Larvicidal effect of Pongamia pinnata plant extracts against Papilio demoleus Linnaeus (Insecta: Lepidoptera: Papilionidae)

Abstract

Larvae of the citrus butterfly, Papilio demoleus are serious pests in citrus orchards. Since synthetic pesticides have several ill effects on human health and the ecosystem, biopesticides are feasible alternative to synthetic pesticides. Indian beech tree, Pongamia pinnata plant extracts are well known for their medicinal and pesticidal properties. So, a study was carried out to evaluate P. pinnata plant's aqueous leaf and seed extracts, and seed oil nanoemulsion at 25, 50, 100, 200, and 400 PPM concentrations against the 4 th instar larvae of P. demoleus. All three test compounds showed concentration-dependent larvicidal activity. Comparatively, leaf extracts showed better larvicidal activity than seed extracts and nanoemulsion of the seed oil. The highest mortality was observed with leaf, seed extracts, and seed oil emulsions at 82.61%, 78.26%, and 73.91% respectively, at 400 PPM concentration. LC 50 and LC 90 values were lowest for leaf extracts (57.97 and 855.93 PPM), while the highest for seed oil nanoemulsion (107.09 and 1947.90 PPM). This is the first report of the efficacy P. pinnata leaf and seed extracts and seed oil nano emulsions against 4 th instar larvae of P. demoleus.

Full text

Research Article
Volume 37 No. 2 (June) 2023
Society for Biocontrol Advancement
(Copyright 2000 SBA)
Xanthopimpla spp. on Sesamia inferens pupa–X. avolineata: A) 4th instar, B) pupa, C) adult emerged
from host pupa; X. stemmator: D) 4th instar, E) pupa, F) adult emerged from host pupa…………….95
Journal of Biological Control, 37(2): 113-122, 2023, DOI: 10.18311/jbc/2023/32497
ABSTRACT: Larvae of the citrus buttery, Papilio demoleus are serious pests in citrus orchards. Since synthetic pesticides have several ill
eects on human health and the ecosystem, biopesticides are feasible alternative to synthetic pesticides. Indian beech tree, Pongamia pinnata
plant extracts are well known for their medicinal and pesticidal properties. So, a study was carried out to evaluate P. pinnata plant’s aqueous
leaf and seed extracts, and seed oil nanoemulsion at 25, 50, 100, 200, and 400 PPM concentrations against the 4th instar larvae of P. demoleus.
All three test compounds showed concentration-dependent larvicidal activity. Comparatively, leaf extracts showed better larvicidal activity
than seed extracts and nanoemulsion of the seed oil. The highest mortality was observed with leaf, seed extracts, and seed oil emulsions at
82.61%, 78.26%, and 73.91% respectively, at 400 PPM concentration. LC50 and LC90 values were lowest for leaf extracts (57.97 and 855.93
PPM), while the highest for seed oil nanoemulsion (107.09 and 1947.90 PPM). This is the rst report of the ecacy P. pinnata leaf and seed
extracts and seed oil nano emulsions against 4th instar larvae of P. demoleus.
