
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Int J Trop Insect Sci

Table 2 Principal components


(PCs) with Eigen values and var- PCs Variables Eigen value % Variance Cumulative % of Variance
iances in B. tabaci population in
cotton 1 Ta, Tm, Tmn, Rd., Ws 4.468 40.615 40.62
2 RHa, RHm, RHmn 3.633 33.02 73.64
3 Wd, Rf 1.507 13.701 87.34

component regression (PCR). Both the Rhm and RHmn were Screening of cotton varieties to Bemisia tabaci
selected from PC-2 for PCRA, due to its better association
with B. tabaci dynamics. However, from PC-3, Rf only was All cotton cultivars showed susceptibility to B. tabaci
accepted because of its substantial correlation with B. tabaci adults to a varying extent under both open and shade
population. The multi-regression equation developed between conditions (Table 3). Significant differences were ob-
B. tabaci population and other selected weather variables served in B. tabaci infestation among cultivars grown un-
(Tmn, RHm, RHmn and Rf) from PCA and correlation matrix der open (F8,19 = 6.27; p = 0.023) and shade (F8,19 = 3.66;
for 2015 to 2017 was: p = 0.019) conditions. The incidence of B. tabaci in culti-
Whitefly adult population / 3 leaves = 0.348 (Tmn) – 0.044 vars grown under shade appeared earlier in comparison to
(RHm) + 0.649 (RHmn) – 0.005 (Rf) – 0.012 – 15.689 (at those grown in open field. Moreover, the population
P < 0.05; R = 0.93; R2 = 0.87 and RMSE = 3.41%). build-up of B. tabaci was very high (15.77 ±
0.85 – 23.35 ± 1.92 adults / 3 leaves) among the cultivars
Timing for whitefly sampling in cotton grown under shade. However, it varied from 9.45 ±
0.87 – 11.27 ± 1.44 adults / 3 leaves in different cultivars
Daily whitefly adult counts taken at hourly interval for under open field grown cotton (Table 3). The whitefly
2 months starting from May 13, 2016 to July 02, 2016 showed infestation was higher in cultivar Ankur 3028 which was
significant differences between the time of samplings in terms statistically at par with F2228 under both open and shade
of number of whitefly adult recorded (Fig. 3). Overall, conditions. However, F1861 and RCH 650 had compara-
B. tabaci adults were observed in higher numbers when sam- tively lower B. tabaci adult population under open and
pled before 10:00 AM (F4,25 = 7.82; p = 0.032; N = 15) shade conditions, respectively (Table 3). In general,
followed by whitefly counts before 7:00 AM (Fig. 3). SMW 27 to 30 favoured the incidence of B. tabaci pop-
Population counts taken before 4:00 PM showed the mini- ulation (Fig. 2). Significant differences were observed in
mum adult population counts of B. tabaci (Avg. = 8.91 ± yield (Table 3) of different cotton cultivars grown under
0.85 adults/ 3 leaves; N = 15). open and shade conditions (F8,2 = 26.30 & 32.26 for open

Average no. of whitefly adults / 3 leaves


Fig. 3 Fluctuations in B. tabaci
18
counts in cotton crop at different 16
14
intervals of the day 12
10
8
7:00 AM 10:00 AM 2:00 PM 4:00 PM 6:00 PM 6
100 4
2
90 0
7:00 AM 10:00 AM 2:00 PM 4:00 PM 6:00 PM
Time intervals
80
No. of whitefly adults / 3 leaves

70

60

50

40

30

20

10

Observation Dates
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Table 3 Incidence of B. tabaci in


different cultivars in different S. Cultivar No. of whitefly adults / 3 leaves (Mean ± S.E.) Paired ‘t’ Yield Kg/ha
conditions during 2016–2017. No. value
(Data recorded for 20 weeks; 15 Open Shade Mean Open Shade
plants/variety / week were
observed) 1 RCH 650 9.49 ± 1.27ab 15.77 ± 1.24a 6.28 ± 0.85 7.383** 2877b 2545ab
b a ** a
2 NCS855 9.56 ± 1.63a 19.47 ± 2.05 9.91 ± 0.69 14.286 3286 2770a
3 Ankur3028 11.27 ± 2.10f 23.35 ± 2.79f 12.07 ± 1.03 11.695** 2765bc 2140bc
4 Bio6588 10.76 ± 1.86d 21.04 ± 3.31ef 10.28 ± 1.49 6.876** 3142ab 2322b
5 F1378 9.89 ± 1.35c 20.80 ± 2.31e 10.92 ± 1.48 7.364** 2453c 2053bc
6 F1861 9.36 ± 1.06a 19.48 ± 1.88b 10.59 ± 0.98 10.837** 2315c 1985c
7 LH2108 9.82 ± 1.37c 19.95 ± 2.13c 10.13 ± 0.89 11.319** 2257c 1840c
8 F2228 11.02 ± 1.80e 23.17 ± 2.53f 12.15 ± 0.92 13.219** 2354c 2025bc
9 F2383 9.26 ± 1.38a 20.26 ± 2.32d 11.00 ± 0.97 11.304** 2683bc 1835c
LSD (P = 0.05) 0.21 0.26 366 310

