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REVIEW
Nanoparticles for pest control: current status and futureperspectives
C. G. Athanassiou1 • N. G. Kavallieratos2 • G. Benelli3,7 • D. Losic4 •
P. Usha Rani5 • N. Desneux6
Received: 3 October 2016 / Revised: 19 June 2017 / Accepted: 21 June 2017 / Published online: 21 August 2017
� Springer-Verlag GmbH Germany 2017
Abstract In the current paper, we reviewed the use of
nanoparticles (NPs) in crop protection, emphasizing the
control of pests in the agricultural and urban environment.
At the same time, we provide the framework on which the
technology of NPs is based and the various categories of
NPs that are currently used for pest control. Apart from the
use of NPs as carriers of a broad category of active
ingredients, including insecticides and pheromones, some
NPs can be used successfully as insecticides alone. More-
over, several types of NPs are produced by natural
resource-based substances, which make them promising
‘‘green’’ alternatives to the use of traditional pest control
agents. Finally, the potentials in the use of NPs are briefly
illustrated and discussed.
Keywords Nanotechnology � Green synthesis �Nanopesticides � Nanotoxicity � Nanoencapsulation �Nanoinsecticides
Key message
• There is a knowledge gap on the use of nanoparticles in
pest control.
• We reviewed the use of nanoparticles for insect control
and the different categories of pests that can be
controlled.
• Nanoparticles should become important components in
an IPM-based strategy in the agro-food and urban
environment.
Introduction
Despite the fact that there are several available alternative
methods, pest control is still largely based on the use of pes-
ticides, in the sense of organic chemical-based ingredients that
are applied on the crops, the commodity, or the urban envi-
ronment. Even today, many of the registered pesticides are
neurotoxic, which means that their primary mode of action
interferes with the insects’ nervous system and may pose risks
of mammals. Newer compounds, such as the insecticides that
are adenosine triphosphate (ATP) disruptors or insect growth
regulators (IGRs), have been introduced recently in the mar-
ket and have gradually reduced the use of neurotoxic com-
pounds, but there are still concerns about their environmental
impact. In this regard, pesticide use has been related with
mammalian toxicity, environmental contamination, and
Communicated by M. Traugott.
& C. G. Athanassiou
1 Laboratory of Entomology and Agricultural Zoology,
Department of Agriculture, Crop Production and Rural
Environment, University of Thessaly, Phytokou Str.,
38446 N. Ionia, Magnesia, Greece
2 Laboratory of Agricultural Zoology and Entomology,
Department of Crop Science, Agricultural University of
Athens, 75 Iera Odos Str., 11855 Athens, Attica, Greece
3 Department of Agriculture, Food and Environment,
University of Pisa, Via del Borghetto 80, 56124 Pisa, Italy
4 School of Chemical Engineering, The University of Adelaide,
Adelaide, SA 5005, Australia
5 Biology and Biotechnology Division, CSIR-Indian Institute
of Chemical Technology, Tarnaka, Hyderabad 500007, India
6 INRA (French National Institute for Agricultural Research),
Universite Cote d’Azur, CNRS, UMR 1355-7254, Institut
Sophia Agrobiotech, 06903 Sophia Antipolis, France
7 The BioRobotics Institute, Scuola Superiore Sant’Anna,
Viale Rinaldo Piaggio 34, 56025 Pontedera, Pisa, Italy
123
J Pest Sci (2018) 91:1–15
https://doi.org/10.1007/s10340-017-0898-0
bioaccumulation. These variables, along with the increased
frequency of resistance development by many insect species
to many of the currently used compounds, are major key
challenges in agriculture, and may considerably limit the
active ingredients that are effective. To address these prob-
lems, new pest control strategies are required through intro-
duction of innovative pest-resistive concepts and advanced
technologies for pest management.
Nanotechnology is emerging as a highly attractive research
field toward achieving these goals, offering new methods for
designing novel active ingredients with nanoscale dimen-
sions, as well as their formulation and delivery, which are
collectively referred to as ‘‘nanopesticides.’’ Nanopesticide
research, introduced relatively recently, is an emerging field
that can be defined as application of nanotechnology for crop
protection. This field compromises broad research aspects
including study of fundamental understanding of interaction
of nanoscale materials and insects, formulation of the active
ingredients into nanoemulsions and dispersions using existing
pesticides, development of new nanopesticide formulations
using nanomaterials as active pesticide agents, or using these
nanomaterials as nanocarriers for their delivery (Smith et al.
2008; Yasur and Usha Rani 2013; Benelli et al. 2017). This
broad nanopesticide research is expected to address the main
limitations of the existing pest control strategies and provides
new advanced nano-based formulations that remain stable and
active in the target environment (i.e., not heavily affected by
sun, heat, and rain), penetrate the target organism (insect),
resist defense of the pest, remain benign to plants and mam-
mals, be cost effective to formulate and manufacture, and
preferably possess a new mode of action (Smith et al. 2008;
Benelli 2016a, b).
Nanoparticles for pest control: definition, concepts,and perspectives
Nanoparticles (NPs) can be defined as a subclass of ultrafine
particles with characteristic dimensions from 1 to 100 nm and
have properties that are not shared by non-nanoscale particles
with the same chemical composition (Auffan et al. 2009). The
basis of the 100-nm limit is the fact that unique properties that
differentiate particles from the bulk material typically develop
at a critical size of under 100 nm. However, because other
phenomena (e.g., transparency or turbidity, ultrafiltration,
stable dispersion) that extend the upper limit are occasionally
considered, the use of the prefix ‘‘nano’’ (‘‘ma9mo’’ in Greek,
meaning small, dwarf) is accepted for dimensions smaller than
500 nm (Aleman et al. 2007). The size, shape (spherical, rods,
tubes, irregular), surface-to-volume ratio, crystal phase (crys-
talline, amorphous), and chemical composition (e.g., metallic,
carbon, inorganic, organic, polymeric) are key parameters
which define many outstanding properties of these materials
relevant for their use in pesticide application, including toxi-
city. A broad variety of materials were synthesized or used
from natural materials to make NPs in different forms and
chemical composition including metal, metal oxides, semi-
conductor quantum dots (QDs), carbon, ceramics, silicates,
lipids, polymers, proteins, dendrimers, and emulsions (Nie-
meyer and Doz 2001; Oskam 2006; Puoci et al. 2008). Some
common benefits of NP-based pesticide formulations include:
(a) increased solubility of water insoluble active ingredients,
(b) increased stability of formulation, (c) elimination of toxic
organic solvents in comparison with conventionally used
pesticides, (d) capability for slow release of active ingredients,
(e) improved stability to prevent their early degradation,
(f) improved mobility and higher insecticidal activity due to
smaller particle size, and (g) larger surface area which is likely
to extend their longevity (Sasson et al. 2007).
