J Pest Sci (2018) 91:1–15 https://doi.org/10.1007/s10340-017-0898-0

REVIEW

Nanoparticles for pest control: current status and future perspectives

1 2 3,7 4 C. G. Athanassiou • N. G. Kavallieratos • G. Benelli • D. Losic • 5 6 P. Usha Rani • N. Desneux

Received: 3 October 2016 / Revised: 19 June 2017 / Accepted: 21 June 2017 / Published online: 21 August 2017 Ó Springer-Verlag GmbH Germany 2017

Abstract In the current paper, we reviewed the use of agents. Finally, the potentials in the use of NPs are briefly nanoparticles (NPs) in crop protection, emphasizing the illustrated and discussed. control of pests in the agricultural and urban environment. At the same time, we provide the framework on which the Keywords Nanotechnology Á Green synthesis Á technology of NPs is based and the various categories of Nanopesticides Á Nanotoxicity Á Nanoencapsulation Á NPs that are currently used for pest control. Apart from the Nanoinsecticides use of NPs as carriers of a broad category of active ingredients, including insecticides and pheromones, some Key message NPs can be used successfully as insecticides alone. More- over, several types of NPs are produced by natural • There is a knowledge gap on the use of nanoparticles in resource-based substances, which make them promising pest control. ‘‘green’’ alternatives to the use of traditional pest control • We reviewed the use of nanoparticles for insect control and the different categories of pests that can be controlled. Communicated by M. Traugott. • Nanoparticles should become important components in an IPM-based strategy in the agro-food and urban & C. G. Athanassiou [email protected] environment.