Values (mean ± SE) with the same letter within a column are not significantly different at p < 0.05
‘**’ indicate the significance of paired‘t’ test at P < 0.01

and shade grew cotton, respectively; p = 0.025. NCS 855 reduction of phenol contents (6.24 folds) was recorded in
recorded maximum yield under both open (3286 kg/ha) Ankur 3028 grown in shade over open conditions (Fig. 5).
and shade (2770 kg/ha) grown conditions. Flavonoids production differed significantly across different
The results of biochemical analysis of leaf tissues revealed cultivars and different conditions of cultivation (F1,8 = 10.32;
significant differences among cultivars grown under different p = 0.012). Higher production of flavonoids (range: 14.62 ±
conditions (Figs. 4, 5 and 6). Total soluble sugars (mg/g DW) 0.64 – 48.48 ± 2.32 μg/g DW; Cultivars = 9; N = 3) was ob-
content was higher in plants grown in open and decreased in served in plants grown under open conditions as compared to
plants grown under shade in all the cultivars except Ankur those grown under shade effect (range: 1.98 ± 0.04 – 33.75 ±
3028 (Fig. 4). The cultivar Ankur 3028 had lower sugars 1.30 μg/g DW; Cultivars = 9; N = 3). RCH 650 was found to
(F1,8 = 10.63; p = 0.011) content both under open conditions produce higher flavonoids, whereas, it was lowest in F1861
(6.85 mg/g DW) and shade conditions 6.84 mg/g DW). under both the conditions, respectively.
Significant differences were observed in sugar content among
all the cultivars grown under different conditions (F1,8 = 6.38; Management of Bemisia tabaci in field
p = 0.008). Bioseed 6588 had higher sugar content (20.41 and
11.55 mg/g DW, respectively in open and shade conditions) The pooled data of two trials conducted during 2017 on per-
compared to other cultivars. Similarly, significant reduction in cent reduction of B. tabaci adult population 3, 7, 10 and
phenol (μg/g DW) content was observed in all cotton cultivars 14 days after treatment with different pesticides is presented
when grown under shade (range: 21.86 ± 1.85 – 76.99 ± in Table 4. There were significant differences between differ-
3.21 μg/g DW; Cultivars = 9; N = 3) as compared to open ent treatments 3 days (F(17,4) = 5.46, p = 0.021), 7 days
(range: 42.78 ± 2.85 – 221.0 ± 8.21 μg/g DW; Cultivars = 9; (F(17,4) = 6.27, p = 0.034), 10 days (F(17,4) = 9.45, p = 0.015)
N = 3) conditions (F 1,8 = 8.67; p = 0.012). Maximum and 14 days (F (17,4) = 3.71, p = 0.031) after pesticide

Fig. 4 Variation in sugar levels 24


(leaf tissues) among different 22
Sun Shade
Total Soluble Sugars (mg/g DW)

varieties/hybrids of cotton grown 20


under open and shade 18
16
14
12
10
8
6
4
2
0
Bioseed Ankur F 1861 BT RCH F 2383 F 1378 LH 2108 F 2228 NCS 855
6588 3028 650
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Int J Trop Insect Sci