This review presents the recent advances in the devel-
opment of NP-based formulations on the basis of three
major concepts: the improvement of conventional pesticide
formulations, the development of delivery systems and the
use of NPs as nanocarriers, and solid NPs used as active
pesticide agents.
Nanoparticles to improve pesticide formulations
Recently, a number of plant-synthesized NPs have been
investigated for their efficacy against arthropod pests of
economic importance, including moths (Roni et al. 2015),
beetles (Abduz Zahir et al. 2012), lice (e.g., Pediculus
humanus capitis) (Jayaseelan et al. 2011), hard ticks (e.g.,
Haemaphysalis bispinosa) (Abduz Zahir and Abdul
Rahuman 2012), louse flies (e.g., Hippobosca maculata)
(Jayaseelan et al. 2012), and mosquitoes (Benelli 2016a, b).
However, not surprisingly, the majority of research dealing
with nanosynthesis of insecticides focused on mosquito
control. More than 100 research products were found in the
SCOPUS database using the keywords ‘‘plant nanoparticles
mosquitoes’’ (Benelli 2016a).
Most of currently used pesticides are poorly water sol-
uble molecules, and their formulations are based on
emulsifiable concentrates (ECs), oil-in-water (O/W)
emulsions, or similar formulations that are variations of the
above (Knowles 2009). ECs usually consist of organic
solvents that are expensive, flammable, and toxic, or a
blend of surfactant emulsifiers to ensure spontaneous
emulsification into water in the spray tank. O/W emulsions
do not have these shortcomings because they are based on
the removal of solvent and the introduction of a mixture of
a non-ionic surfactant, block polymers, and polymeric
surfactants; nevertheless, one of the major drawbacks in
their use is the fact that emulsification requires high-energy
input (Kah et al. 2013; Kah and Hofmann 2014).
2 J Pest Sci (2018) 91:1–15
123
To address these disadvantages, new formulations based
on micro- and nanoemulsions were introduced with the
capability to provide NPs in sizes from 20 to 100 nm
(Tadros et al. 2004; Lawrence and Warisnoicharoen 2006;
Knowles 2009; Tomlin 2009; Song et al. 2009). Several
microemulsion formulations are available on the market,
including plant growth regulators and systemic fungicides,
for broad-spectrum disease control in different types of
target plants (Tomlin 2009; ObservatoryNano 2010).
Microemulsions are more stable than nanoemulsions,
which require high-energy input that may be difficult to
scale up for commercial agrochemical production, or may
not be practical for on-site preparation by the handlers
(e.g., high-shear stirring, high-pressure homogenizers, or
ultrasound generators). Compared to other conventional
formulations, microemulsions provide numerous advan-
tages including improved tank mix compatibility, improved
stability, reduced low flammability, reduced handler toxi-
city (due to low solvent content), and most importantly
enhanced efficacy due to improved penetration or uptake
resulting from the high solubilizing power of surfactants
(Green and Beestman 2007; Knowles 2009). However,
there are certain disadvantages of these substrates, such as
low content of active ingredients (\30%), high concen-
tration of surfactants (*20%), and the limited number of
suitable surfactant systems (Lawrence and Waris-
noicharoen 2006). These limitations can be partially solved
by another formulation concept based on nanodispersion or
nanosuspension, where active ingredients of nanocrystals,
or crystalline or amorphous NPs of 50 nm (prepared by
specific procedure), create nanodispersions having similar
properties to solutions (Muller and Junghanns 2006).
Interestingly, this approach is not widely applied yet, with
only a few reported examples (triclosan and novaluron)
(Zhang et al. 2008; Elek et al. 2010).
The development of sustainable release systems using
NPs could increase the performance and the efficiency of
pesticides and also might reduce their adverse environ-
mental effects. Generally, NPs can easily penetrate into
plant cells making them a ‘‘nanocarrier’’ transport system.
They are able to deliver products accurately, as they are
customized to transfer a particular biomolecule to the cell,
tissue, or organism when needed (Du et al. 2013). Several
inorganic nanomaterials with unique physical and chemical
properties, such as metals, metal oxides, silica- and carbon-
based materials, and semiconductors, have been engineered
for tracking or delivery purposes (Kunzmann et al. 2011).
Nanodelivery vehicles can increase seed vigor, plant
growth, and in some cases crop yield in addition to crop
protection from pests and diseases, while they can be also
used for genetic manipulation (Kole et al. 2013). The
small-sized NPs often enter plant cells through binding to a
carrier protein, ion channels, or creating new pores (Rico
et al. 2011). Plant cell walls have the remarkable capability
of impeding the entry of NPs. In spite of this doubtful
impact of nanomaterial application on plants, some of the
current studies focus on the phytotoxicity of NPs (Lee et al.
2010; Slomberg and Schoenfisch 2012) and the influence of
NPs on plant development (Khodakovskaya et al. 2009;
Balalakshmi et al. 2017). Torney et al. (2007) reported that
NPs can effectively deliver biomolecules into plants, and
this idea has been expanded by other researchers for a
wider range of cases (Martin-Ortigosa et al. 2012a, b). The
available reports indicate that plant cells can take up very
small NPs (Yasur and Usha Rani 2013, 2015).
The uptake efficiency and effects of various NPs on
growth and metabolic functions vary remarkably among
plants and has been thoroughly tested. As carriers, NPs are
able to reach the plant internal systems easily and may
cause significant changes to these systems. Rodriguez et al.
(2011) noted that most of the available studies on phyto-
toxicity of NPs are based on germination and root elon-
gation, factors which cannot be always reliable indicators
to evaluate NP toxicity to plants. Khodakovskaya et al.
