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Main plant volatiles as stored grain pest management approach: A review

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 Journal of Agriculture and Food Research 4 (2021) 100127

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Journal of Agriculture and Food Research

journal homepage: www.journals.elsevier.com/journal-of-agriculture-and-food-research/

Main plant volatiles as stored grain pest management approach: A review

Kabrambam Dasanta Singh a, c, Adesina Jacob Mobolade a, b, Rupjyoti Bharali c,
Dinabandhu Sahoo a, Yallappa Rajashekar a, *
a
Insect Bioresource Laboratory, Animal Bioresources Programme, Institute of Bioresources and Sustainable Development, Department of Biotechnology, Govt. of India,
Takyelpat, Imphal, 795001, Manipur, India
b
Department of Crop, Soil, and Pest Management Technology, Rufus Giwa Polytechnic, P. M. B, 1019, Owo, Ondo State, Nigeria
c
Department of Biotechnology, Gauhati University, Guwahati, 781014, Assam, India

A R T I C L E I N F O A B S T R A C T

Keywords: Insect pests inflict severe damage to stored food grains in many parts of the world. Though effective and reliable,
Plant volatile organic compounds (PVOC) several discouraging aspects of synthetic pesticides such as high cost, non-biodegradability, and the harmful ef-
Stored product insects fects on humans and the environment have urged agriculturist to look for an alternative approach that is
Pest control
powerful, eco-friendly, and economically viable. Plant volatile organic compounds are known to possess insec-
Eco-friendly
ticidal properties. They may be advocated for alternatives to synthetic insecticides. This review focused on how
Biopesticides
plant volatile organic compounds can be used as botanicals pesticides, which could reduce the application of
synthetic insecticides in stored grain pest's management. The review discussed key challenges for product
commercialization for instance i) availability of natural resources, ii) maintaining quality, iii) simplification of the
legislation. The review also highlights the importance of having clear objectives in the biopesticides research.
While a dedicated regulatory framework exclusively for biopesticides manufacturing could help in expanding its
use.

1. Introduction
The current human population of our planet is approximately 7.6
billion and, the number is projected to reach approximately 8.6 billion in
2030, and 9.8 billion in 2050 [1]. Food and Agriculture Organization
(FAO) predicted that the world may face a huge scarcity of food if the
total world food production is not increased by 70% by the year 2050 [2].
Even though, the available land resources could be enough to feed the
future world population, FAO however cautioned that majority of this
potential land is suitable for growing only a few crops, not necessarily the
crops with highest demand and it is concentrated in a few countries [2].
Food grains and pulses constitute most consumed and the most common
stored food products in the world, especially in the tropical and
sub-tropical regions, hence occupying a crucial position in the resolution
of food insecurity problems. Unfortunately, more than 70% of the pro-
duced grains are stored in villages in traditional structures such as
earthen pots, silos, gunny bags, steel drums, and baskets [3]. This often
leads to loss of food grains and pulses, particularly in less developed
countries where the need is the greatest [4]. There are various factors
which cause postharvest losses of food grains and pulses, and damage
inflicted by insects represents the highest threat. It has been reported that
there is a wide range of losses of approximately 5–30% of the world's
total agricultural production due to insect infestation alone on stored
food grains [5,6]. This wide variation in the estimation is partly due to
different geographical zones, different climatic conditions, also the
disparity in the major crops grown. There is also no concrete method to
accurately estimate the losses [5].
Insects can cause enormous damage to grains and pulses by directly
consuming the kernels or through the accretion of exuviae, webbing, and
cadavers. Accumulation of insect detritus may result in loss of food
commodities qualitatively as well as quantitatively, thereby making the
grain unfit for human consumption [6]. Insect infestation may change the
environment of the storage chamber which could provide favorable
conditions for invasive storage fungi that cause further losses [7]. Major
primary stored grain pests include rice weevil, Sitophilus oryzae (L.),
granary weevil, Sitophilus granarius (L.), (Coleoptera: Curculionidae),
lesser grain borer, Rhyzopertha dominica (F.), (Coleoptera: Bostrichidae),
Khapra beetle, Trogoderma granarium (Everts), (Coleoptera:

* Corresponding author. Institute of Bioresources and Sustainable Development, Department of Biotechnology, Govt. of India, Takyelpat Institutional Area, Imphal,
795001, Manipur, India.
E-mail address: yrajashekar.ibsd@nic.in (Y. Rajashekar).

