Pesticide Induced Resurgence of Rice Planthoppers major resurgence species are as follows: BPH- Nilaparvata lugens Stal WBPH- Sogatella furcifera Horvath SBPH- Laodelphax striatellus Fallen Introduction Type and Form of Resurgence Population Characteristics of Planthopper Resurgence Resurgence Factors of planthoppers Planthoppers reproduction associated factors Hormoligosis Pesticides influence male accessory gland protein Conclusion Prospective Research Direction

1. Speaker
Devendra K. Meena
Chairman Seminar Leader
Dr. Bishwajeet Paul Dr. Sachin S. Suroshe
Division of Entomology
ICAR- Indian Agricultural Research Institute
New Delhi
Pesticide Induced Resurgence of Rice Planthoppers

2. Contents
 Introduction
 Type and Form of Resurgence
 Population Characteristics of Planthopper Resurgence
 Resurgence Factors of planthoppers
 Planthoppers reproduction associated factors
 Pesticides influence male accessory gland protein
 Conclusion
 Prospective Research Direction

3.  Planthoppers are most problematic & serious insect pest of rice crops
across Asia.
 Several species are prevalent in agro ecosystems of rice but major
resurgence species are as follows:
1. BPH- Nilaparvata lugens Stal
2. WBPH- Sogatella furcifera Horvath
3. SBPH- Laodelphax striatellus Fallen
(Zhang et al., 2014)
The Concept
 Pest resurgence came in 1960s, caused mainly by insecticides that
indiscriminately killed beneficial arthropods and target pests
(Bartlet, 1964)
Introduction

4.  Resurgence an abnormal increase in
pest population or damage following
pesticides application often far
exceeding the EIL
 Pesticide cause changes in the pest’s
behaviour, dispersal, development and
fecundity or enhanced reproduction
indicating the resurgence.
(Hardin et al., 1995).
Cont…
N. lugens
S. furcifera
L. striatellus

5. Types of Resurgence
Primary pest resurgence:
 Target pest population responds to a pesticide
treatment by increasing to a level at least
higher than the population level observed
before the treatment.
A: Both majority of Pests & Natural
enemies (NEs) were killed.
B: Plant pests re-colonize first.
C: Pest unrestrained by NEs then increase
to a level greater than A.
A
B
C
 The type of resurgence found on the modern cropping system
(Dutcher, 2007)

6. Secondary pest resurgence:
 Occurs when a non-target, but
injurious, pest population increases
in a crop after it is treated with a
pesticide to control a primary pest
population.
A: Pesticide is applied to suppress pest 1
but also kills natural enemies that feed
on pest 2.
B: Pest 2 free from regulation of NEs then
pest 2 becomes a major problem.
Cont…

7. Conceptual Framework of Forms of Resurgence
Based on the time related process ( Wu et al., 2019).

8. Population Characteristics of Planthopper
Resurgence
 After applications of insecticides, planthopper populations were suppressed
for approximately 3 days, then rapidly rebounded.
 Patterns of BPH & WBPH population size changes after application of
Triazophos :
a. A continuous population increase to a peak followed by a decline
b. An immediate decline
c. A decline followed by a higher peak and then a decline.
(Wu et al., 2019)

9. Cont…
 Sublethal Nitenpyram concentrations led to increased
macropterous/brachypterous BPH ratios.
 Symptoms of resurgence population:
a) Larger number of planthopper individuals with flight-capability
b) Increase theromotolerance
c) Increase body weight
d) Increase valvula length
e) Stimulate reprodution
f) Hopper burn in rice field
(Wu et al., 2019)
Hopper burn

10. Reduction in competitive
pest species
Reduction of NEs
services
Influence rice physiology
and biochemistry Insecticide rate
Insecticide type
Timing of insecticides
application
Method of application
Sub-lethal doses of
insecticides
Influence parasitoid
behaviour and fecundity
Influence rice gene
transcription profiles
Influence plant
hormones
Pesticide-induced
susceptibility to planthoppers
Mortality of natural
enemies
Resurgence
Altered survival of
Different satge of target
pest
Stimulation of feeding &
Reproduction of target pest
Stimulation of
neurosecretory forces to
enhance yolk formation
A
B
CD
Factors influencing pesticide induced resurgence of plant hoppers.
A: Host plant, B: Related to NE,s & other insects, C: Insecticides D: Planthoppers
(Chelliah and Bharathi, 1993)
Resurgence factors of planthoppers