(2009) revealed that carbon nanotubes have a positive
impact on tomato plants through an increase in seed ger-
mination and growth, and they suggested that these effects
are due to the carbon nanotubes ability to penetrate the
seed coat and enhance crucial water uptake. It has been
shown that NPs, such as nano-ZNO particles at certain
optimum concentration, promote growth of seedlings of
mung bean, Vigna radiata (L.) R. Wilczek, and gram,
Cicer arietinum L. (Mahajan et al. 2011). Treating castor
seeds, Ricinus communis L., with silver NPs did not affect
seed germination rate nor growth of lepidopteran insects on
the seeds (Yasur and Usha Rani 2013, 2015). Studies with
transmission electron microscopy (TEM) of NP effects on
plants confirmed their penetration into the cell organelles
and localization of the NPs at mitochondria or nucleolus in
both plant and insect tissues, which suggests that they can
be used for targeted delivery of pesticides or fertilizers
(Yasur and Usha Rani 2013, 2015). Plant-mediated syn-
thesis of NPs was confirmed by UV-visualization spec-
trophotometry, followed by scanning electron microscopy
(SEM) and/or transmission electron microscopy, energy-
dispersive X-ray spectroscopy (EDX), Fourier transform
infrared spectroscopy (FTIR), and X-ray diffraction studies
(XRD) (Rajan et al. 2015).
Pesticide delivery system using nanoparticlesas nanocarriers
Learning from drug delivery concepts introduced in med-
icine where NPs have been successfully used for delivery
of therapeutics for medical therapy, a similar concept was
J Pest Sci (2018) 91:1–15 3
123
developed for pest control, known as ‘‘pesticide delivery
system’’ (PDS) (Tsuji 2001). The aim is to make the active
ingredients available to a specified target at concentrations
and durations designed to accomplish the intended effect
by maintenance of the fullest biological efficacy and
reduction of various harmful effects (Ghormade et al.
2011). Controlled delivery is particularly important to
provide optimized release of necessary and sufficient
amounts of pesticides over a period of time to obtain the
maximum biological efficacy and to minimize potential
harmful effects (Tsuji 2001). The advantage of using NPs
as nanocarriers is in their ability to have high effective
loading due to the larger surface area, easy attachment of
single and several different pesticide molecules, and a
reasonably fast mass transfer to the target, i.e., insects’
body. Pesticides, when encapsulated, are likely to have a
more gradual release over time, which requires their
application less often as compared with very highly con-
centrated and perhaps toxic initial applications followed by
repeated applications. At the same time, NPs delay the loss
in efficacy due to degradation.
Several different concepts for loading of active pesticide
molecules on NPs may include adsorption, covalent
attachment mediated by different ligands, encapsulation,
and entrapment inside NP (Fig. 1). Controlled and slow
release of the active molecules can be achieved based on
degradation properties of the nanocarrier (e.g., polymer),
bonding of the ingredients to the material, and the envi-
ronmental conditions. The most attractive NPs that are
considered as carriers for delivery of pesticides are based
on polymers (soft NPs), synthetic silica, titania, alumina,
Ag, Cu, and natural minerals/clays with nanoscale dimen-
sions (inorganic or solid NPs). Some common paradigms
of insecticides explored using this nanotechnology
approach are essential oils, including neem oil (Anjali et al.
2010; Xu et al. 2010; Jerobin et al. 2012); garlic essential
oil (Yang et al. 2009); Artemisia arborescens L. (Asterales:
Asteraceae) essential oil (Lai et al. 2006); Lippia sidoides
L. (Lamiales: Verbenaceae) oil (Abreu et al. 2012);
Catharanthus roseus extract (L.) G. Don (Pavunraj et al.
2017) and juniper oil (Athanassiou et al. 2013). Nanode-
livery systems for pheromones (Bhagat et al. 2013; Hell-
mann et al. 2011; Trematerra et al. 2013) and various plant
extracts also have been proposed (e.g., capsaicin from chili
peppers, Bohua and Ziyong 2011; Lansiumamide B extract
from the seeds of Clausena lansium (Lour.) Skeels, Yin
et al. 2012).
Nanoporous materials particularly possess organized
pore distributions and increased surface areas which
enhance the capacity of sorbents and enable incorporation
of functionality. This property provides better sensitivity in
detection methods, and improved selectivity and yield in
catalyst-based synthesis (Appell and Jackson 2013).
Nanoencapsulation is another very important technique
which can be utilized for safer handling of pesticides with
less exposure to the environment. Carbon nanotubes were
discovered in 1991. These are only a few nanometers in
diameter, but they can conduct electricity better than cop-
per and they are 100 times stronger than steel but only one-
sixth of its weight. This is one good example of the benefits
of nanomaterial application (Lok 2010). Among the vari-
ous NPs available, silica-based NPs have generated interest
as potential delivery agents of agrochemicals in plants.
This is mainly due to their structural flexibility in forming
NPs of various sizes and shapes, and also their ability to
form pores for loading biomolecules (Campbell et al. 2011;
Jang et al. 2013; Athanassiou et al. 2013). Two types of
engineered silica NPs have been described: solid and
mesoporous silica NPs (MSN) (Slomberg and Schoenfisch
2012; Wanyika et al. 2012). MSNs are formed by a matrix
of well-ordered pores that allow high loading capacity of
molecules like proteins (Popat et al. 2011). Also, it is
possible to modify the surfaces of MSNs, which permits
the NP to be customized to specific experimental needs
(Trewyn et al. 2007). MSNs also were used in the slow
release of urea as a fertilizer in soil and water (Wanyika
Fig. 1 Schematic representation of different polymer nanoparticles
for delivery of pesticides, a adsorption on nanoparticle; b attachment
on nanoparticle by different linkers; c encapsulation inside polymeric
hydrophobic or hydrophilic core (polymer micelles); and d entrapment
inside polymeric nanoparticle (prepared by DL)
4 J Pest Sci (2018) 91:1–15
123
et al. 2012). Gold plating of MSN surfaces increased NP
density and, subsequently, the ability to pass through the
plant cell wall upon bombardment, thus improving their
performance (Martin-Ortigosa et al. 2012b). The uptake
and phytotoxicity of non-porous silica NPs in the seedlings
of rice and roots of Arabidopsis also has been demonstrated
(Nair et al. 2011; Slomberg and Schoenfisch 2012). In this
regard, calcinated non-porous silica NPs could be trans-
ported into roots of Arabidopsis thaliana (L.) Heynh.
(Brassicales: Brassicaceae) without causing any phytotoxic
effects (Slomberg and Schoenfisch 2012).
NPs are important gene carriers in various types of
plants, and they can be further utilized to effectively
overcome transgenic silencing via controlling the copies
and function of DNA (Kumar et al. 2016). Also, NPs can
mediate multigene transformation without involving the
traditional building method of a complex carrier (Fu et al.
