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

athanassiou@agr.uth.gr

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

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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

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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

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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

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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

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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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