Fig. 5 Production of phenols 270


Sun Shade
among different cotton varieties/ 240

Total Phenols (µg/g DW)


hybrids grown under open and
210
shade
180

150

120

90

60

30

0
Bioseed Ankur F 1861 BT RCH F 2383 F 1378 LH 2108 F 2228 NCS 855
6588 3028 650

application. All the treatments caused significant reduction Discussion


of B. tabaci adults when compared to control (Table 4).
After 3 days, diafenthiuron 50 WP @ 500 g/ha was most Abiotic factors like temperature, relative humidity etc. play a
effective in reducing B. tabaci population but was statis- very important role in initial infestation, promoting spread,
tically at par with thiamethoxam, flonicamid, dinotefuran, and further development of insect-pests (Bale et al. 2002;
fipronil and clothianidin. Nimbicidine and Achook caused Tomar 2010; Pathania et al. 2019). Moreover, changes in abi-
30.99 and 31.11% reduction in the population of otic factors viz. temperature, CO2, and relative humidity alter
B . t a b a c i , r e s p e c t i v e l y, a f t e r 3 d a y s o f s p r a y. the nutritional composition of host plants, which may render it
Pyriproxyfen was the least effective treatment after 3 days unpalatable or nutritionally better for the herbivores (Sterner
of spray (24.14% reduction) and was at par with and Elser 2002). Bemisia tabaci is a thermophilic insect
spiromesifen. Maximum reduction (range: (Avidov 1956) and it is evident from the present study that
42.91 – 77.01%) in B. tabaci population was obtained at this pest is well adapted to cotton-agroecosystem, to build-up
7 DAS (Table 4). Flonicamid was found to be the best in its population faster during the summers. Being polyphagous,
reducing B. tabaci population (77.01%) at 7 DAS, but B. tabaci remains active in low or high numbers around the
was statistically at par with clothianidin (74.70%) and year on other crops or weed host plants (Hussain and Trehan
thiamethoxam (70.09%) followed by diafenthiuron 1933; Hussain et al. 1936; Butler Jr et al. 1986; Johnson et al.
(66.35%). Pyriproxyfen (68.62% reduction) and 1982; Melamed-Madjar et al. 1979; Gerling 1984; Gerling
flonicamid (62.43% reduction) gave the best results after 1996). Our studies indicate that it shifts to cotton seedlings
10 days of spray application and were statistically at par immediately after the cotton emergence during mid-May and
with each other. Ethion was found least effective treat- establishes itself by the end of June on the upper leaves of the
ment in reducing B. tabaci population (26.42%) after plant. The young and succulent leaves of cotton plant lure
10 days of spray. Verticillium lecanii was found moder- B. tabaci to build up faster. Maximum incidence of B. tabaci
ately effective with 40.80% reduction in B. tabaci popu- was recorded during July and August which was in agreement
lation after 10 days of spray application. The efficacy of with the findings of Abro et al. (2004), Hanumantharaya et al.
different treatments persisted up to 10 days of spray (2008), Solangi et al. (2008), Godhani et al. (2009) and Babu
application. and Meghwal (2014). Maximum (range: 31 to 40.04 °C) and

Fig. 6 Fluctuation in flavonoids 55


Sun Shade
levels among different cotton 50
varieties/hybrids grown under 45
open and shade 40
Flavonoids (µg/g DW)

35
30
25
20
15
10
5
0
Bioseed Ankur F 1861 BT RCH F 2383 F 1378 LH 2108 F 2228 NCS 855
6588 3028 650
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Int J Trop Insect Sci

Table 4 Bio-efficacy of different pesticides against Bemisia tabaci in cotton during 2017