2012; Martin-Ortigosa et al. 2012a). Torney et al. (2007)
reported the efficient delivery of DNA and chemicals
through silica NPs internalized in plant cells, with no
specialized equipment. A 3-nm mesoporous silica NP
(MSN) was successfully utilized for delivering DNA and
chemicals into isolated plant cells (Barron 2007; Galbraith
2007). DNA was introduced successfully in tobacco and
corn plants using this technology (Torney et al. 2007).
Green synthesis of protein-lipid conjugated Ag NPs using
Sterculia foetida L. (Malvales: Sterculiaceae) seed extract
and its anti-proliferative activity against HeLa cancer cell
lines showed their biocompatibility and translocation into
the HeLa cells (Rajasekharreddy and Usha Rani 2014a).
Polymer nanoparticles as nanocarriers
Polymer nanocarriers are based on polymer NPs, and they
include polymeric nanospheres and nanocapsules. Their
attractiveness is based on flexibility to design a complex
drug delivery system including multiple pesticides with
different mode of actions, scalable preparation, biocom-
patibility, and biodegradability. The active molecules in
polymer nanospheres are randomly distributed in a poly-
mer matrix in nanocapsules with a core–shell structure that
can act as a reservoir for encapsulation of a hydrophobic
drug (Torchilin 2006). Polymer nanocapsules, also known
as polymer micelles, provide advantages over larger cap-
sules by having better stability of the spraying solution,
increased uptake, increased spraying surface, and reduced
phytotoxicity owing to a more homogeneous distribution
that provides them with better protection. In both cases,
polymer NPs serve as a protective reservoir and diffusion-
controlled release carrier which can be controlled
depending on degradation and permeability properties of
the polymer. Another important feature of polymer
nanocarriers is their protective function for application of
phytochemicals (secondary metabolites) and essential oils
which have stability problems, so this can increase their
cost effectiveness. In the case of essential oils, their
chemical instability in the presence of air, light, moisture,
and high temperatures that causes rapid evaporation and
degradation of some active components is a major concern,
and their incorporation into a controlled release nanocarrier
will prevent rapid evaporation and degradation, enhance
stability, and maintain the minimum effective dosage/ap-
plication (Ghormade et al. 2011).
Many types of polymers have been evaluated for
designing polymer NP formulations, which are similar to
those used in the pharmaceutical or cosmetic sectors,
consisting mainly of polyesters (e.g., poly-e-caprolactone
and polyethylene glycol (PEG)), polysaccharides (e.g.,
chitosan, alginates, and starch), and recently biodegradable
materials of biological origin such as beeswax, corn oil, or
lecithin or cashew gum (Abreu et al. 2012; Nguyen et al.
2012). Among them, polyethylene glycol-based amphi-
philic copolymers are so far most attractive due to their
biodegradability, easy processing, and well-explored
properties (Torchilin 2006; Shakil et al. 2010).
The release studies of series of plant protection mole-
cules (mainly pesticides) from PEG polymer nanoformu-
lations in water have shown significantly slower release
(several weeks) compared to commercial formulations,
including imidacloprid (Adak et al. 2012), thiamethoxam
(Sarkar et al. 2012), carbofuran (Pankaj et al. 2012), thiram
(Kaushik et al. 2013), and beta-cyfluthrin (Loha et al.
2011). Bioassay studies also showed that some of these
PEG-based formulations are more effective than commer-
cial products for the control of insects and nematodes
(Loha et al. 2012; Pankaj et al. 2012). Yang et al. (2009)
used essential oil from garlic loaded on polymer NPs
coated with PEG for control of adults of the red flour
beetle, Tribolium castaneum (Herbst) (Coleoptera: Tene-
brionidae), with very good results. In fact, in that study,
efficacy remained over 80% after 5 months due to the
controlled slow release of the active components, in com-
parison with free garlic essential oil (11%). This indicated
the feasibility of PEG-coated NPs loaded with garlic
essential oil for control of stored-product pests.
It is important to note that the greater efficacy of these
nanoformulations relative to the commercial formulations
was generally only noticeable over a relatively long period
(i.e., 30 days) which is likely due to their slower release
rather than to an increased uptake of the released pesticide
by the target organisms. Some disadvantages of polymer-
based nanoformulations are their very slow release (in
some cases), reduced environmental stability, higher pro-
duction cost, and high-energy preparation methods
(Torchilin 2006).
J Pest Sci (2018) 91:1–15 5
123
Inorganic nanoparticles as nanocarriers
Solid inorganic NPs have been intensively studied in the
last two decades for the formulation of pharmaceuticals, as
they combine the advantages of nanoemulsions, liposomes,
and polymer NPs, while simultaneously avoiding their
disadvantages by providing better stability, more control-
lable release, higher loading, and simpler production
resulting in lower cost (Dimetry and Hussein 2016; Benelli
2016a). Hence, it is not surprising that this trend was used
for the development of advanced pesticide delivery sys-
tems (Choy et al. 2007; Ghormade et al. 2011; Kim et al.
2012; Kah et al. 2013; Werdin-Gonzalez et al. 2016; Small
et al. 2016; Sujitha et al. 2017).
Silica NPs are among the most attractive inorganic NPs
explored as nanocarriers for pesticide delivery, which
include insecticides, growth promoters, fungicides,
biopesticides, and pheromones (Barik et al. 2008). Silicon
has long been known to enhance plant tolerance to various
abiotic and biotic stresses, and silica NPs have therefore
naturally been suggested as potential candidates for
increasing the control over a range of agricultural pests
(Barik et al. 2008). Novel formulations based on silica NPs
have been proposed recently for the slow release of
chlorfenapyr and growth promoters with promising results
(Mingming et al. 2013; Song et al. 2012). Field tests
demonstrated that the insecticidal activity associated with
silica NPs was twice as high as that of chlorfenapyr asso-
ciated with microparticles or without particles (Song et al.
2012). The mechanism involved is different from the
insecticide formulations that have no NPs, and observed
higher efficacy is probably related to the sustained and
slow release (i.e., over 10–20 weeks) providing high
localized concentration over a long time.
The potential of nanosilica to control insects during
grain storage has been reported in recent works. For
example, Debnath et al. (2011) reported higher insect
mortality from treatment with silica NPs (15–30 nm) than
with bulk silica (100–400 nm) confirming that NPs with
smaller size have higher efficacy. Furthermore, a study on
influence of surface modification of silica NPs using dif-
ferent coatings (hydrophobic, hydrophilic, or lipophilic)
indicated a mechanical mode of action that could be
enhanced for smaller particles. This study indicated that
silica NPs of the same size coated with 3-mercaptopropy-
ltriethoxysilane were more efficient than those coated with
hexamethyl disilazane for reasons, however, that are poorly
understood (Debnath et al. 2012). Also, in that work, the
application rates were generally comparable with those
recommended for commercially available diatomaceous
earths (0.5–2 g/kg of grain), and hence the additional costs
involved in engineering NPs may not be justified by the
slight (if any) increase in efficacy. At the same time, these
rates are considered too high for ‘‘real-world’’ applications.