11. Influence of pesticides on physiology and biochemistry
of rice plants
 Oxalic acid (OA) acts in rice resistance to BPH, but triazophos and imidacloprid,
lead to reduced OA content in rice which favourable for BPH feeding.
 Buprofezin, imidacloprid, and decamethrin lead to higher reduction of sugars and
free amino nitrogen which benefits to planthoppers.
 Concentrations of the insect inhibitory neurotransmitter γ-aminobutyric acid in rice
plants were reduced following treatments with the herbicides, butachlorebtazone,
the antibiotic jinggangmycin (JGM).
(Cheng et al., 2012; Lui et al., 2012).

12.  Cytokinins, including zeatins riboside (ZR), act on cell division, elongation and
influence the intensity and direction of photosynthate flows.
 ZR content in rice leaves decreased significantly three days after separate foliar
sprays & rice root treated with buprofezin, imidacloprid, JGM and triazophos.
 The level of malondialdehyde (MAD) in rice leves and sheath increase by the
application of imidacloprid that facilitate to BPH feeding.
(Qiu et al., 2004).
Cont..

13. Pesticides influence rice gene transcription
profiles
 225 genes that were differentially expressed after an imidacloprid
treatment; 117 were up-regulated, and 108 were down-regulated.
 Of these, specific expression of genes encoding plant lipid transfer
protein, lignin peroxidase, and flavonol-3-o-methyl transferease was
changed.
 This type of change responsible for the imidacloprid induced rice
susceptibility to BPH, which inflicted more damage on treated than
control rice plants. (Cheng et al., 2012)

14. Pesticide-induced susceptibility to planthoppers
 PIS facilitates planthopper feeding, survival, and fecundity and may there by
promote resurgence.
 Applications of bisultap, imidacloprid, JGM, butachlor, bentazone, metolachlor,
bensulfuron-methyl, acetochlor, are led to increased damage level of rice plant
infested by Planthoppers.
 Repeated pesticide applications extended the duration of PIS, which, again, may
facilitate planthopper resurgence.
(Wu et al., 2001)

15. Case study-I
Aim of study:
 This study was to clarify the mechanism of insecticide-induced
susceptibility to BPH.

16. Materials and methods
Materials
 The rice (Oryza sativa L.) variety, Zhen Dao 2 (japonica rice) was used in the
trials.
 Laboratory starin of BPH used.
 Foliar sprays were applied with 30 and 60 ppm Imidacloprid.
Quantification of imidacloprid induced biochemical changes
 Malondialdehyde (MDA) levels & oxalic acid levels, are important
indicators of resistance to BPH.
 Measured MDA & oxalic acid level then rice plants to examine the
susceptibility of rice plants to BPH after exposure to Imidacloprid (IMI).

17.  Imidacloprid treatments viz., 60
and 30 ppm significantly
increasing injury level of rice
plants infested by BPH nymphs
compared to the untreated
control plants
 Damage levels on 60 ppm
imidacloprid teatment was
significantly greater than for
the 30 ppm imidacloprid
treatment.
Finding of study
Effect of Imidacloprid on the injury
level of rice plants infested by BPH

18.  Imidacloprid, significantly affected the amount of MAD & oxalic acid.
 Significantly, greater amounts of MAD were present in the leaf blades
treated with 30 and 60ppm imidacloprid at 3 and 6 day after foliar
spray (DAF) compared to the leaf blades of the control.
 However, the oxalic acid content of leaf sheaths at 3, 6 and 9 DAF was
significantly, lower than the oxalic acid content of the control samples.
Finding of study
Effects of imidacloprid on the level of (A) MDA content, (B) Oxalic acid
content in rice plants