https://doi.org/10.1016/j.jafr.2021.100127
Received 7 November 2019; Received in revised form 21 January 2021; Accepted 24 February 2021
2666-1543/© 2021 The Author(s). Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-
nc-nd/4.0/).
K.D. Singh et al.
Dermestidae), and the pulse beetle Callosobruchus chinensis (L.) (Cole-
optera: Bruchidae) [6]. There are also several secondary pests that inflict
damage to stored grain, such as Tribolium castaneum (Herbst), (Coleop-
tera: Tenebrionidae), rusty grain beetle, Cryptolestes ferrugineus (L.),
(Coleoptera: Cucujidae), saw toothed grain beetle, Oryzaephilus sur-
inamensis (L.), (Coleoptera: Silvanidae), mites, (Acarina: Tetranychidae)
Liposcelis corrodens, (Psocoptera: Liposcelidae) [6]. Improper storage
methods could lead to the loss of huge amount of food grains and pulses
throughout the world. Thus, farmers in anticipation of grain losses due to
pest infestation are forced to sell their produce early after harvest with
minimum monetary returns.
The objective of the current review was to identify the gaps in the
food storage system and propose an alternative approach for stored grain
pest management. The review briefly covered the different approaches of
stored grain pest management, considering both traditional and
chemical-based practices, emphasizing on the recent advancement in the
field. The varied mode of action and target site of plant volatiles organic
compounds (PVOCs) on insect's biological system has been discussed.
The review also explored the reasons for low adoption of plant volatiles
as favored approach.
2. Stored grain pest management approaches
2.1. Traditional practices
The struggle between mankind and his insect enemies has a history
even older than the early period of human civilization. Farmers have
always depended on several indigenous traditional knowledges to pro-
tect stored grain products from insect damage. Several crop-specific
storage techniques have been developed throughout the globe to retain
the quality and quantity aspects of the food until their consumption or it
is transported somewhere else. Farmers developed various conventional
structures for food grains storage using locally available raw materials
such as bamboo, straw, wooden plank, mud, bricks, cow dung, etc. [8].
The use of plant parts or plant extracts as natural insecticides was also
very much common. In fact, it was the introduction of nicotine, rotenone,
derris dust, and pyrethrum from Nicotiana tabacum (L) (Solanaceae),
Lonchocarpus spp. (Fabaceae), Derris elliptica (Wall.) Benth. (Fabaceae),
and Chrysanthemum cinerariaefolium (Asteraceae), respectively, in the
1850s, which led to the wide-scale use of plant extracts as insecticides
[9]. Pyrethrum, an insecticide based on pyrethrin extracted from the
flower heads of C. cinerariifolium [10] is very effective against several
insect pests, including moths and larvae. Therefore, it has been used
universally to protect stored grains and products from insect damage in
both temperate and tropical climates [11]. Several others plant extracts
and plant preparation have also been found to act against various insect
pests. In the year 1939, Paul Muller, a Swiss chemist, developed a new
compound that greatly changed the fate of farmers throughout the world.
The development of dichloro diphenyl trichloroethane (DDT) by Muller
marked the advent of a new synthetic pesticide era. DDT performed a
great role during World War II in which many diseases like typhus and
malaria carried by insects, took the lives of many soldiers and civilian.
2.2. Conventional practices of stored-grain pests control
The control of insect pests from damaging food grains in an effective
way has long been the task of postharvest technologies throughout the
world. With the advent of the chemical era, the use of synthetic in-
secticides was established as the most successful and reliable means of
controlling storage insects throughout the world [12]. Synthetic fumigants
are extensively and exclusively used in many developing countries as a
measure to effectively kill all the developmental stages of insect pests
within the storage facilities [6,13]. Methyl bromide and phosphine were
the chemical fumigants most used to protect stored grain pests all over the
globe. However, methyl bromide has proven detrimental to the strato-
spheric ozone layer and listed as an ozone-depleting compound in 1993
2
Journal of Agriculture and Food Research 4 (2021) 100127
and has since been phased out as per the Montreal Protocol [14]. It created
a paradigm shift in the magnitude of the used of phosphine, not just in
quantity but also extended its application to a variety of stored products
other than the food grains, such as spices, cocoa beans, dried fruit, nuts,
and even fresh fruits [15]. However, the adoption and implementation of
synthetic insecticides have been characterized by several shortcomings,
such as toxicity to humans and livestock, ozone depletion, toxicity to
non-target organisms, product adulteration, erratic supplies, and unavail-
ability at critical periods [15]. Pest resurgence and secondary pest out-
breaks are other major problems associated with synthetic pesticides.
Persistent use of such chemicals also leads to the emergence of resistant
strains of the targeted pests [16]. Development of resistance in target pests
against phosphine is one typical example [17]. Moreover, the cost of in-
secticides often puts a burden on the economic status of small-scale
farmers. There is an urgent need for an alternative approach that could
effectively scale down the use of chemical insecticides. In this regard, plant
volatile organic compounds have long been advocated as effective alter-
natives to synthetic chemical insecticides for pest management.
3. Plant volatile organic compounds (PVOC) as an alternative to
synthetic pesticides
Plants being one of nature's chemical producers provide several
bioactive organic chemicals whose major role in plants was found to be
defensive, especially against insect pests (Table 1) [12,18,19]. Those
organic bioactive compounds provide an odor that is typically volatile in
nature and hence termed as plant volatile organic compounds (PVOC).
Such compounds have been traditionally used by farmers all over the
world in the fight against stored grain pests. The dawn of synthetic in-
secticides, after the Second World War, has made a significant impact on
agriculture with farmers drifting away from these old traditions. How-
ever, considering the dangers associated along with the chemical in-
secticides, use of plant components with no or fewer threats forms the
most viable option for the effective control measures against the various
pests of tropical agricultural systems [12,20,21].
There are various plant species which embody a rich source of phy-
tochemicals that could be explored for use as insecticides [22]. The
secondary metabolites of plants were once considered to be waste
products. However, the important role played by them in the plant de-
fense mechanisms make them as one of the most interesting aspects of
crop protection [23]. In addition, they also act as attractant or repellent
in insect-pest management. Secondary metabolites are known to influ-
ence the growth and development, ecdysis, mating behavior, fertility,
and adult emergence of insect pests [24]. Numerous defensive chemicals
of plant origin have already been identified. Plant volatiles organic
compounds are generally much safer to human beings and to the envi-
ronment (Table 2). There is also less chance of developing resistance to
the different botanical pesticide by the insect pests since these botanical
pesticides possess a mixture of chemical components of a complex nature.
Hence, plant-derived molecules could thrive in the fight against
insecticide-resistant insect pests [25]. It is well documented that farmers,
especially in the developing countries like Asia, Africa, and other parts of
the world are using botanicals as a measure to protect stored grains from
bruchid infestation with varying degrees of success [26].
The secondary metabolites are often involved in plant defense
mechanism, but not directly involved in growth, development, or
reproduction of plant. Secondary metabolites include terpenoids, phe-
nolics and alkaloids [27] and these phytochemicals possess enormous
potential to act as biopesticides (Table 1). Over 2000 plant species boast
pesticidal properties against several stored grain pests [28]. Several au-
thors also set forth various plant products along with their efficacy
against the stored grain pests [29,30]. These plant-derived botanicals are
generally used in the form of aqueous/solvent extracts, powders, slurries,
volatiles and oils, or as shredded segments [6,21]. Hence, plant-derived
botanicals hold promise as an alternative to synthetic insecticides to
lessen the negative impact of the pesticide on the environment.
K.D. Singh et al. Journal of Agriculture and Food Research 4 (2021) 100127