There are several studies that demonstrated the use of
hollow silica NPs as carriers for the controlled release and
UV shielding of avermectin and validamycinis (Li et al.
2006, 2007; Liu et al. 2006). The rate of release of these
molecules was influenced by temperature, pH, and shell
thickness. The release profile of encapsulated avermectin
was shown to have a multistage pattern which was inter-
preted as being due to the release of active ingredient located
in different parts of the particles (i.e., external, in pore
channels, and in the internal core). The absence of phyto-
toxicity was also demonstrated for several plants sprayed
with concentrations up to 3200 mg/l (Park et al. 2006).
Using nanoparticles alone as pesticides
NPs having insecticidal properties can be used not only as
nanocarriers, but also as an active pesticide agent or
biopesticide (Barik et al. 2008; Elango et al. 2016). Most
promising examples are based on amorphous nanosilica
obtained from various natural sources like the shell wall of
phytoplankton, epidermis of vegetables, burnt pretreated
rice hulls, straw at thermoelectric plants, and volcanic soil;
some of these materials have particle sizes that exceeds
1 lm, but they have minute pores that are considerably
smaller than 100 nm (Korunic 1998; Athanassiou et al.
2005; Barik et al. 2008). The silica NPs were physio-sor-
bed by the cuticular lipids disrupting the protective barrier
and thereby causing death of insects purely by physical
means with a mode of action similar to that observed for
diatom particles used for protection of stored grain
(Korunic 1998; Vayias and Athanassiou 2004; Barik et al.
2008; Kavallieratos et al. 2017). Application of NPs on the
leaf and stem surface did not alter either photosynthesis or
respiration in several groups of horticultural and crop
plants. They did not cause alteration of gene expression in
insect trachea and were, thus, qualified for approval as a
nanobiopesticide. Use of amorphous silica as a
nanobiopesticide is considered safe for humans by World
Health Organization (WHO). Debnath et al. (2011) repor-
ted that silica NPs caused 100% mortality in adults of the
rice weevil, Sitophilus oryzae (L.) (Coleoptera: Cur-
culionidae). Furthermore, surface charged modified
hydrophobic silica NPs (3–5 nm) were successfully used to
control a range of agricultural insect pests and animal
ectoparasites of veterinary importance (Ulrichs et al. 2006).
It was successfully applied as a thin film on seeds to
decrease fungal growth and boost cereal germination
(Robinson and Salejova-Zadrazilova 2010). Therefore,
nanosilica particles have promising applications for control
6 J Pest Sci (2018) 91:1–15
123
of stored grain and household pests, animal parasites,
fungi, and worms.
Silver and other mineral-based nanoparticles
Like other NP categories, metal-based NPs can be com-
bined with pesticides, and enable the reduction of appli-
cation dose (Perez de Luque and Rubiales 2009) or
enhance the efficacy of insecticidal formulations (Liu et al.
2008; Werdin Gonzalez et al. 2014; Patil et al. 2016).
However, several previous research efforts have been
conducted on various metal nanomaterials that exhibit
insecticidal properties themselves in order to enhance the
potential tools for alternative and effective control of
agricultural or stored-product pests but also of pests that
are related with humans’ and animals’ health. These
materials have been synthesized either exclusively chemi-
cally or by involving living organisms (Dubey et al. 2009).
Nanomaterials of the former category that have shown
insecticidal efficacy are aluminum oxide (ANP) or nanos-
tructured alumina (NSA) (Al2O3), zinc oxide (ZNP) (ZnO),
titanium oxide (TNP) (TiO2), and silver NPs (AgNPs). For
example, Ki et al. (2007) found almost complete mortality
of the case-bearing clothes moth, Tinea pellionella (L.)
(Lepidoptera: Tineidae), larvae in wool fibers treated with
20 ppm of nanosilver colloid (SNSE, sulfur nanosilver
ethanol-based colloid) 14 days after exposure and consid-
erable reduction of the weight loss of the treated fiber
compared with the controls. Stadler et al. (2009) reported
complete mortality of R. dominica and S. oryzae adults in
wheat treated with 1000 ppm of NSA dust after 9 days of
exposure and approximately 95% mortality after only
3 days of exposure. Furthermore, NSA that was produced
by combustion of glycine and aluminum nitrate applied as
dust on wheat at doses ranging from 62.5 to 1000 ppm
caused[94% mortality of S. oryzae adults after 15 days of
exposure at 57 and 75% relative humidity (Stadler et al.
2012). Nevertheless, the efficacy of this NSA for control of
R. dominica adults resulted in lower overall mortality
levels than for S. oryzae. Similar results were obtained
when three novel NSA dusts, based on chemical solution
methods, were applied on wheat for control of R. dominica
and S. oryzae (Buteler et al. 2015). The mode of action of
these dusts is based on the absorption of epicuticular lipids
through capillarity, causing death due to dehydration
(Stadler et al. 2012; Buteler et al. 2015). The efficacy of
NSAs, however, depends on their individual physical
characteristics, i.e., particle size, particle morphology, and
surface area, but also on other biotic and abiotic factors
such as target species, dose, exposure interval, and relative
humidity (Stadler et al. 2012; Buteler et al. 2015). Contrary
to results for NSA, the application of other NPs, i.e., ZNP
and TNP, mixed as dusts with rice did kill adults of S.
oryzae, although the overall mortality did not exceed 65%
at 1000 ppm after 7 days of exposure. However, the
increase in dose of TNP hydrophobic to 2000 ppm caused
93% adult mortality (Goswami et al. 2010). Still,
2000 ppm should be considered as a high application
concentration.
Paradigms of nanoparticle use for pest control
Apart from stored-product pests, nanomaterials have also
been tested for control of agricultural pests. For example,
AgNP dust, stabilized with polyvinyl pyrrolidone, was
applied to R. communis leaves for control of castor semi-
looper, Achaea janata (L.) (Lepidoptera: Noctuidae), and
the oriental leafworm moth, Spodoptera litura (F.) (Lepi-
doptera: Noctuidae). It was found that AgNPs negatively
influenced the growth (i.e., larval weight and period of
development, pupal weight, and adult weight) of both
species as a result of the physiological changes in the body
of the insects due to the presence of NPs (Yasur and Usha
Rani 2015). There are also several recent paradigms of
successful implementation of NPs for this use (Patil et al.