19. Impacts of pesticide application on natural
enemies of planthoppers
 Agricultural chemicals challenge
natural enemies in two ways:
i. by killing some individuals
and, in surviving individuals
ii. by sharply reducing their
abilities to search for and
locate pest eggs, larvae, pupae,
and adults.
(Wu et al., 2019)
Lycosa pseudoannulata
Cyrtorhinus lividipennis

20. Pesticides effect on natural enemies
Natural enemies Pesticides Effect References
Cyrtorhinus
lividipennis
Butachlor, Disopropyl S-
benzyl phosphorothiolate,
Triazophos and
Deltamethrin
High mortality,
Reduction in prey
consumption
Cheng et
al.,1999; Xu et
al.,2000
Lycosa
pseudoannulata
Chlorpyriphos, Abamectin, More lethal Cheng et
al.,1999)
Pirata subpiraticus Bisultap, Methanidophos
and Buprofezin ,
Triazophos and
Pymetrozine , Butachlor,
Oxyfluorfen, Oxadiazon,
and Metolachlor
Functional response
less to prey , Negative
effect on egg
development
Li et al., 2000
Anagrus nilaparvatae Pymetrozine ,
Imidacloprid, Triazophos
and Deltamethrin
Reduction in foraging
capacity, Sensory
response, Survival &
parasitism
Liu et al.,2010

21. Fig. Comparisons of arrangement of yolk granules of egg of P.subpiraticus
(a) Untreated control, (b) Pymetrozine treated eggs c) Triazophos-treated eggs.
(Xu et al., 2000)
 Triazophos and pymetrozine have a serious negative effect on egg development of
the P. subpiraticus
 Yolk granules in eggs showed a loose arrangement, and some eggs remain empty.

22. Pesticide BPH WBPH SBPH
Abamectin + × ×
Acetochlor + × ×
Bentazone + × ×
Bisultap + × ×
butachlorebtazone + × ×
Carbamate + × ×
Carbendazim + × +
Carbofuran + × ×
Carbaryl + × ×
Chlorpyrifos + × ×
Cyclosulfamuron + × ×
Daizinon + × ×
Jinggangmycin + + -
Methanidophos + + +
Triazophos + + +
(Wu et al., 2019)
Effect of pesticides on reproduction of rice planthoppers
A plus sign (+) represents stimulation, a minus sign (−) represents suppression of reproduction
& a multiplication sign (×) represents unclear results

23. Aim of studies:
 The present study was to examine the pesticides that stimulate the
reproduction of BPH, WBPH and SBPH.
 The avoid resurgence occurrence of these three planthopper species.
Case study-II

24. Materials & Method
Rice variety, insect and pesticides
 The rice vareity Ningjig was used.
 Laboratory strains of BPH, WBPH and SBPH.
 Pesticides triazophos (TZP) & jinggangmycin (JGM) were used.
Experiment
 300 third-instar nymphs were released onto the rice plants at the tillering stage and
sprayed with 40 ppm TZP and 200 ppm JGM & maintain control plant.
 The nymphs were allowed to develop to the final fifth-instar stage on the treated and
collected then placed into glass jars with untreated rice plants.
 The development of the nymphs was recorded until adults emerged.
 After the emergence of adults from the same replicate (pot), one female and one
male adult were placed in a glass cup for egg-laying.

25. Finding of study
In figure showed that TZP and JGM significantly stimulated the fecundity of BPH,
WBPH & SBPH females.
The two pesticides showed that the fecundity treated with TZP was
significantly higher than that with JGM.
Effects of TZP and JGM on the number of eggs laid per female by three
planthopper species

26. Planthoppers reproduction associated factors
 Physiological and biochemical effects of pesticides on
Planthopper reproduction
 Flight muscle
 Analysis of gene functions
 Thermotolerance

27. Physiological and biochemical effects of pesticides on
planthopper reproduction
 JH titers in insects body are regulated by: JH production in corpora
allata and amount of JH esterase.
 Triazophos, deltamethrin & jinggangmycin treatments led to increased
(45–50%) circulating JH-III titers in BPH females over 1–3 days post-
emergence (PE).
 The increased hormone titers are due to reduced levels of active JH
esterase during the first three days PE. (Xu et al., 2016)