Table 1
List of plant volatiles and their insecticidal activity.
Plant species Family Part of the Product Active principles Bioassay test Target Insect References
plant

Acorus calamus (L.) Acoraceae Rhizome extract β- Asarone Contact, S. zeamais [76]
Aloysia citriodora (Pal

au) Verbenaceae Leaves Essential citronellal and sabinene Repellent, T. castaneum, T. confusum [100]
oils fumigant, contact
A. polystachya (Pal

au) Verbenaceae Leaves Essential carvone and limonene Repellent T. castaneum, T. confusum [100]
oils
Artemisia annua (L.) Asteraceae Leaves Essential 1, 8-cineole Fumigant T. castaneum [101]
oils
Baccharis salicifolia (Ruiz Asteraceae Leaves Extract 3-Carene Contact, Repellent T. castaneum, S. zeamais [102]
& Pav.)
B. salicifolia Asteraceae Leaves Extract β-Pinene Contact, Fumigant T. castaneum, S. zeamais [73]
Brugmansia suaveolens Solanaceae Flowers Fractions – Oviposition Zabrotes subfasciatus [103]
(Willd.) deterent
Carum carvi (L.) Apiaceae Leaves Essential Carvone Contact R. dominica, S. oryzae, [104]
oils Limonene, (E)- Anethole S. zeamais
Chamaecyparis obtusa Cupressaceae Leaves Essential Bornyl acetate Contact fumigant S. oryzae, [105]
(Siebold & Zucc.) oils C. chinensis
Chenopodium ambrosioides Amaranthaceae Leaves Essential Hexadecane Contact T. castaneum, S. granarius [106,107]
(L.) oils
Cinnamomum aromaticum Lauraceae bark extract Cinnamaldehyde Contact T. castaneum, S. zeamais [108]
(Nees.) Fumigant
Antifeedant
Citrus Rutaceae Fruit peel Essential Limonene Eugenol Fumigant Contact T. castaneum, S. oryzae [109]
oils
Colocasia esculenta var. Araceae Rhizome Extracts 2, 3-Dimethylmaleic anhydride Fumigant S. oryzae, T. castaneum, C. [21]
esculenta (L.) Schott chinensis
Convolvulus arvensis (L.) Convolvulaceae Leaves Extracts Hexadecanoic acid Contact R. dominica, S. oryzae [110]
Conyza dioscordis (L.) Asteraceae Leaves Extracts Dicotlyhexanedioate Contact T. castaneum, S. granarius [106]
(Desf.)
Coriander sativum (L.) Apiaceae Seeds Essential Linalool Contact S. oryzae, R. dominica and [36]
oils C. pusillus
Cupressus lusitanica (Mill.) Cupressaceae Leaves Essential umbellulone and α-pinene Contact, Fumigant T. castaneum, A. obtectus, S. [33]
oils cerealella and S. zeamais
Duguetia lanceolata St.- Hil. Annonaceae Leaves Extract 2,4,5-trimethoxystyrene Oviposition Zabrotes subfasciatus [111]
deterent
Eucalyptus spp. Myrtaceae Leaves Essential α-Terpinene Fumigant S. oryzae [110]
oils 1, 8-Cineole
α -pinene
Eucalyptus saligna (Sm.) Myrtaceae Leaves Essential p-Cymene (Cymol) Contact, T. castaneum, S. oryzae [33]
oils Fumigant,
Repellent
Evodia ruticarpa (A. Juss.) Rutaceae Fruit Essential Triterpenes Fumigant, T. castaneum, S. zeamais [112]
T.G. Hartley oils Repellent
Feeding deterrent
Feoniculum vulgare (Mill.) Apiaceae Fruit Extract phenylpropenes (E)-anethole Contact S. oryzae, L. serricorne [35]
Estragole (þ)-Fenchone Fumigant
Juniperus foestidissima Cupressaceae Juvenile Essential Citronellol Fumigant T. granarium [113]
(Willd.) branches oils
Lantana camara (L.) Verbanaceae Leaves Extracts Coumaran Fumigant S. oryzae, T. castaneum, R. [29]
dominica
Melaleuca cajuputi Myrtaceae Leaves Essential Terpine-4-ol Terpiniolene Contact Fumigant T. castaneum, S. oryzae, E. [114,115]
(Powell) oils γ - Terpinene kuehniella, R. dominica
Mentha citrate (Ehrh.) Lamiaceae Aerial part Essential Carvone, Menthol, Linalool, Contact, Fumigant T. castaneum, C. maculatus [116]
oils Linalyl acetate
Nardostachys jatamansi Caprifoliaceae Roots Essential Aristolone Contact, Fumigant T. castaneum, S. oryzae [117]
(D.Don.) oils
Ocimum canum (Sims) Lamiaceae Dried leaves Essential Linalool Fumigant T. castaneum, S. granarius [118]
oils
Ocimum kilimandscharium Lamiaceae Fresh aerial Essential Camphor Contact S. oryzae [119]
(Gürke) part oils
Pimenta racemose (Mill.) Myrtaceae Leaves Essential Linalool Fumigant S. zeamais [120]
oils
Rosmarinus officinalis Lamiaceae Leaves Essential Camphor Fumigant S. oryzae [121]
(Spenn.) oils
Spent hops Flowers Extracts Xanthohumol Feedant deterent S. granarius L., T. confusum [122]
and T. granarium
Tagetes filifolia (Lag.) Asteraceae Aerial parts Essential (E)-anethole and estragole Fumigant T. castaneum [123]
oils
Thespesia populnea (L.) Malvaceae Leaves Extract Phenol Fumigant, Contact C. maculatus [124]
Zingiber officinale (Roscoe) Zingiberaceae Rhizome Essential 1, 8-cineole Repellent, T. castaneum, S. zeamais [125]
oils Fumigant
Z. officinale Zingiberaceae Rhizome Essential β-Zingiberene Antifeedant, IGR T. castaneum [120]
oils