2016; Nayak et al. 2016; Benelli 2016a; Lee et al. 2017).
The progress in chemistry, but also consumers’ and
environmental concerns or objections to the use of syn-
thetic materials, propelled scientists to find alternative
methods of production of nanomaterials, so called ‘‘green
synthesis’’ of metal NPs (Benelli and Lukehart 2017). The
idea of green synthesis is based on the fact that various
organisms are capable of generating non-organic materials
(Simkiss and Wilbur 1989). Microorganisms, such as
bacteria, actinomycetes, fungi, yeasts, and viruses, but also
plant extracts have been used for the synthesis of metal
(silver, gold, platinum, palladium, titanium, and zirconium)
NPs (Dubey et al. 2009; Narayanan and Sakthivel 2010).
Recent research efforts point out the potential of the green
synthesis of metal NPs, chiefly AgNPs, for use against a
wide spectrum of noxious pest species either in the labo-
ratory or in the field. For example, Jayaseelan et al. (2011)
reported that AgNPs synthesized by leaf aqueous extract of
Tinospora cordifolia (Thunb.) Miers (Ranunculales:
Menispermaceae) caused complete mortality of the head
louse, P. humanus capitis De Geer (Phthiraptera: Pedicul-
idae) adults after 1 h of exposure at 25 mg/l.
Regarding mosquito control, most of the research has
focused on larvicidal and pupicidal activity of NPs against
the malaria vector Anopheles stephensi Liston (Diptera:
Culicidae), the filariasis vector Culex quinquefasciatus Say
(Diptera: Culicidae), and the arbovirus vectors Aedes
aegypti (Linnaeus in Hasselquist) and Aedes albopictus
(Skuse) (Diptera: Culicidae). In several cases, the NPs’
J Pest Sci (2018) 91:1–15 7
123
toxicity against neglected mosquito vectors, such as
Anopheles subpictus (Grassi) (Diptera: Culicidae) and
Culex tritaeniorhynchus Giles (Diptera: Culicidae), has
been also assessed (Govindarajan and Benelli 2016). As a
general trend, plant-synthesized NPs showed promising
activity against young instars of mosquito vectors, with the
majority of LC50 values ranging from 1 to 30 ppm. Among
the different tested species, C. quinquefasciatus larvae and
pupae were the most resistant to the toxic activity of plant-
synthesized NPs (Benelli 2016a). However, there has been
little effort to shed light on the toxicity mecha-
nism(s) leading to larval and pupal death in mosquito lar-
vae and pupae exposed to green-synthesized NPs. It has
been hypothesized that the biotoxicity against mosquito
young instars may be related to the ability of NPs to pen-
etrate through the exoskeleton. In the intracellular space,
NPs can bind to sulfur from proteins or to phosphorus from
DNA, leading to the rapid denaturation of organelles and
enzymes. Subsequently, the decrease in membrane per-
meability and disturbance in proton motive force may
cause loss of cellular function and cell death (Subramaniam
et al. 2015). In these studies, the residual toxicity of metal
ions against mosquito young instars had little role because
UV–Vis spectrophotometry results highlighted peak satu-
ration after 60, 120, or 180 min, indicating complete
reduction of metal ions (Murugan et al. 2015a).
Furthermore, plant-synthesized NPs showed promising
activity as ovicides and adulticides. In experiments con-
ducted with A. stephensi, A. aegypti, and C. quinquefas-
ciatus, egg hatchability was reduced by 100% after a single
exposure to 30 ppm of Sargassum muticum-synthesized
silver NPs (Madhiyazhagan et al. 2015). The toxicity
mechanism(s) exerted by silver NPs on mosquito eggs is
currently unknown. Similar results were obtained when
larvae of the mosquitoes A. subpictus and C. quinquefas-
ciatus were exposed in 20 mg/l AgNP solution for 24 h.
Also, 100% larval mortality of A. subpictus and C. quin-
quefasciatus was recorded after 24 h of exposure to AgNPs
synthesized by leaf aqueous extract of Mimosa pudica L.
(Fabales: Fabaceae) at 25 mg/l (Marimuthu et al. 2011). In
the same study, it was found that 89% of the exposed
larvae of the tick Rhipicephalus microplus Canestrini
(Acari: Ixodidae) were dead when exposed for 24 h in
20 mg/l of the same solution. Similarly, AgNPs synthe-
sized by leaf aqueous extract of Annona squamosa L.
(Magnoliales: Annonaceae) resulted in 100% mortality of
pupae or 1st–4th instar larvae of C. quinquefasciatus and
100, 98, and 89% mortality of 1st–3rd instar larvae, 4th
instar larvae, and pupae of Anopheles stephensi Liston
(Diptera: Culicidae), respectively, at 10 ppm (Arjunan
et al. 2012). AgNPs synthesized by root aqueous extract of
Delphinium denudatum Wall (Ranunculales: Ranuncu-
laceae) caused 100% mortality of 2nd instar larvae of A.
aegypti L. (Diptera: Culicidae) after 48 h of exposure at
1000 ppm (Suresh et al. 2014). In a field test, Dinesh et al.
(2015) showed that the AgNPs synthesized by leaf aqueous
extract of Aloe vera (L.) Burm.f. (Asparagales: Xanthor-
rhoeaceae) resulted in an overall reduction of 74.5, 86.6,
and 97.7% after 24, 48, and 72 h of application in water
reservoirs, respectively, of 1st–4th instar A. stephensi lar-
vae. Similarly, Suresh et al. (2015) reported 47.6, 76.7 and
100% mortality of A. aegypti larvae 24, 48, and 72 h,
respectively, after application of AgNPs synthesized by
leaf aqueous extract of Phyllanthus niruri L. (Mal-
pighiales: Phyllanthaceae). Concerning adulticidal toxicity,
only a few records are available. Silver NPs synthesized
using Feronia elephantum Correa (Sapindales: Rutaceae)
leaf extract were toxic to adults of A. stephensi, A. aegypti,
and C. quinquefasciatus, with LD50 values ranging from
18.041 to 21.798 lg/ml (Veerakumar and Govindarajan
2014). Silver NPs biosynthesized using Heliotropium
indicum L. (Eudicotidae: Boraginaceae) leaf extract have
been evaluated for control of adults of A. stephensi, A.
aegypti, and C. quinquefasciatus, and the maximum effi-
cacy has been observed against A. stephensi
(LD50 = 26.712 lg/ml) (Veerakumar et al. 2014). Silver
NPs prepared using neem leaf extract were toxic to C.
quinquefasciatus adults, with LC50 of 0.53 ppm calculated
after 4 h of exposure (Soni and Prakash 2014). Phyllanthus
niruri-synthesized silver NPs tested against A. aegypti
adults resulted in an LC50 of 6.68 (Suresh et al. 2015).