KEYWORDS: Biopesticides, citrus buttery larvae, Pongamia seed oil nanoemulsion, Pongamia seed extract
(Article chronicle: Received: 20-01-2023; Revised: 11-04-2023; Accepted: 14-04-2023)
Larvicidal effect of Pongamia pinnata plant extracts against Papilio demoleus Linnaeus
(Insecta: Lepidoptera: Papilionidae)
MAHESH LINGAKARI*, MADHAVI MADDALA and SRIKANTH BANDI
Department of Zoology, Osmania University, Hyderabad – 500007, Telangana, India
*Corresponding author E-mail: mahehslingakari@gmail.com
INTRODUCTION
India is the 2nd largest producer of fruits and vegetables
globally (NHB, 2020-21). In India, citrus (12.4 % of total
fruit production) is the third most important fruit crop after
banana and mango, which account for 32.6 % and 22.1 %
of total fruit production, respectively (NHB, 2017). Larvae
of the citrus buttery (Papilio demoleus) are voracious
feeders, with later instars being the most damaging stage.
Heavy infestation leads to the complete defoliation of citrus
orchards (Lewis, 2009).
Pesticides are the major component in controlling insect
pests of agricultural and health importance (Valbuena et al
2021). More than 1000 pesticides are in use worldwide in
controlling the insect pests. Approximately 2 million tonnes
of pesticides are utilized annually worldwide (Sharma et al.,
2019).
Indiscriminative use of pesticides has negative eects
such as environmental pollution, loss of biodiversity, and
human health issues ranging from nerve damage to cancers.
Indiscriminate usage of pesticides results in bioaccumulation.
Persistent Organic Pollutants (POPs) were identied in
penguins, sh, and invertebrates in Antarctica (Ko et al.,
2018; Morales et al., 2022) and in amphibians in South Africa
(Wolmarans et al., 2021). When an individual is exposed
to pesticides above the safe levels, it may lead to acute or
chronic poisoning which includes cancer and infertility,
and toxic residues in food, water, air and soil (Arivoli &
Tennyson, 2013). More than 650 species of insects and mites
have developed resistance to insecticides (Jayaraj, 2005). At
least 27 species of insects have been described as resistant
to Bacillus thuringiensis toxins (Siegwart et al., 2015).
Along with primary metabolites, plants produce many
types of secondary metabolites and use them in a variety
of ways. A lot of secondary metabolites such as Alkaloids,
Flavonoids, Terpenoids, Phenols, and Saponins which are
well known for their pesticidal properties. Hence, plants
may be regarded as natural pesticide factories. Plant species
that belong to Meliaceae, Rutaceae, Malvaceae, Asteraceae,
and Canellaceae families are a source of the most promising
secondary metabolites (Dimetri, 2014). Biopesticides are
natural substances that have pesticidal properties and are
produced by plants, fungi, and other microorganisms.
Antifeedants and insecticidal toxicants can play a signicant
role as part of integrated pest management (Isman, 2002).
113