1 Laboratory of Entomology and Agricultural Zoology, Department of Agriculture, Crop Production and Rural Introduction Environment, University of Thessaly, Phytokou Str., 38446 N. Ionia, Magnesia, Greece Despite the fact that there are several available alternative 2 Laboratory of Agricultural Zoology and Entomology, Department of Crop Science, Agricultural University of methods, pest control is still largely based on the use of pes- Athens, 75 Iera Odos Str., 11855 Athens, Attica, Greece ticides, in the sense of organic chemical-based ingredients that 3 Department of Agriculture, Food and Environment, are applied on the crops, the commodity, or the urban envi- University of Pisa, Via del Borghetto 80, 56124 Pisa, Italy ronment. Even today, many of the registered pesticides are 4 neurotoxic, which means that their primary mode of action School of Chemical Engineering, The University of Adelaide, Adelaide, SA 5005, Australia interferes with the insects’ nervous system and may pose risks of mammals. Newer compounds, such as the insecticides that 5 Biology and Biotechnology Division, CSIR-Indian Institute of Chemical Technology, Tarnaka, Hyderabad 500007, India are adenosine triphosphate (ATP) disruptors or insect growth regulators (IGRs), have been introduced recently in the mar- 6 INRA (French National Institute for Agricultural Research), Universite´ Coˆte d’Azur, CNRS, UMR 1355-7254, Institut ket and have gradually reduced the use of neurotoxic com- Sophia Agrobiotech, 06903 Sophia Antipolis, France pounds, but there are still concerns about their environmental 7 The BioRobotics Institute, Scuola Superiore Sant’Anna, impact. In this regard, pesticide use has been related with Viale Rinaldo Piaggio 34, 56025 Pontedera, Pisa, Italy mammalian toxicity, environmental contamination, and 123 2 J Pest Sci (2018) 91:1–15 bioaccumulation. These variables, along with the increased relevant for their use in pesticide application, including toxi- frequency of resistance development by many insect species city. A broad variety of materials were synthesized or used to many of the currently used compounds, are major key from natural materials to make NPs in different forms and challenges in agriculture, and may considerably limit the chemical composition including metal, metal oxides, semi- active ingredients that are effective. To address these prob- conductor quantum dots (QDs), carbon, ceramics, silicates, lems, new pest control strategies are required through intro- lipids, polymers, proteins, dendrimers, and emulsions (Nie- duction of innovative pest-resistive concepts and advanced meyer and Doz 2001;Oskam2006;Puocietal.2008). Some technologies for pest management. common benefits of NP-based pesticide formulations include: Nanotechnology is emerging as a highly attractive research (a) increased solubility of water insoluble active ingredients, field toward achieving these goals, offering new methods for (b) increased stability of formulation, (c) elimination of toxic designing novel active ingredients with nanoscale dimen- organic solvents in comparison with conventionally used sions, as well as their formulation and delivery, which are pesticides, (d) capability for slow release of active ingredients, collectively referred to as ‘‘nanopesticides.’’ Nanopesticide (e) improved stability to prevent their early degradation, research, introduced relatively recently, is an emerging field (f) improved mobility and higher insecticidal activity due to that can be defined as application of nanotechnology for crop smaller particle size, and (g) larger surface area which is likely protection. This field compromises broad research aspects to extend their longevity (Sasson et al. 2007). including study of fundamental understanding of interaction This review presents the recent advances in the devel- of nanoscale materials and insects, formulation of the active opment of NP-based formulations on the basis of three ingredients into nanoemulsions and dispersions using existing major concepts: the improvement of conventional pesticide pesticides, development of new nanopesticide formulations formulations, the development of delivery systems and the using nanomaterials as active pesticide agents, or using these use of NPs as nanocarriers, and solid NPs used as active nanomaterials as nanocarriers for their delivery (Smith et al. pesticide agents. 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 Nanoparticles to improve pesticide formulations new advanced nano-based formulations that remain stable and active in the target environment (i.e., not heavily affected by Recently, a number of plant-synthesized NPs have been sun, heat, and rain), penetrate the target organism (insect), investigated for their efficacy against arthropod pests of resist defense of the pest, remain benign to plants and mam- economic importance, including moths (Roni et al. 2015), mals, be cost effective to formulate and manufacture, and beetles (Abduz Zahir et al. 2012), lice (e.g., Pediculus preferably possess a new mode of action (Smith et al. 2008; humanus capitis) (Jayaseelan et al. 2011), hard ticks (e.g., Benelli 2016a, b). Haemaphysalis bispinosa) (Abduz Zahir and Abdul Rahuman 2012), louse flies (e.g., Hippobosca maculata) (Jayaseelan et al. 2012), and mosquitoes (Benelli 2016a, b). Nanoparticles for pest control: definition, concepts, However, not surprisingly, the majority of research dealing and perspectives with nanosynthesis of insecticides focused on mosquito control. More than 100 research products were found in the Nanoparticles (NPs) can be defined as a subclass of ultrafine SCOPUS database using the keywords ‘‘plant nanoparticles particles with characteristic dimensions from 1 to 100 nm and mosquitoes’’ (Benelli 2016a). have properties that are not shared by non-nanoscale particles Most of currently used pesticides are poorly water sol- with the same chemical composition (Auffan et al. 2009). The uble molecules, and their formulations are based on basis of the 100-nm limit is the fact that unique properties that emulsifiable concentrates (ECs), oil-in-water (O/W) differentiate particles from the bulk material typically develop emulsions, or similar formulations that are variations of the at a critical size of under 100 nm. However, because other above (Knowles 2009). ECs usually consist of organic phenomena (e.g., transparency or turbidity, ultrafiltration, solvents that are expensive, flammable, and toxic, or a stable dispersion) that extend the upper limit are occasionally blend of surfactant emulsifiers to ensure spontaneous considered, the use of the prefix ‘‘nano’’ (‘‘ma9mo’’ in Greek, emulsification into water in the spray tank. O/W emulsions meaning small, dwarf) is accepted for dimensions smaller than do not have these shortcomings because they are based on 500 nm (Alema´netal.2007). The size, shape (spherical, rods, the removal of solvent and the introduction of a mixture of tubes, irregular), surface-to-volume ratio, crystal phase (crys- a non-ionic surfactant, block polymers, and polymeric talline, amorphous), and chemical composition (e.g., metallic, surfactants; nevertheless, one of the major drawbacks in carbon, inorganic, organic, polymeric) are key parameters their use is the fact that emulsification requires high-energy which define many outstanding properties of these materials input (Kah et al. 2013; Kah and Hofmann 2014). 123 J Pest Sci (2018) 91:1–15 3