Mimusops elengi L. (Ericales: Sapotaceae)-synthesized
silver NPs resulted in LC50 values of 13.7 ppm against A.
stephensi and 14.7 ppm against A. albopictus (Subrama-
niam et al. 2015). Recently, it has been reported that a
single exposure to doses ranging from 100 to 500 ppm of
Hypnea musciformis (Wolfen) (Ericales: Cystocloniaceae)-
fabricated silver NPs greatly reduced A. aegypti longevity
in both sexes, as well as female fecundity (Roni et al.
2015). Another common pest that is associated with public
health issues, the housefly, Musca domestica L. (Diptera:
Muscidae), was treated at the adult stage with 10 ml/l of
AgNPs synthesized by leaf aqueous extract of Manilkara
zapota (L.) P. Royen (Ericales: Sapotaceae) and was
completely suppressed after 4 h of exposure (Kamaraj
et al. 2012). The cotton bollworm, Helicoverpa armigera
(Hubner) (Lepidoptera: Noctuidae), was found to be very
susceptible to AgNPs synthesized by leaf aqueous extract
of Euphorbia hirta L. (Malpighiales: Euphorbiaceae) since
all larval instars and pupae exhibited high mortality levels
(C80%) after only 4 days exposure in cotton, Gossypium
hirsutum L. (Malvales: Malvaceae), leaves that had been
treated with the NPs at 10 ppm (Durga Devi et al. 2014).
Apart from terrestrial plants, marine plants have been used
for the synthesis of metal NPs for control of insect pest
species that impact public health or agriculture. For
8 J Pest Sci (2018) 91:1–15
123
example, Vinayaga Moorthi et al. (2015) reported that
AgNPs synthesized by aqueous extract of Sargassum
muticum (Yendo) Fensholt (Fucales: Sargassaceae), origi-
nally collected from the Gulf of Mannar (India), caused
physiological and anatomical abnormalities in the body of
4th instar larvae of the common castor, Ariadne merione
(Cramer) (Lepidoptera: Nymphalidae). Similarly, Murugan
et al. (2015c) showed that AgNPs synthesized by aqueous
extract of Caulerpa scalpelliformis (R. Brown ex Turner)
C. Agardh (Bryopsidales: Caulerpaceae) were highly toxic
to 1st–4th instar larvae of C. quinquefasciatus causing
C80% mortality at 10 ppm. In the same study, the authors
suggested that C. scalpelliformis AgNPs exhibit synergistic
effect with Mesocyclops longisetus (Thiebaud) (Cy-
clopoida: Cyclopidae) as a novel biological control strat-
egy against larvae of C. quinquefasciatus. The
mycosynthesis of metal NPs has also revealed interesting
prospects for the management of certain insect pest species
(Amerasan et al. 2016). According to Salunkhe et al.
(2011), AgNPs synthesized by the filamentous fungus
Cochliobolus lunatus R. R. Nelson and Haasis (Pleospo-
rales: Pleosporaceae) resulted in complete mortality of
2nd–4th instar larvae of A. aegypti and A. stephensi at 5 or
10 ppm after 24 h of exposure. Another fungus,
Chrysosporium tropicum J. W. Carmich. (Onygenales:
Onygenaceae), has been used for the synthesis of AgNPs
and gold NPs (AuNPs) which were highly toxic, causing
100% mortality, to the 2nd instar after 1 h of exposure and
the 1st instar after 24 h of exposure, respectively (Soni and
Prakash 2012). AgNPs synthesized by extracellular filtrate
of the entomopathogenic fungus Trichoderma harzianum
Rifai (Hypocreales: Hypocreaceae) resulted in 92, 96, and
100% mortality of 1st, 2nd, and 3rd–4th instar larvae or
pupae of A. aegypti, respectively, at 0.25% concentration
after 24 h of exposure (Sundaravadivelan and Padmanab-
han 2014).
Nanopesticide formulations
There is great interest in the use of technologies such as
encapsulation and controlled release methods for the use of
pesticides. The scope for applying NPs and nanocapsules to
plants for agricultural use has been stressed by several
researchers (Pavel et al. 1999; Cotae and Creanga 2005;
Pavel and Creanga 2005; Joseph and Morrison 2006). The
formulations that contain NPs within the 100–250 nm size
range are made by numerous companies. A few employ
suspensions of nanoscale particles (nanoemulsions), which
can be either water or oil-based, and contain uniform
suspensions of pesticidal NPs in the range of 200–400 nm.
The emulsions can be easily incorporated into gels, creams,
liquids, and have multiple applications for preventative
measures, treatment, or preservation of the harvested
product.
One of the recent popular controlled releases of agro-
chemicals is the use of silica-based materials. Wen et al.
(2005) employed porous hollow silica NPs (PHSN) as
pesticide carriers to study the controlled release behavior of
avermectin pesticide. The PHSN carriers markedly delayed
the release of the pesticide, and they concluded that PHSNs
could be exploited in controlled pesticide delivery appli-
cation. As NPs have large surface areas, they can absorb
and bond other compounds easily, circulate more easily in
lepidopteran systems, and potentially be exploited for
pesticide development (Barik et al. 2008). Many terpene
compounds are reported to have antifeedant activity and
are highly volatile in nature. Formulations using certain
plant extracts in combination with nanosilica greatly
enhanced insecticidal activity and shelf life of the extracts
(Madhusudhanamurthy et al. 2013). Similar formulations
made with a-pinene and linalool combined with nanosilica
not only enhanced bioactivity of the plant pure chemicals
but also the stability of the formulation with higher zeta
potential, controlled release of the botanical compound,
and enhanced shelf life of the isolated botanicals (Mad-
husudhanamurthy et al. 2013). These formulations showed
good antifeedant activity against S. litura and A. janata
(Madhusudhanamurthy et al. 2013; Usha Rani et al. 2014).