IGR ¼ Insect Growth Regulator.

3
K.D. Singh et al. Journal of Agriculture and Food Research 4 (2021) 100127

Table 2 infesting stored grains (Fig. 1). Plants are known to produce diverse
Mammalian toxicity of some plant volatiles organic compounds. secondary phenolic compounds which could have played a major in
Active ingredient Route Animal Mammalian toxicity LD50 inflicting the contact toxicity and mortality effect to these stored grain
tested (mg/kg) insects [12,26,29,31]. Kim et al. [32] reported that the extract from the
Anethole Oral Rat 2090 Cinnamomum cassia (L.) (Lauraceae) bark and oil, Cocholeria aroracia (L.)
β-asarone Oral Rat 275 (Brassicaceae) oil, and Brassica juncea (L. Czern) (Brassicaceae) oil
Carvacrol Oral Rat 810 showed potent insecticidal activity against C. chinensis. Reports on the
1,8-Cineole Oral Rat 2480 bioassay-guided experiment of Mexican cypress, Cupressus lusitanica
Apiol Intravenous Dog 500
Anisaldehyde Oral Rat 1510
(Mill.) (Cupressaceae) and Sydney blue gum, Eucalyptus saligna (Sm.)
Trans-Anethole Oral Rat 2090 (Myrtaceae) also showed contact toxicity to adults of Sitotroga cereallela
(þ)Carvone Oral Rat 1640 (Olivier) (Gelechiidae), Acanthoscelides obtectus (Say) (Chrysomelidae),
Cinnamaldehyde Oral Guinea pigs 1160 Sitophilus zeamais (Motschulsky) (Coleoptera: Curculionidae) and
Citral Oral Rats 4960
T. castaneum [33]. The essential oils of C. lusitanica and E. saligna were
Cuminic Oral Rats 1390
aldehyde more effective against A. obtectus and S. cerealella with LC50 values of
Eugenol Oral Rats 2680 0.05–0.11% v/w in contact toxicity and 4.07–7.02 μl/L air in fumigation
Dillapiol Oral Rats 1000–1500 [33]. The dose dependent nature of contact toxicity was demonstrated by
3-Isothujone Sub-cutaneous Mice 442.2 Alpinia extract which shows significant increase in the toxicity with
D-Limonene Oral Rats 4600
Linalool Oral Rats 1000
increasing exposure dose against Lasioderma serricorne (Fabricius)
Maltol Oral Rats 2330 (Coleoptera: Ptinidae) adults [34]. Estragole, (E)-anethole and (þ)-fen-
Menthol Oral Rats 3180 chone are the Foeniculum fruit-derived constituents which are found to be
2-Methoxyphenol Oral Rats 725 toxic to S. oryzae adults by the direct contact application [35]. The
Methyl chavicol Oral Rats 1820
essential oil extracted from seeds of Coriander sativum (L.) (Apiaceae)
Methyl eugenol Oral Rats 1179
Myrcene Oral Rats 5000 contains linalool, which is found to be very active against stored rice
Pulegone Intraperitoneal Mice 150 pests viz; S. oryzae, R. dominica and Cryptolestes pusillus (Sch€ onherr)
ϒ-terpinene Oral Rats 1680 (Coleoptera: Laemophloeidae) [36]. The essential oils and its bioactive
Terpinen4-ol Oral Rats 4300 molecules from aerial part of Pelargonium hortorum (L.H. Bailey) (Ger-
Thujone Sub-cutaneous Mice 87.5
aniaceae) exhibited contact toxicity against Liposcelis bostrychophila
Thymol Oral Mice 1800
(Badonnel) (Psocoptera: Liposcelididae) and S. zeamais with LD50 values
Source [6]. 149.88 μg/cm2 and 14.41 μg/adult respectively [37]. Many compounds
were isolated from T. apollinea L., viz., Isoglabratephrin, (þ)-glabra-
3.1. Contact toxicity tephrin, tephroapollin-F and lanceolatin-A, which showed adulticidal
activity against S. oryzae, R. dominica and T. castaneum at concentrations
Plant products with potent insecticidal activity could be used for the of 0.875, 1.75 and 3.5 mg mL 1 [38] 100% contact toxicity was also
control of stored beetles. Many authors have reported that plant volatiles observed from the essential oils of Hyptis suaveolens (L.) Poit (Lamiaceae)
are toxic and effective in enhancing the mortality of adult beetles and Ageratum conyzoides (L.) (Asteraceae) against T. castaneum, at

Fig. 1. Molecular structure of plant volatile organic compounds with contact toxicity.