S. No. Treatment detail Dosage (g/ml)/ha % reduction in whitefly adults /3 leaves in cotton (Pooled data of 2 trials)

3 DAT 7 DAT 10 DAT 14 DAT

1 Acetamprid 20SP 100 36.72(36.82)bc 60.22(51.02)bc 36.59(37.02)bc 15.54(22.61)b


2 Buprofezin 25SC 1000 44.22 (41.57)bc 58.08 (49.70)bc 35.88 (36.51)bc 6.41 (12.19)bc
3 Chlorpyriphos 20EC 1250 47.39 (43.37)b 66.12 (54.73)b 29.11 (31.15)c 5.47 (10.61)bc
4 Clothianidin 50DWG 40 49.42 (44.61)ab 74.49 (59.80)ab 58.35 (49.85)ab 39.52 (38.82)a
5 Diafenthiuron 50WP 500 63.07 (52.84)a 66.35 (54.61)b 50.78 (45.42)b 24.61 (28.75)ab
6 Dinotefuron 20SG 125 55.27 (48.04)ab 62.50 (52.28)bc 52.44 (46.41)ab 27.63 (30.32)ab
7 Ethion 50EC 2000 47.23 (43.28)b 51.68 (45.98)cd 26.42 (29.80)c 1.58 (3.57)c
8 Fipronil 5SC 1500 52.70 (46.52)ab 61.23 (51.53)bc 29.89 (32.94)c 9.06 (16.41)b
9 Flonicamid 50WG 150 58.73 (50.08)ab 77.01 (61.67)a 62.43 (52.26)ab 40.56 (39.27)a
10 Profenophos 50EC 1250 39.78 (36.27)bc 45.50 (40.62)d 43.30 (41.03)bc 12.51 (17.44)b
11 Pyriproxyfen 10EC 1250 24.14 (28.70)c 61.03 (51.45)bc 68.62 (56.23)a 37.61 (34.99)a
12 Spiromesifen 22.9SC 500 26.54 (30.67)c 50.21 (45.10)cd 48.17 (43.89)b 18.75 (22.20)b
13 Thiamethoxam 25WG 100 62.20 (52.14)a 70.09 (57.12)ab 49.43 (44.65)b 10.37 (14.36)bc
14 Triazophos 40EC 1500 41.40 (39.97)bc 54.77 (47.81)c 42.26 (40.45)bc 13.03 (18.16)b
15 Verticillium lecanii 1.15WP 2500 36.27 (36.51)bc 43.42 (41.00)d 40.80 (38.86)bc 19.00 (22.06)b
16 Nimbicidine 300 ppm 2500 30.99 (33.71)c 42.91 (40.63)d 35.75 (36.31)bc 15.71 (22.14)b
17 Achook 1500 ppm 2500 31.11 (33.05)c 42.91 (40.88)d 36.29 (36.89)bc 14.31 (21.20)b
18 Thiacloprid 21.7 SC 600 44.85 (41.97)bc 54.90 (47.85)c 48.19 (43.94)b 23.48 (23.80)ab
LSD (p = 0.05) (8.64) (6.27) (9.45) (12.37)

Values in parenthesis are arcsine transformed; DBT days before treatment, DAT days after treatment
Values (mean ± SE) with the same letter within a column are not significantly different at p < 0.05

minimum temperature (range: 22.9 to 27.66 °C), morning insect-pests (Bale et al. 2002; Tomar 2010). During the study,
relative humidity of 75 to 97% and evening relative humidity we observed a significant positive correlation of B. tabaci
26 to 70% is favourable for multiplication of B. tabaci in population build up with minimum temperature, maximum,
cotton. Kaur et al. (2009) reported that the peak of whitefly minimum relative humidity, and rainfall which are in conso-
population was observed when the maximum and minimum nance with the findings of Purohit et al. (2006), Umar et al.
temperature was less than 36 °C and more than 26 °C, respec- (2003), Kataria et al. (2017) and Janu and Dahiya (2017).
tively. However, Prasad et al. (2008) and Reddy and Rao Earlier studies carried by Tomar (2010) on cotton aphid,
(1989) observed a somewhat different maximum and mini- Aneni et al. (2014) on oil palm leafminer and Pathania et al.
mum temperature range of 29 - 32 °C and 18 - 22 °C, respec- (2019) on pomegranate aphid also emphasized higher corre-
tively, for the population build-up of whitefly which may be lation of insect population with weather factors. Opposite to
attributed to the different regions of study or different ecotype the findings of Selvaraj et al. (2010) and Singh and Butter
of B. tabaci. The population build-up during 2016 and 2017 (1985), the maximum temperature was found to have a non-
shown somewhat similar trend, however, it was exceptionally significant correlation with B. tabaci population in our case,
very high in 2015. The possible reason for this was compara- which might be attributed to different ecological conditions
tively lower temperature and higher RH during 2015 as com- and their interaction with the insect. Wind speed, wind direc-
pared to 2016 and 2017. More frequent rains (384.40 mm) tion, and solar radiations showed non-significant relation to
between SMW 19 to 43 (Fig. 2) during 2015 caused reduction B. tabaci population dynamics, which was also reported by
in average minimum and maximum temperature by 1 – 2 °C Shitole and Patel (2009).
(Fig. 1a and c) and increase in RH by 2 – 3% which resulted in Regular monitoring and surveillance of insect-pests in dif-
favourable microclimate (Fig. 2) for B. tabaci to develop and ferent crops play important role in decision making for
spread in cotton fields. However, moderate to heavy rainfall implementing timely management options (Aslam et al.
and comparatively higher temperature recorded between 2001; Kalaris et al. 2014).Several sampling methods have
SMW 22 to 26 in 2017 resulted in the delay of the first peak been developed to monitor whitefly (Aslam et al. 2001;
of B. tabaci in cotton. Prevailing weather conditions greatly Naranjo and Flint 1995; Tonhasca et al. 1994; Butler Jr et al.
influence the change in the biology and population build-up of 1986; Ohnesorge and Rapp 1986) but there was lack of
Author's personal copy
Int J Trop Insect Sci