These nanoformulations are easily dispersible, which was
confirmed from the dispersion studies. Shelf-life analysis
of nanoformulations with the above terpenes did not affect
the dispersion, size, zeta potential, or bioactivity of the
nanoformulations in up to 6 months of storage (Mad-
husudhanamurthy et al. 2013; Usha Rani et al. 2014). The
controlled release property of the formulation was affected
only when the compounds were stored for more than
6 months.
Nanopesticides are in various forms, such as particles
or in aqueous solution that form an aggregate with the
hydrophilic ‘‘head’’ regions in contact with the sur-
rounding solvent sequestering the hydrophobic single-tail
regions in the micelle center, and they can consist of
organic ingredients (e.g., a.i., polymers) and/or inorganic
ingredients (e.g., metal oxides). Nanoformulations are
like other common pesticide formulations, and they aid in
increasing the apparent solubility of a poorly soluble
active ingredient or in releasing the active ingredient in a
slow or targeted manner, thus protecting the active
ingredient against premature degradation. They are
expected to have significant impacts on the fate of active
ingredients. The existing knowledge of nanopesticides
does not allow us to fairly assess the advantages and
disadvantages of their use.
A new delivery system for pesticides in the form of
nanoformulation comprising the incorporation of A.
J Pest Sci (2018) 91:1–15 9
123
arborescens essential oil into solid lipid NPs (SLN) with
the high-pressure homogenization technique using Com-
pritol 888 ATO as lipid and Poloxamer 188 or Miranol
Ultra C32 as surfactants has become popular (Lai et al.
2006). It was found that the average diameter of A.
arborescens essential oil-loaded SLN did not change dur-
ing storage and increased slightly after spraying the SLN
dispersions. Interestingly, the rapid evaporation of the
essential oil was reduced due to SLN and indicates that the
SLN formulations are suitable carriers in agriculture.
Potential advantages described are the solubilization of
hydrophobic pesticides/herbicides thereby discounting the
use of toxic organic solvents.
It is important that the changes in method of synthesis of
NPs may cause changes in dimensions and shape, as well
as in the risks associated with the use of such materials.
There are differences in the activities of biologically or
eco-synthesized NPs and the normal or chemically syn-
thesized NPs and their effects on plants and arthropod
pests. There are several advantages of biologically syn-
thesized NPs over the chemically synthesized ones. Eco-
toxicological studies using Daphnia magna Straus
(Cladocera: Daphniidae) showed that the silver NPs
biosynthesized from the medicinal and aromatic plant
Piper betle L. (Piperales: Piperaceae) leaf extract showed
less toxicity than the silver NPs synthesized chemically.
These results revealed that the biosynthesized AgNPs are
environmentally safer due to the protein core shell formed
around the NPs during biosynthesis (Usha Rani and Raja-
sekharreddy 2011). Similar results were shown with pal-
ladium (Pd) and platinum (Pt) NPs biosynthesized with P.
betle extracts, indicating their eco-friendly characteristics
(Rajasekharreddy and Usha Rani 2014b). The application
of NPs in mammalian systems is more advanced compared
to their use in plants, which is still a relatively new concept
(Cifuentes et al. 2010; Wang et al. 2012).
Future perspectives
Number of publications and successfully explored exam-
ples show very strong research in this field and consider-
able confidence that nanopesticide-based formulations,
such as nanoemulsions, nanodispesions, and NPs have a
bright future and potential for developing safer and more
effective chemical pesticide formulations for pest control,
which potentially could result in revolutionary changes in
this field. However, due to potential toxicity concerns of
nanomaterials, which are not standardized yet, not well
understood, and not explored, this development will likely
go through strong scrutiny by international and national
safety regulators with requests for more research on
environmental and human impacts of these materials.
Nevertheless, despite the extensive research on plant-me-
diated synthesis of NPs for arthropod control, there is a gap
between theory and practical applications, especially on a
large-scale (Benelli 2015; Murugan et al. 2015b, c, d).
The process of nanomaterial synthesis is also important,
and the changes in method of synthesis may cause changes in
dimensions and shape, as well as in the risks associated with
the use of such materials. Therefore, risk assessment studies
are essential before the use of such materials, since there are
no specific guidelines to use these formulations on nano-
materials, so the toxic nature of these compounds to plants
and insects need to be analyzed. A great deal of work is still
needed on nanopesticide formulations before they become
more popular in pest management by combining analytical
techniques that can detect, characterize (e.g., through size,
size range, shape or nature, and surface properties), and
quantify the active ingredient and adjuvants emanating from
the formulations. Nanotechnology will make agriculture
eco-friendly and profitable by reducing the usage of crop
protection chemicals. Smart delivery of fertilizers, pesti-
cides, and growth regulators, including nanosensors for real-
time monitoring of soil conditions, crop growth, and pest and
disease attack, are made possible by the development of
nanodevices and products. There seems to be a bright future
for nanotechnology in the agricultural sector, just as in other
areas, though the progress is slow.
Author contributions
CGA and ND conceived and designed the paper. CGA,
NGK, GB, DL, URP, and ND contributed with different
sections on the manuscript.
Acknowledgements We would like to thank James Throne (USDA-
ARS) for his constructive comments on an earlier version of this
manuscript. DL acknowledges support from Grain Research Devel-
opment Corporation (Grants UA 000131 and UA 000151). GB is
supported by PROAPI (PRAF 2015) and University of Pisa,
Department of Agriculture, Food and Environment (Grant ID:
COFIN2015_22). URP expresses here acknowledgments to Jyothsna
Yasur for her support while preparing the manuscript and also to the
Ministry of Earth Sciences, New Delhi for the research grant related
with NPs. CGA would like to thank the General Secretariat for
Research and Technology for the Grants GSRT11-ROM-30-2-ET29
and 1422-BET-2013 and the Research Committee of the University of
Thessaly for the Grants ELKE-UTH-4198 and 4975. Funders had no
role in the study design, data collection and analysis, decision to
publish, or preparation of the manuscript. Mention of trade names or
commercial products in this publication is solely for the purpose of
providing specific information and does not imply recommendation or
endorsement by the University of Thessaly, Agricultural University of
Athens, University of Pisa, University of Adelaide, CSIR-Indian
Institute of Chemical Technology and French National Institute for
Agricultural Research.
10 J Pest Sci (2018) 91:1–15
123
Compliance with ethical standards
Conflict of interest The authors declare that they have no conflict of
interest.
Human and animal rights The research did not involve human
participants and/or animals.
Ethical approval This article does not contain any studies with
human participants performed by any of the authors.
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