4
K.D. Singh et al.
250 ppm while Coleus aromaticus (Benth.) (Lamiaceae) at 350 ppm [39].
The essential oil of C. lusitanica contains compounds such as umbellulone
(18.38%) and α-pinene (9.97%) which showed contact toxicity with LC50
values of 0.05–0.11% v/w against T. castaneum, A. obtectus, S. cerealella
and S. zeamais [33]. Recent report suggested that, Perillaldehyde, a major
constituent in oil of Lippia javanica var. javanica (Burm. f.) Spreng (Ver-
benaceae), showed contact toxicity against S. zeamais. 100% mortality of
S. zeamais was observed after 48 h exposure to Perillaldehyde at con-
centration 10 mg/mL [40].
3.2. Fumigant toxicity
Fumigation is one of the methods in stored products pest management.
Fumigation is done for killing insects or to avoid further damage to
infested commodities. Fumigants are substances that vaporize at the
temperature above 5  C (Fig. 2). They act in gaseous or smoke form with
high penetration power and usually applied in an enclosure system. In the
vapor phase, plant volatile organic compounds can penetrate through the
insect's respiratory system and exhibit its toxic effect [41]. The fumigant
activity of plant products may be due to different functional groups
attached to these volatile chemicals which enable them to persist in a
closed environment for a longer time [42]. One of the advantages of bio-
fumigants is that it has the potential to provide a novel mode of action
against insects that could nullify the danger of cross-resistance as well as
offering a new lead for the design of target-specific molecules [29,43].
Hamdi et al. [44] reported the fumigant toxicity of the essential oils from
Tunisian and Algerian L. nobilis against Ephestia kuehniella (Zeller) (Lepi-
doptera: Pyralidae) (Mediterranean flour moth). Nenaah & Ibrahim [45]
reported the insecticidal activity of Pimpinella anisum (L.) (Apiaceae),
Cinnamomum camphora (L.) (Lauraceae) essential oils against T. granarium
and T. castaneum. The plant volatile coumaran molecule from Lantana
camara (L.) (Verbanaceae) showed grain protectant properties against
stored grain pests [29]. 2, 3-Dimethylmaleic anhydride is a plant volatile
organic compound from Colocasia esculenta var. esculenta (L.) Schott
(Araceae) that was toxic to various stored grain pests [21,46]. 1, 8 cineole
isolated from Artemisia annua (L.) (Asteraceae) showed potent fumigant
toxicity against adult T. castaneum [47]. The main components of the
essential oils of Chinese medicinal herb, Blumea balsamifera (L.) (Aster-
aceae) leaves were 1, 8-cineole, 4-terpineol and α-terpineol and it was
reported to show distinct fumigant toxicity against S. zeamais adults [48].
In a comparison study of twenty different plant-derived oils for their
acaricidal and insecticidal property, it was found that A. graveolens,
Achillea millefolium (L.) (Asreraceae) and Eucalyptus dives (Schauer) (Myr-
taceae) were toxic to S. oryzae and S. zeamais in the fumigant bioassay
Fig. 2. List of molecular structure of plant volatile organic compounds with fumigant activity.
5
Journal of Agriculture and Food Research 4 (2021) 100127
[49]. In another study, the fumigant activity of EOs from Zingiber officinale
(L.) (Zingiberaceae) and Mentha pulegium (L.) (Lamiaceae) was tested
against eggs, larvae and adults of Callosobruchus maculatus (Fabricius)
(Chrysomelidae). The LC50 value of EOs of Z. officinale was reported to be
1.151, 2.336 and 2.183 μl/l air for eggs, larvae and adults of C. maculatus
respectively. While it was 0.072, 0.113 and 0.093 μl/l air essential oil of
M. pulegium for eggs, larvae and adults of C. maculatus respectively [50].
4. Main mode of action of plant volatile organic compounds
Phytochemicals exhibit their effect on insects in several manners,
including toxicity, repellency, antifeedant or feeding deterrent, fumigant,
growth inhibitor, and suppression of reproductive behavior and reduc-
tion of fecundity and fertility [6]. Another important aspect of insect
control is to elucidate the mode of action of the natural insecticides as it
will provide rational information on the proper formulation (Fig. 3).
Plant volatile organic compounds from many plant extracts and essential
oils consist of alkanes, alcohols, aldehydes, and terpenoids, especially
monoterpenoids (Table 1) [28,29,51].
4.1. Growth and development regulators/inhibitors
Phytochemicals are known to affect growth, development, and
metamorphosis of insect. These cause irreversible changes in the physi-
ology and behavior of insect, such as reduction in weight of larvae, pupa,
and adult, as well as prolonged larval and pupal periods [52]. Several
plant volatiles with potential insect growth regulator and sterilant
characteristics have been assessed in this respect (Fig. 4). Various plant
extracts showed inhibition in percentage pupation upon larval treatment
[53]. Essential oil from Cymbopogon schoenanthus (Spreng.) (Poaceae)
showed inhibition of growth and development in all life stages of
C. maculatus [54]. Plant-derived botanicals were also found to inhibit the
development of eggs and immature stages inside grain kernels. Aqueous
extracts of common cocklebur Xanthium strumarium (L.) (Asteraceae) leaf
was also reported to show several insecticidal properties including
toxicity, repellency, inhibition of fecundity and adult emergence of the
insects, and grains protection against C. chinensis [55].
4.2. Hormone regulator
Several investigations have been carried out to screen various plant
extracts for their juvenilizing effect. Rani and Jamil [56] discovered that
plant extracts of water hyacinth contain a juvenile hormone analogue,
which causes abnormal moulting and metamorphosis of stored grains
K.D. Singh et al. Journal of Agriculture and Food Research 4 (2021) 100127

Fig. 3. Various molecular targets and mode of actions of insecticides.