Larvicidal eect of Pongamia pinnata plant extracts against Papilio demoleus
114
Using plant oils as insecticides reduces the risks to the
environment and non-target organisms as they are volatile
in nature and have minimum residual activity (Koul, 2016).
A 20% Jatropha curcas (physic nut) seed oil exhibited
59.2% larvicidal activity against the third nymphal instar
of the desert locust, S. gregaria after 7 days of application
(Bashir & El Shae, 2013). Garlic and Lemon essential oils
are ecient larvicides against Spodoptera littorals with LC50
values of 19.95% and 24.20% and LC90 value of 39.18%
and 47.04% (Ali et al., 2017). Pontianak citrus peel oil was
a good larvicide with 76.25% mortality and LC50 value was
4% against the larvae of S. litura (Widjayanti et al., 2018).
Essential oils of Satureja khuzistanica Jamzad LC50 value was
23.36 and 167.96 PPM against the 4th instar larvae and adults
of Leptinotarsa decemlineata (Say), respectively (Saroukolai
et al., 2014). Pongamia pinnata seed oil has antimicrobial
(Kesari & Rangan, 2010), and low toxicity to human cervical
cancer cells (Raghav et al., 2019) properties. Even though
P. pinnata plant extracts and seed oils are proven to possess
larvicidal properties against a variety of insect pests, they
have not been tried against P. demoleus larvae. Hence, the
present study intended to test the larvicidal ecacy of the
P. pinnata plant extracts and seed oils against the 4th instar
larvae of P. demoleus.
MATERIALS AND METHODS
Test insect culture: Eggs and early larval instars of
P. demoleus were collected from sweet orange (Citrus
sinensis) plantations located in P. A. Pally village of the
Nalgonda district of Telangana State, India. After bringing it
to the laboratory, the eggs were washed with 0.02% sodium
hypochlorite, dried, and allowed to hatch. The collected
early instar larvae and newly hatched larvae were reared on
C. sinensis leaves under 25± 2°C temperature, 5–11 hours
of light-dark photoperiod, and 75±5% relative humidity
conditions. The third, fourth, and fth instar larvae were used
for the bioassays.
Extraction of test compounds
Pongamia (Millettia) pinnata, commonly known as
the Indian beech tree, belongs to the family Fabaceae. The
healthy seeds and leaves of the P. pinnata were collected
from the Osmania University campus, Hyderabad, Telangana
State, India. Collected seeds and leaves were washed with
running tap water rst to remove the dirt. Later, they were
washed with distilled water and shade dried for 15 days.
Later, they were used for preparing aqueous extracts and oil
extraction. 100 gms of dried seeds and leaves were ground
in an electrical blender, mixed with 200 ml of distilled water
and boiled for two hours at 60°C. later the extracts were
collected by ltering with Whatman lter paper No.1. Oil
was extracted from the dried seeds by cold pressing method.
The collected oil and aqueous seed extracts were stored in the
refrigerator until usage.
Preparation of test solutions
Dierent concentrations (400, 200, 100, 50, and 25
PPM) of P. pinnata Aqueous Leaf Extracts (PALE), P. pinnata
Aqueous Seed Extracts (PASE), and P. pinnata Aqueous
Seed Oil nanoemulsion (Pp-SONE) were prepared from
the extracted oil and aqueous seed extract by adding Tween
80 and distilled water in appropriate quantities. To prepare
homogeneous PALE, PASE, and Pp-SONE solutions, the
mixtures were placed on a Magnetic stirrer for 1 hr, and later
they were ultrasonicated for 10 mins.
GC-MS Analysis
PALE, PASE, and Pp-SONE compounds were subjected
to GC-MS analysis on GC-MS -QP2010 PLUS (Shimadzu,
Japan) with Turbo Mass. Compounds were separated on
a capillary column (DBS MS column of 0.25 x 30 x 0.25
mm). The oven temperature was programmed with the initial
isothermal temp. of 50°C and then increased up to 280°C at
the rate of 10°C per min and nally hold for 15 min. 1 uL
sample was injected by keeping the injection port at 250°C.
Mass detection was done via an electro-ionization source set
at 220°C. Helium gas of 99.999% purity was used as carrier
gas at a 1 ml. min ow rate. The molecular weight range was
set at 22 to 620 amu. Molecular weight, Molecular ion peak,
fragmentation pattern, and the number of hits were used to
identify the names of compounds by comparison with the
NIST library.
FTIR analysis
FTIR spectroscopy analysis of the PALE, PASE, and
Pp-SONE samples was carried out on Bruker – Tensor-
IR 27 system. identify the potential biomolecules in the
PMLE responsible for the reduction and also the capping
reagent responsible for the stability of the bio-reduced silver
nanoparticles. FTIR spectrum was recorded at a resolution of
4 cm-1, in the wave numbers range 500-4000cm-1.
Zeta potential
The Pp-SONE sample was subjected to the Dynamic
Light Scattering (DLS) analysis on Malvern Zetasizer nano
ZS90, UK instrument to know the size dimension and surface
charge of the test compound.
Larvicidal bioassay
Larvicidal bioassays were conducted in the Entomology
laboratory of the Department of Zoology, Osmania university
from July 2022 to November 2022. Clean plastic jars were
used for conducting bioassays. The leaf spray method was
followed. Fresh C. sinensis leaves were sprayed with the