28.  Imidacloprid, triazophos, and deltamethrin treatments led to increased
protein contents, particularly vitellogenin, in BPH ovary and fat body.
 Foliar spray and topical application of triazophos and jinggangmycin
foliar spray significantly increased fat body and ovarian protein levels.
 Amounts of unfractionated lipids, fatty acids & soluble sugar
were higher in adults that developed from nymphs treated with
various concentrations of deltamethrin, triazophos, and
imidacloprid.
(Hu et al., 2010; Zhu et al., 2014)

29. Flight muscle associated with pesticide induced BPH
reproduction
 Planthopper migratory capacity and distance are closely related to resurgence.
 Transmission electron microscope (TEM) studies shows that the diameters of
female muscle myofibrils are larger at day one (by 31%) and two (by 21%)
post emergence following triazophos treatment.
 Similarly, sarcomere lengths and mitochondrial volumes were larger when
treated with triazophos.
 Triazophos, imidacloprid, and deltamethrin treatments led to enhanced flight
speed and distance.
 We infer that exposure to some insecticides can increase overall migratory
potential.
(Wan et al., 2013)

30. Aim of study:
 To understand the cause of triazophos induced enhancements in the flight capacity of BPH.
 The implications of this work for BPH management.
Materials & Method:
 Rice variety: Huaidao 9, Insects: BPH and insecticide: Triazophos
 Transmission electron microscopy (TEM) observations.
Case study-III

31. Finding of study
Fig: Changes in the myofibrillar diameter of N.
lugens adults after triazophos treatment
compared to untreated control (CK)
The data shown in figure
indicated the treated with 40
ppm of triazophos, the Diameter
of cross section myofibrillar
(DCM) at one and two DAE
were significantly greater than
those of the untreated control.

32. Finding of study
 The data showed that the
triazophos treatment
significantly increased the
sarcomere length at two and
three DAE greater than those
of the control.
 The percentage of
mitochondrial volume in the
muscle fibres at one and two
DAE was greater than that of
the control.
Changes in the sarcomere length of N. lugens adults
after TZP treatment
The percentage of mitochondria volume in the
muscle fibre of adult N.lugens.

33. Analysis of Gene Functions
 Hydroxysteriod dehydrogenase-like protein 2 and long chain fatty
acid coenzyme A ligase act in the carbendazim and triazophos-
induced SBPH reproductive increases. (Zhang et al., 2018)
 Fatty acid synthase (FAS), adipose triglyceride lipase, acetyl-CoA
carboxylase (ACC), and EST-1 participate in jinggangmycin-
induced stimulation of BPH reproduction. (Jiang et al., 2017)
 Acyl-coenzyme A oxidase mediates triazophos-induced BPH
reproductive stimulation . (Liu et al., 2017)

34. Pesticides enhance accessory gland proteins
 Males transfer seminal fluids, which include sperm and accessory
gland protein (AGP) to females via mating & AGPs influence female
behaviors, including oviposition.
 Insecticide-treated males transferred more AGPs to females, where
they contribute to enhanced egg production.
 Treating third-instar BPH nymphs with 25 and 50 ppm triazophos &
deltamethrin led to roughly double the amounts of AGPs in the adult
males prior to mating (1 and 2 days PE).
(Wang et al., 2010)

35. Proteomic Analysis of male accessory gland
 TZP-treated unmated BPH males versus untreated unmated males & TZP-treated
unmated males versus treated mated males showed 16 differentially expressed
proteins in the treated males compared to their untreated counterparts, 10 increases
and 6 decreases.
 Act-5C Protein, which acts in flight muscle isoforms, sperm individualization, and
mushroom body development, was upregulated 19-fold.
 Spermatogenesis associated protein 5 and testis development protein NYD-SP6
were upregulated 3.1 and 5.5-fold, respectively.
 These proteins are involved in spermatogenesis, & they enhancing male
contributions to BPH reproduction & increased fecundity.
(Ge et al., 2011)

36. Aim of the Study:
 The present investigation was to examine the effects of sub-lethal
doses of insecticides on protein contents in the male accessory glands
of N. lugens.
 The stimulating effect of insecticide treated males on the fecundity of
the females via mating.
Case study-IV