Fig. 4. Chemical structure of phytochemicals showing hormone regulator, chemosterilant, oviposition suppression in stored grain insects.

insects. Their role in regulating the reproduction of insect is also well
studied [57] (Fig. 4). Lingampally et al. [58] reported that Solasodine at
concentration of 1 μg/μl could inhibit moulting and induced several
morphogenetic abnormalities which lead to the death of fifth instar
larvae of Tribolium confusum (Jacquelin du Val) (Tenebrionidae) during
moulting and could affect the percentage of adult emergence.
4.3. Oviposition deterrent
Oviposition deterrents are chemicals which prevent or avoid insect
from egg laying. Oviposition deterrents have huge potential to prevent
insect infestation and can offer the first line of defense against insect pest.
Plant volatiles are generally used as cues by ovipositing females for

6
K.D. Singh et al.
locating host plant or substrates [59,60]. Many experts have reported the
involvement of PVOC in part or completely preventing egg laying as well
as the emergence from the laid eggs on stored grains by different families
of insect pests [61–63]. 1, 8 cineole isolated from essential oils and their
volatile component of various plants within Lamiaceae family was found
to affect the oviposition rate of various insect [64]. Used of garlic oil as an
oviposition deterrent is also common [65]. The EOs of Eucalyptus citriodora
(Hook.) (Myrtaceae), Eucalyptus globulus (Labill.) (Myrtaceae) and Euca-
lyptus. Staigeriana (F.Muell. ex. F.M. Bailey) (Myrtaceae) have severe effect
on the oviposition, thereby reducing the viability of eggs and insect's
emergence of Zabrotes subfasciatus (Chrysomelidae) and C. maculatus [66].
Essential oils of other plants viz., Trachyspermum ammi (L.) (Apiaceae),
Anethum graveolens (L.) (Apiaceae) and, Nigella sativa (L.) (Ranunculaceae)
has shown to affect the oviposition potential and delays the developmental
period of T. castaneum [67]. It also caused deformities in insect meta-
morphosis. Laurus nobilis (L.) (Lauraceae) and Rosmarinus officinale (L.)
(Lamiaceae) are known to cause egg mortality [68]. In a study, the effect of
finely powdered and intact dried leaves of Ocimum canum Sims (Lam-
iaceae) on adults of Zabrotes subfasciatus (Roheman) in dried Pinto beans
were determined. It was reported that the finely powdered dried leaves
completely suppressed the oviposition at 2% W/W, with an EC50, of 0.45%
W/W. While there was no effect of intact dried leaves on the insect's
population [69]. In a similar report, powdered and intact dried leaves from
four locally grown plant species i.e. Chenopodium ambrosioides (L.)
(Amaranthaceae), Tagetes minuta L. (Asteraceae), Azadirachta indica A. Juss
(Meliaceae), C. lusitanica, applied at a rate of 1.5 kg per 100 kg beans
(Phaseolus vulgaris) against A. obtectus and Z. subfasciatus was compared
under laboratory conditions. C. ambrosioides was found to be the most
effective with 100% mortality of adult insects in less than three days and
no progeny. T. minuta applied as powder also increased mortality and
reduced oviposition and progeny production significantly. While A. indica
or C. lusitanica applied as powder or as whole leaves, had no significant
effects upon mortalities, oviposition rate, or progeny production compared
with control treatments [70].
4.4. Antifeedant
“Antifeedants” or “feeding deterrents” are the chemical substances that
disrupt the feeding behavior of insect by making the treated food
Fig. 5. Chemical structure of plant volatile organic compounds with antifeedant activity.
7
Journal of Agriculture and Food Research 4 (2021) 100127
unappealing or unpalatable [71]. Antifeedants can also induce cessation of
feeding either temporarily or permanently. The presence of certain
chemicals in plants prevents insects from feeding on them, thus leads to
starvation of the insects and, eventual mortality (Fig. 5). A very distinctive
feature of antifeedants is the way it inflicts effect on insects when in
contact with such substances. Antifeedant attempts to eliminate insects
without ever disturbing the ecological balance. Antifeedant don't kill the
target insect, rather it allows them to be available for their natural en-
emies. The deleterious effects could be activated to serve a novel role in the
management of stored grain insect pest. The identification of azadirachtin
and neem seed extracts, during 1970s and 1980s, as potent feeding
deterrent pave the way for natural antifeedant [10]. The essential oils from
Gaultheria procumbens (L.) (Ericaceae) showed potent antifeedant proper-
ties against Coleopteran insects S. oryzae and R. dominica [72]. The feeding
behavior of three stored grain insects, S. oryzae, R. dominica and
T. castaneum were reported to change significantly when flavanoids
compounds, Isoglabratephrin, (þ)-glabratephrin, tephroapollin-F and
lanceolatin-A (Fig. 4) isolated from Tephrosia apollinea (Delile), were
treated at different test concentrations of 0.65, 1.3 and 2.6 mg g– 1. The
relative growth rate and efficiency of conversion of ingested food were also
significantly reduced by all the treated insects [38].
4.5. Repellent activity
Repellents are chemical substances that protect plants or stored grain
products from insect's damage by rendering the stored grains as unat-
tractive, unpalatable or offensive to the infesting insect pests (Fig. 6).
PVOC mostly affect adult beetles causing them to flee from treated grains,
or not to invade it at all. The properties of repellency of plant volatiles
could have an important implication in the traditional postharvest stor-
age system. Generally, they are available locally and it makes them
further an attractive candidate in the management of stored-grain insect
pests. The α-terpineol, pulegol and germacrol volatile compounds iso-