information regarding sampling time. We found that the infestation of B. tabaci in shade-grown cultivars could be one
B. tabaci adult counts in cotton grown in summer were sig- of the reasons for the reduced activity of sugars, phenols, and
nificantly higher if sampled before 10:00 AM in the morning flavonoids. Our findings were corroborated with the outcomes
hours as compared to the rest of the day. These results suggest of Wei et al. (2010) who observed a decrease in soluble sugars
that monitoring of B. tabaci in cotton should be done before in different plant hosts due to infestation of Lygus lucorum
10:00 hours for saving time and predicting the actual situation Mayer-Dur 1843 (Hemiptera: Miridae). Similarly, a decrease
of the field, which may help in timely management of this in protein content and deterioration of starch properties in
pest. barley due to Metopolophium dirhodum (Walker, 1849)
Distinguishable infestation in all the nine cotton cultivars (Hemiptera: Miridae) infestation was also verified by Lornez
was noticed around mid-June, though B. tabaci incidence in and Collins (1989). Aphids utilize amino acids from phloem
cotton most likely had started earlier by mid of May. We have sapto meet out their nitrogen requirements and deplete protein
observed differences in susceptibility among cotton cultivars content (Douglas 2003). Ojimelukwe et al. (1999) observed
to B. tabaci infestation under similar environmental condi- that infestation of pulse beetles in cowpea seeds led to the
tions. Though, no cultivar was free from infestation, Ankur depletion of protein, starch and sugar content. Reduction of
3028 and Bioseed 6588 were found most susceptible cultivars, soluble sugar, protein, and amino acid content was also no-
however, RCH 650 showed comparatively lower infestation ticed in highly infested fuji apple twigs by woolly apple aphid,
of B. tabaci. One of the possible reasons for the higher infes- Eriosoma Lanigerum (Zhou et al. 2013) was in concurrence
tation in Ankur 3028 and Bioseed 6588 was its more succulent with our results. Furthermore, we tried to establish a linear
new growth. Several workers already observed that the association with the B. tabaci infestation versus leaf nutrient
growth, development, survival, and reproduction of insects status and the results revealed a negative correlation of leaf
were affected by the characteristics of host plant to some ex- total soluble sugars (Pearson’s = − 0.29; R2 = 0. 80; p < 0.05),
tent (Tsai and Wang 2001; Liu et al. 2004; Akkopru et al. total phenol contents (Pearson’s = − 0.48; R2 = 0.23; p < 0.05)
2015). An ecological explanation for the detected pattern of and flavonoids content (Pearson’s = − 0.58; R 2 = 0.34;
infestation in different cotton cultivars could be due to selec- p < 0.05). It was obvious from the studies that shady area
tive behaviour of whiteflies. Furthermore, the cultivars grown was most preferred for the initiation of infestation by
in shade were much preferred by B. tabaci and experienced B. tabaci, moreover, both shade effect and higher infestation
more damage as compared to genotypes grown in open con- of B. tabaci interfere with the host plant secondary metabolite
ditions. It was noticed earlier that B. tabaci infestation in field production.
was higher on the border rows wherever there were shade In our experiment, eighteen pesticides were tested against
effects of trees, walls etc. near the standing crop (unpublished B. tabaci under field conditions, among these, some were
report). The possible reason for higher infestation under shade found effective while others were found less effective in con-
was the 1 – 2 °C difference in minimum and maximum tem- trolling B. tabaci in cotton. The applied treatments didn’t
perature and 5 – 10% difference in minimum and maximum show any phytotoxic effect on cotton plants. From the results
relative humidity, which is more favourable for the build-up of it can be concluded that the tested pesticides can be grouped in
B. tabaci population. Also, such an area could serve as a to 2 categories viz. flonicamid (belongs to IRAC Group 29,
reservoir of the pest for further infestation which should be rapidly inhibit the feeding), clothianidin (broad spectrum sys-
checked by timely monitoring of B. tabaci population in the temic insecticide acts as acetylcholine agonist), diafenthiuron
border areas of cotton fields. (a proinsectide, caused immediate paralysis) and
Total sugars, phenols, and flavonoids were higher in all the thiamethoxam (broad spectrum systemic insecticide) gave im-
cotton cultivars when grown in open conditions as compared mediate results within 2–3 days of spray and remain effective
to plants of the same cultivar grown under shade. Moreover, up to 10 days after spray, whereas the other group viz.
the infestation of B. tabaci was exceptionally high in the pyriproxyfen (a JH analogue) and spiromesifen (a tetronic
shade-grown cultivars in comparison to open-grown cotton acid derivative and lipid biosynthesis inhibitor) were slow in
cultivars. Solar radiations, quality, and intensity of light play action initially because of their mode of action but gave better
a substantial effect on biochemicals metabolism/ synthesis, results afterwards and were effective for 10–14 days after
thus influencing the flavonoid biosynthesis (Dussi et al. spray. The differences in relative toxicity of these pesticides
1995). Romani et al. (2002) and Bruckova et al. (2016) also were due to their different mode of actions. If we see the
observed higher flavonols content in open-air grown lettuce average control of B. tabaci provided by different treatments,
plants than in greenhouse conditions grown plants. Moreover, maximum reduction was achieved by flonicamid 50 WG
the content of phenolic compounds in different crops could be followed by clothianidin 50 WDG, diafenthiuron 50 WP,
influenced by different conditions viz. agronomical, environ- dinotefuran 20SG thiamethoxam 25 WG and pyriproxyfen
mental and the genetic background of the host plant (DuPont 10 EC. Similar results have been observed by Rajasekhar
et al. 2000; Tomas et al. 2000; Nicolle et al. 2004). The higher et al. (2018) and Kharel et al. (2016) which corroborates our
Author's personal copy
Int J Trop Insect Sci