LINGAKARI et al.
115
prepared test solutions separately. Control leaves were
sprayed with distilled water and Tween 80 mixture. After
drying the leaves, 5 fourth instar larvae of the same size were
introduced into each plastic jar. The insects were allowed to
feed on the treated leaves for 24 hrs. Thereafter untreated
fresh leaves were provided to all the larvae till treated larvae
survive or control larvae pupate. Wet tissue papers were
placed in each petri dish to avoid early drying of the leaf discs.
The experiment was replicated ve times. Observations were
recorded, and the per cent of larval mortality was calculated
and corrected by Abbott’s (1925) formula.
Corrected Mortality (%) = % MT - % MC / 100 - % MC *100
where, %MT = % larval mortality in treatment.
%MC = % larval mortality in control.
Obtained data were subjected to probit analysis by using
SPSS software. The results were expressed as Mean ± SD.
The level of signicance was set at p<0.05.
RESULTS
Larvicidal bioassay
The results of the PALE, PASE, and Pp-SONE
larvicidal bioassay and Probit analysis are given in Table
1. Concentration-dependent ecacy was observed in all
three test compounds. Percent mortality values ranged from
30.43% at 25 PPM to 82.61% at 400 PPM for PALE. These
values ranged between 26.09% to 78.26% for PASE and
21.74% to 73.91% for Pp-SONE at the same concentrations.
LC50 values were calculated to be 57.97 PPM, 80.77 PPM,
and 107.09 PPM, while LC90 Values were found to be 855.93
PPM, 1172.7 PPM, and 1947.9 PPM for PALE, PASE, and Pp-
SONE respectively. Obtained data were subjected to probit
analysis using SPSS software. As per the probit transformed
results (Figure 4), the obtained results were signicant with
reference to the expected results.
GC-MS analysis
GC-MS chromatograms of the PALE, PASE, and
Pp-SONE samples are given in Figure 1. The bioactive
compounds were recognized based on their relative peak
retention time and peak area percentages with the help of
the National Institute of Standards and Technology (NIST)
library. The results revealed that Cholesta-4,6-diene-3-one,
Glycine-N-pentadecauorooctananoyl-hexadecyl ester,
Naphthalene-1,2,3,4-tetrahydro-1-phenyl, and 1-Amino-4-
bromoanthraquinone-2-carboxaldehyde are the bioactive
compounds present in the PALE sample. PASE sample was
identied to possess n-heptadecanol-1, Friedelan-3-one,
Decanoic acid, Undulatin, and 2,3-bis (trimethylsiloxy)
propyl as the principal bioactive compounds, while the Pp-
SONE sample consists of 3.5-Hexadien-2-one, 5-methyl-
6-(4-nitrophenyl), Crepidine, Integerrimine, and Trans-
chalcone.
FTIR Analysis
The results of the FTIR analysis to determine the
functional groups of the tested phytochemicals are as
follows. Figure 2 shows the FTIR spectra of PALE, PASE,
and Pp-SONE in the 500 – 4000 cm-1. The medium peaks
in the PALE spectra (Figure 2A) at 3354 cm-1 indicate N-H
stretch and 1639 cm-1 C=O stretch. Both peaks conrm the
presence of Aromatic amino acids with free amino groups.
The peaks at 3371 cm-1 and 1618 cm-1 in the FTIR
spectrum of PASE (Figure 2B) are due to the O-H and C=C
stretching, indicating the presence of the CF3 group of
organic halogen compounds. The peaks at 1226 cm-1 also
conrm the presence of Organic halogen compounds at 1639
cm-1 peak is due to unsaturated hydrocarbons.
FTIR spectrum of Pp-SONE (Figure 2C) has C-H
bending at 1458 and 1372 cm-1 conrming the CH3 group
and N-Methyl Amino, Tertiary, Aliphatic Amines. The peaks
at 1711 cm-1 and 1744 cm-1 have C=O stretch indicating
Aliphatic amino or Carbonyl compounds. C-H stretch at 3007
cm-1, which is possibly due to aromatic nitro compounds. The
peaks at 2923 and 2855 cm-1 indicate the C-H stretch and may
be assigned to metal Carbonyl compounds and stained rings
or activated carbonyl compounds. The C-F stretch at 1164
cm-1 is assigned to uorine compounds.
Zeta potential
Dynamic Light Scattering (DLS) results (Figure 3)
showed that the size distribution of the prepared Pp-SONE
particles ranged from 134.16 nm to 402.44 nm (Figure 3A)
with an average particle size of 260.9 nm with a Polydispersity
Index value (PDI) of 0.342. The surface charge of the Pp-
SONE particles was found to be -54.7 mV (Figure 3B). The
negative charge of the Pp-SONE particles conrms the high
stability of the Nanoemulsion synthesized.