lated from Baccharis salicifolia (Ruiz & Pav.) (Asteraceae) were revealed
that shows potent repellent properties against T. castaneum [73]. The
ar-turmerone isolated from Curcuma longa (L.) (Zingiberaceae) rhizomes
were reported to show effective repellent activity against S. zeamais [74].
Different solvent extracts (Hexane, chloroform, ethyl acetate) of three
widely grown plants Sphaeranthus indicus (L.) (Asteraceae), Tephrosia
K.D. Singh et al.
Fig. 6. List of chemical structure of plant volatile organic compounds with repellent activity.
purpurea (L.) pers. (Fabaceae) and Prosopis juliflora (Sw.) DC. (Fabaceae)
were reported to show repellent activity against T. castaneum. Repellent
activity of hexane extract of P. juliflora were reported with EPI value in
2.5% 0.11 and 0.33 at 1 h and 6 h respectively, while the EPI value of
chloroform extract of T. purpurea 2.5% at 6 h was 0.17. For S. indicus the
EPI value was 0.65 at 2.5% and 6 h [75]. (Z)-asarone is an active con-
stituent isolated from the enthanolic extract of Acorus calamus (L.)
(Acoraceae). This compound is reported to have strong repellency against
S. zeamais [76]. The repellent property of essential oils of Callistemon
lanceolatus (Sm.) Sweet (Myrtaceae) and Lippia alba (Mill.) N.E. Brown
(Verbenaceae) against C. chinensis is also well documented [77]. The
essential oils of aromatic plants are such as Cymbopogon fexuosus (pao-
ceae), C. winterianus (paoceae) and C. martini (paoceae) were also re-
ported to have strong repellent property against T. castaneum and were
significantly repellent at 1.41 μL/cm2 [78].
4.6. Ovicidal effects
Substance or agent that has the potential to kill eggs especially the
eggs of insects, mites etc. are considered to have ovicidal effect. Many
plants are known to possess the ovicidal property. This property of plants
is of great importance in the management of insect-pests at every stages
of their life cycle, thereby preventing the damage caused by other stages
[79]. Application of botanicals on eggs could tremendously reduce the
number of adult emergence which is probably due to either chemical
toxicity and/or physical properties, which cause changes in surface
tension within the egg similar to those of oils [80]. Salunke et al. [81]
revealed that flavonoids isolated from Calotropis procera (Ait.) R. Br.
(Apocynaceae) were toxic to eggs of C. chinensis with 100% progeny
suppression at 10 mg/mL concentration. The essential oils of Indian dill,
Anethum sowa (L.) (Apiaceae) were also reported to show ovicidal effect
on eggs of C. maculatus [82]. L-menthol is an active component, isolated
from the essential oil of Mentha arvensi L. (Lamiaceae), which has high
8
Journal of Agriculture and Food Research 4 (2021) 100127
ovicidal effect on eggs of T. castaneum [83]. The EOs of cardamom
(Elletaria cardamomum) L. (Zingiberaceae), Cinnamomum zeylanicum
Blume (Lauraceae), Sygium aromaticum L. Merrill. et. Perry) (Myrtaceae),
Eucalyptus spp. and Azadirectica indica A. juss (Meliaceae) were also
found to have ovicidal effect on the eggs of T. castaneum [84].
4.7. Chemosterilants
Chemosterilants are substances which deprive insects of their ability
to reproduce. Such substances produce irreversible sterility without
affecting their mating behavior or its life span but only prevent the
production of F1 progeny. In some cases, eggs may not be laid, fail to
hatch, larvae may not pupate, or the pupal development will be incom-
plete. Chemosterilants cause damage to the ovaries resulting in inhibition
of egg formation [77,85]. Thus, ovarian development is prevented, and it
leads to sterility. Chemosterilants has proven to be an important aspect of
integrated pest management programs as it reduces the occurrence of
pest-resistant [28]. Saxena et al. [86] found that asarone isolated from
the rhizomes of A. calamus possessed insect chemosterilant properties,
causing inhibition of insect's interstitial cell activity. The active principle,
1, 3, 7-trimethylxanthine isolate from seed extract of proved effective as
chemosterilant for C. chinensis [87].
4.8. Behavioral disturbance
Like other toxic compounds, plant derived insecticides may also
induce changes in the behavior of insects. They either stimulate or reduce
the insect's mobility or flight patterns, and even cause physiological al-
terations [88]. Naturally, insects will tend to move away from the
insecticide exposed area as soon as the presence of toxic compounds is
detected. Besides EOs are known to inhibit acetylcholiesterases enzyme
on insect's nervous system while also disrupting the GABAergic [89] and
aminergic transmissions [90]. However, essential oils when given in sub
K.D. Singh et al.
lethal dose on insects can contribute to the development of resistance
against traditional insecticides that could also compromise the manage-
ment strategy of insect-pests [91,92]. In an experiment, Haddi et al. [93]
investigated the toxicity and locomotory as well as respiration responses
induced by essential oils of clove and cinnamon on S. zeamais. It was
reported that S. zeamais populations gave stimulatory response in median
survival time when exposed to sublethal dose. The respiratory rates of
S. zeamais (i.e., CO2 production) were significantly reduced under low
concentrations of the essential oils.
5. Why low commercialization of products based on PVOCs
The insecticidal properties of several plants are being well recog-
nized. Many researchers are working in this subject, and there are also
several peer scientific publications and potential patents. Isman and
Grieneisen [94] analyzed over 20,000 research publications on botanical
insecticides from 1980 to 2012. Their analysis pointed towards many
flaws in the recent publication on botanical insecticides that compromise