findings. Diafenthiuron provided good control of whitefly particular insect-pest or disease involving the abiotic fac-
adults, as already reported by Aslam et al. (2004), Tariq tors is of great significance in pest management. The in-
et al. (2016) and Kharel et al. (2016). Kadam et al. (2014) also festation of whitefly appeared first in border/ shady parts of
reported the effectiveness of dinotefuran 20 SG and the field; and both growing conditions and B. tabaci infes-
clothianidin 50 WDG in controlling B. tabaci in cotton, tation affects the defence mechanism of the plant via reg-
which is in consonance to our findings. The results of the ulating secondary metabolite production ability of cotton
present studies are not in agreement with the results of Kaur plants. In general the study warrants the adoption of pest
et al. (2015) who determined that trizophos was most effective monitoring for timely decision making in formulating pest
insecticides against whitefly as it was found less effective management strategies. Need-based and timely applica-
against B. tabaci in our trials. Repetitive and over excessive tions of pesticides with modern chemistry viz. flonicamid
use of same insecticide is one of the major reasons in 50 WG, pyriproxyfen 10 EC, dinotefuran 20 SG and
reduction of susceptibility of B. tabaci to that particular diflubenzuron 50 WP are effective against B. tabaci under
insecticide. Because of this the insecticides earlier field conditions and can be included in Integrated Pest
recommended against B. tabaci are no longer effective to Management strategies against B. tabaci in cotton.
control this pest. Similarly, Naveen et al. (2017) in a large
scale experiment from different populations of B. tabaci from Acknowledgments We are grateful to reviewers and editor for their crit-
ical review and constructive inputs for the improvement of this manu-
different parts of India on insecticide resistance reported that
script. Thanks are due to Director PAU, Regional Research Station,
Asia-I and Asia-II populations of B. tabaci shown a decline in Abohar, for providing necessary facilities to conduct this study.
susceptibility to cypermethrin, deltamethrin, monocrotophos
and imidacloprid. Furthermore, we have also tested bio- Authors contribution MP and PKA conceived and designed the research.
pesticides viz. Verticillium lecanii, Nimbicidine and Achook, MP, MS and AV conducted the experiments. NK conducted the biochem-
ical analysis of the cotton leaf tissues. MP and AV analysed data. MP
but all were found less effective (<35% average mortality) in
wrote the manuscript. All authors read and approved the manuscript.
controlling B. tabaci under field conditions. Their maximum
control (up to 43% reduction) was achieved up to 7 days after
Compliance with ethical standards
the spray and afterwards, they became ineffective in providing
good control of this pest. However, there were some reports of Disclosure statement The authors have no conflict of interest.
the better efficacy of V. lecanii against B. tabaci in tomato
(Sharma et al. 2015); in Okra (Janghel and Rajput 2016).The
possible reason for their less effectiveness may be high tem- References
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