Larvicidal eect of Pongamia pinnata plant extracts against Papilio demoleus
116
Figure 1. GCMS. A) PALE, B) PASE, AND C) Pp-SONE.

LINGAKARI et al.
117
Figure 2. FTIR Chromatograms. A) PALE B) PASE C) Pp-SONE.

Larvicidal eect of Pongamia pinnata plant extracts against Papilio demoleus
118
Figure 3. Pp-SONE DLS analysis A) Particle size, B) zeta potential.
Table 1. Larvicidal bioassay results of PALE, PASE, and Pp-ZnONPs
Conc. PPM % Mortality LC50 LCL -
UCL LC90 LCL - UCL Stndrd
Error R2χ2 Value
PALE
Control 0
57.97 25.81 -
94.18 855.933 363.64 -
9822.93 0.573 0.983 0.282
25 30.43
50 43.48
100 52.17
200 69.57
400 82.61
PASE
Control 0
80.77 43.31 -
134.00 1172.7 464.99 -
15990.82 0.572 0.966 0.579
25 26.09
50 34.78
100 43.48
200 65.22
400 78.26
PP-
SONE
Control 0
107.09 61.26 -
196.64 1947.9 605.99 -
41994.41 0.593 0.969 0.481
25 21.74
50 30.43
100 39.13
200 56.52
400 73.91

LINGAKARI et al.
119
Figure 4. Probit transformed response graphs of the test compounds. A) PALE, B) PASE, and C) Pp-SONE.
DISCUSSION
The origin of terrestrial vascular plants and large-
scale speciation of arthropods occurred at the same time
during the Mid-Ordovician period, about 450 million
years ago (Bateman et al., 1998), (Ehrlich and Raven,
1964). Many plants have started synthesizing and storing
secondary metabolites, such as alkaloids, avonoids,
terpenoids, phenols, etc., that have biopesticidal properties
as evolutionary adaptation (Fritz & Simms, 1992; Panda &
Khush, 1995). The GC-MS analysis of the test compounds
conrmed several secondary metabolites such as Cholesta-
4,6-diene-3-one, Glycine-N-pentadecauorooctananoyl-
hexadecyl ester, Naphthalene-1,2,3,4-tetrahydro-1-phenyl,
and 1-Amino-4-bromoanthraquinone-2-carboxaldehyde in
PALE, n-heptadecanol-1, Friedelan-3-one, Decanoic acid,
Undulatin, and 2,3-bis (trimethylsiloxy) propyl in PASE, and
3.5-Hexadien-2-one, 5-methyl-6-(4-nitrophenyl), Crepidine,
Integerrimine, and Trans-chalcone in Pp-SONE.

Larvicidal eect of Pongamia pinnata plant extracts against Papilio demoleus
120
Almost all parts of the P. pinnata plant are used to cure
various diseases like tumors, piles, skin diseases, ulcers,
diarrhea, etc. (Shoba and Thomas, 2001). Pongamia pinnata
seed extract prevented oviposition of greenhouse whitey,
Trialeurodes vaporariorum on Chrysanthemum plant
(Pavela and Herda, 2007). Pongamia pinnata oil showed
a good larvicidal eect against the larvae of the thrips,
Frankliniella occidentalis (Stepanycheva et al., 2020) and
against Helicoverpa armigera (Lakshmanan et al., 2017).
Pongam oil and neem oil combination was a good ovicide
against Helicoverpa armigera Hubner and Spodoptera
litura Fabricius (Packiam et al., 2012). Karanja extracts are
eective in controlling stored grain pests, agricultural pests,
and pests of human health importance (Kumar & Singh,
2002). P. pinnata leaf extracts were eective against cassava
pink mealybug, Phenacoccus manihoti (Tran et al., 2022).
In the current study, the results of the larvicidal bioassay
of PALE, PASE, and Pp-SONE given in Figure 5. PALE
showed 82.61 % mortality at 400 PPM and 52.17 % mortality
Figure 5. Larvicidal bioassay results. A) Bar graph, B) Line graph of % mortalities and C) LC50 and LC90 values of test compounds.

LINGAKARI et al.
121
at 100 PPM Concentration. At the same concentrations, PASE
showed 78.26 % and 43.48 % mortalities only, whereas Pp-
SONE showed much less eectiveness with 73.91% and
39.13 % mortalities, respectively. LC50 and LC 90 values
were 57.97 PPM and 855.93 PPM for PALE, 80.77 PPM and
1172.70 PPM for PASE. However, these values were 107.09
PPM and 1947.90 PPM for Pp-SONE. Even though, PALE
performed better than the remaining two test compounds
comparatively, PASE and Pp-SONE also exhibited signicant
results.
CONCLUSION
The present study results conrmed the ecacy of
PALE, PASE, and Pp-SONE against the fourth instar larvae
of P. demoleus. Several secondary phytochemicals were
identied in the GC-MS analysis of the tested phytochemicals.
Further studies are required to know which of the identied
compounds are responsible for the larvicidal ecacy.
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