the reproducibility of data and the strong basis for equitable comparison
with past and future studies. As a consequent, much of the scientific
literature on this filed are of limited use in the progress towards
commercialization or advancement of knowledge, given the resources
expended. The reasons could be due to (i) lack of clear idea in the in-
vestigator's objective of the research (ii) confinement of the experiment
only in the laboratory condition (iii) scarcity of the natural resources (iv)
lack of proper standardization and quality control (v) stringent legisla-
tions, etc. [94–96]. The above-mentioned issues need to be addressed at
first before we could see a significant rise in the percentage of
commercialization. For instance, investigator need to have a clear-cut
objective of their research, whether to focus on the use of crude or
semi refined plant extracts for resource poor farmers in developing
countries, or simply the isolation and characterization of bioactive
compounds for industrialized pesticides development [94]. Many of the
publications are based on the experimental data in laboratory condition.
Those data need to be consistent in the field trial. Besides, there must be
an assurance that the starting material (the potential plant in question) is
abundant enough to meet the demand on consistent basis for industri-
alization, otherwise there will be little value for investing millions of
dollars [95]. The quality of the product and sometimes the chemotype
itself will vary depending on several factors such as varieties, develop-
mental stages, environment which includes soil parameters, climatic
conditions, and even plant's phenological phase. For instance, EOs of two
morphologically distinct varieties of L. javanica growing at different lo-
cations in Malawi were found to produce different major chemical con-
stituents. Perillaldehyde and myrcenone (ipsdienone) were the major
constituents in oil of L. javanica var. javanica and L. javanica var. whytei
respectively. While Perillaldehyde was found to exhibit 100% contact
toxicity at 10 mg/mL against S. zeamais, myrcenone (ipsdienone) was not
toxic at all [40]. Similarly, Tephrosia vogelii (Hook.f.) (Fabaceae)
collected at different time period (Jan, Mar, Jun 2010) from 13 different
farms in Malawi were reported to show significance difference in the
level of tephrosin, deguelin and rotenone (all three phytochemicals with
insecticidal property) [97]. These two examples indicate variation in the
secondary metabolites production could be due to genetic as well as
environmental factors. Therefore, obtaining a standardized secondary
metabolite product is possible when all the favorable conditions are
achieved at right time, which in fact is a huge challenge. To address this
challenge, elicitation products, genetic manipulation and providing the
correct environment for secondary metabolite production by plants have
been suggested [96–98]. Last but probably the most important of these
issues is the strict regulatory requirements, which were framed keeping
in view of the synthetic pesticides. The regulation involved in the
authorization of botanical pesticides is stringent and robust [95]. But
without such regulatory framework, the development of biopesticides
cannot be legalized. Countries with strict and dedicated regulatory norms
are always the most accomplished in commercializing biopesticides [99].
9
Journal of Agriculture and Food Research 4 (2021) 100127
Not only the quality product, but the safety documentation through
proper toxicological studies is also required. Given the complexity of the
metabolic pathway of secondary metabolite production it is not an easy
ride to maintain the requisite quality all the time. It is time to re-evaluate
the existing regulatory norms making it more simplified and develop a
better understanding and cooperation between the research personal and
industries for wide scale dissemination of the technology involving
PVOCs [98].
6. Conclusion
Plant-derived insecticides have always been a major weapon in the
farmers' armory in managing insect pests of their farm produce. It was
only after the discovery of the organochlorine and organophosphate in-
secticides in the late 1930s and early 1940s that the focus shifted to
synthetic insecticides. The present review revealed that plant volatile
organic compounds can be reinstated to accomplish the intention of
reducing the application of synthetic insecticides in the management of
stored grain insect infestation. But at first, we must understand the
constraint associated with commercialization process of products based
on PVOCs. Only after crossing the hurdles plant volatile organic com-
pounds may be recommended as a viable alternative to synthetic in-
secticides since it is economical, easily available at farmer level and eco-
friendly with low mammalian toxicity. Plant volatiles organic com-
pounds potentially offer a solution to problems associated with health
risks, availability, costs and resistance as in the case of synthetic pesti-
cides, and to that of lack of equipment for hermetic storage, gamma
irradiation, and controlled atmospheres.
Declaration of competing interest
The authors, Kabrambam D. Singh, Adesina J. Mobolade, Rupjyoti
Bharali, Dinabandhu Sahoo and Yallappa Rajashekar declare that they
have no conflict of interest.
Acknowledgments
The authors wish to thank the Director, Institute of Bioresources and
Sustainable Development, Manipur, India for his keen interest in this
study. The First author acknowledges the financial support by Depart-
ment of Biotechnology, Ministry of Science and Technology, Govt. of
India, New Delhi through DBT Junior Research Fellowship Number:
DBT/2016/IBSD/727.
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