37. Materials and Methods
Rice variety, insects and insecticides
 The rice variety Shengyou 1 and laboratory strain of BPH were used in the
trials.
 Two insecticides were used in the trials: the pyrethroid 2.5% deltamethrin
EC and the organophosphate 20% triazophos.
Experiments
 After adult emergence, males and females were separated, with 20 males per
replicate used to measure total protein content in male accessory glands.
 Tested four mating treatments: Pair 1 consisted (♂ck × ♀ck), Pair 2 (♂ck ×
♀t), Pair 3 (♂t × ♀ck), and Pair 4 (♂t × ♀t).

38. Finding of study
Table: Protein contents from before and after mating
Triazophos, the highest levels of protein contents were found for both
treatment concentrations before mating.
For deltamethrin, the highest rate of protein was found with the high dose
before mating.
 Here the untreated control had a increase in the amount of protein after
mating, compared to before mating.

39. Effect of triazophos treated males on the fecundity of females via mating
The fecundity of the females after the mating (♂t × ♀t) of treated
males and females was significantly higher.
 As well as treated male mating with untreated female (♂t × ♀ck),
significantly stimulated the fecundity compare to after the mating (♂ck
× ♀t), of untreated males with treated females.
Finding of the study

40. Case study-V
Aim of study:
 To assess the influence of some insecticides being used for
management of rice insect pests on growth and reproduction of brown
planthopper infesting rice.

41. Materials and Methods
Test insect and insecticides
 BPH, was reared on the one month old potted plants of the susceptible rice
variety TN1.
 Planthopper susceptible rice variety, Swarna (MTU7029) was used as test
variety in the experimentation.
 Insecticides viz., chlorpyriphos, profenophos, cypermethrin, deltamethrin,
bifenthrin, lambda cyhalothrin and imidacloprid.
Tested biological parameters of BPH
 Nymphal duration
 Nymphal survival (%)
 Growth index (%)
 Fecundity
 Sex ratio

42. Experimental setup for
reproductive rate (fecundity)
of BPH (A)
A
Experimental setup for
nymphal duration, survival,
growth index and sex ratio of
BPH (B)
B

43. Insecticides significantly influenced reproductive rate of N. lugens adults
when they were allowed to feed and oviposit on the treated plants.
Highest reproductive rate of BPH was observed on bifenthrin and
cypermethrin treated plants with 227.67 and 218.33 nymphs emergence per
two pairs of adult hoppers, respectively.
Finding of study

44. Nymphal duration was not significantly influenced when freshly hatched nymphs of
N. lugens were allowed to feed and develop on insecticide-treated rice plants.
Survival of BPH nymphs on both tested doses of chlorpyriphos & cypermethrin
deltamethrin, bifenthrin and lambda cyhalothrin treated plants was significantly greater
than that of the control.
Growth index & sex ratio were revealed that insecticide applied to rice plants
significantly differ from the control.

45. Conclusions
 Balance should be established between the chemical controls and
biological controls against rice planthoppers, because many
insecticides showed high toxicities against natural enemies.
 We mention above that JGM & carbendazm (CBM) application to
control rice disease should be avoided in the presence of BPH
populations because JGM & CBM stimulates BPH reproduction.
 Triazophos, deltamethrin, bifenthrin, cypermethrin application,
enhances reproduction of planthopper species & also kills natural
enemies or reduces their biological control efficacy.

46. Cont…
 Triazophos, imidacloprid, and deltamethrin treatments led to
enhanced flight speed, distance and male accessory gland
proteins.
 Resurgent populations are influenced by interactions of
insecticides with other factors, such as rice variety and timing
and dosage of fertilization.

47. Prospective Research Directions
 Further research should be carried out on the physiological and
molecular mechanisms.
 The results of such work needs to be incorporated into
resurgence models that link molecular mechanisms to
ecological effects.
 Continued research into planthoppers biology is needed.
 How the mixtures of insecticide and fungicide influence the
planthopper resurgence behaviour further can be exploited.