To address these disadvantages, new formulations based et al. 2011). Plant cell walls have the remarkable capability on micro- and nanoemulsions were introduced with the of impeding the entry of NPs. In spite of this doubtful capability to provide NPs in sizes from 20 to 100 nm impact of nanomaterial application on plants, some of the (Tadros et al. 2004; Lawrence and Warisnoicharoen 2006; current studies focus on the phytotoxicity of NPs (Lee et al. Knowles 2009; Tomlin 2009; Song et al. 2009). Several 2010; Slomberg and Schoenfisch 2012) and the influence of microemulsion formulations are available on the market, NPs on plant development (Khodakovskaya et al. 2009; including plant growth regulators and systemic fungicides, Balalakshmi et al. 2017). Torney et al. (2007) reported that for broad-spectrum disease control in different types of NPs can effectively deliver biomolecules into plants, and target plants (Tomlin 2009; ObservatoryNano 2010). this idea has been expanded by other researchers for a Microemulsions are more stable than nanoemulsions, wider range of cases (Martin-Ortigosa et al. 2012a, b). The which require high-energy input that may be difficult to available reports indicate that plant cells can take up very scale up for commercial agrochemical production, or may small NPs (Yasur and Usha Rani 2013, 2015). not be practical for on-site preparation by the handlers The uptake efficiency and effects of various NPs on (e.g., high-shear stirring, high-pressure homogenizers, or growth and metabolic functions vary remarkably among ultrasound generators). Compared to other conventional plants and has been thoroughly tested. As carriers, NPs are formulations, microemulsions provide numerous advan- able to reach the plant internal systems easily and may tages including improved tank mix compatibility, improved cause significant changes to these systems. Rodriguez et al. stability, reduced low flammability, reduced handler toxi- (2011) noted that most of the available studies on phyto- city (due to low solvent content), and most importantly toxicity of NPs are based on germination and root elon- enhanced efficacy due to improved penetration or uptake gation, factors which cannot be always reliable indicators resulting from the high solubilizing power of surfactants to evaluate NP toxicity to plants. Khodakovskaya et al. (Green and Beestman 2007; Knowles 2009). However, (2009) revealed that carbon nanotubes have a positive there are certain disadvantages of these substrates, such as impact on tomato plants through an increase in seed ger- low content of active ingredients (\30%), high concen- mination and growth, and they suggested that these effects tration of surfactants (*20%), and the limited number of are due to the carbon nanotubes ability to penetrate the suitable surfactant systems (Lawrence and Waris- seed coat and enhance crucial water uptake. It has been noicharoen 2006). These limitations can be partially solved shown that NPs, such as nano-ZNO particles at certain by another formulation concept based on nanodispersion or optimum concentration, promote growth of seedlings of nanosuspension, where active ingredients of nanocrystals, mung bean, Vigna radiata (L.) R. Wilczek, and gram, or crystalline or amorphous NPs of 50 nm (prepared by Cicer arietinum L. (Mahajan et al. 2011). Treating castor specific procedure), create nanodispersions having similar seeds, Ricinus communis L., with silver NPs did not affect properties to solutions (Mu¨ller and Junghanns 2006). seed germination rate nor growth of lepidopteran insects on Interestingly, this approach is not widely applied yet, with the seeds (Yasur and Usha Rani 2013, 2015). Studies with only a few reported examples (triclosan and novaluron) transmission electron microscopy (TEM) of NP effects on (Zhang et al. 2008; Elek et al. 2010). plants confirmed their penetration into the cell organelles The development of sustainable release systems using and localization of the NPs at mitochondria or nucleolus in NPs could increase the performance and the efficiency of both plant and insect tissues, which suggests that they can pesticides and also might reduce their adverse environ- be used for targeted delivery of pesticides or fertilizers mental effects. Generally, NPs can easily penetrate into (Yasur and Usha Rani 2013, 2015). Plant-mediated syn- plant cells making them a ‘‘nanocarrier’’ transport system. thesis of NPs was confirmed by UV-visualization spec- They are able to deliver products accurately, as they are trophotometry, followed by scanning electron microscopy customized to transfer a particular biomolecule to the cell, (SEM) and/or transmission electron microscopy, energy- tissue, or organism when needed (Du et al. 2013). Several dispersive X-ray spectroscopy (EDX), Fourier transform inorganic nanomaterials with unique physical and chemical infrared spectroscopy (FTIR), and X-ray diffraction studies properties, such as metals, metal oxides, silica- and carbon- (XRD) (Rajan et al. 2015). based materials, and semiconductors, have been engineered for tracking or delivery purposes (Kunzmann et al. 2011). Nanodelivery vehicles can increase seed vigor, plant Pesticide delivery system using nanoparticles growth, and in some cases crop yield in addition to crop as nanocarriers protection from pests and diseases, while they can be also used for genetic manipulation (Kole et al. 2013). The Learning from drug delivery concepts introduced in med- small-sized NPs often enter plant cells through binding to a icine where NPs have been successfully used for delivery carrier protein, ion channels, or creating new pores (Rico of therapeutics for medical therapy, a similar concept was 123 4 J Pest Sci (2018) 91:1–15

Fig. 1 Schematic representation of different polymer nanoparticles hydrophobic or hydrophilic core (polymer micelles); and d entrapment for delivery of pesticides, a adsorption on nanoparticle; b attachment inside polymeric nanoparticle (prepared by DL) on nanoparticle by different linkers; c encapsulation inside polymeric developed for pest control, known as ‘‘pesticide delivery L. (Lamiales: Verbenaceae) oil (Abreu et al. 2012); system’’ (PDS) (Tsuji 2001). The aim is to make the active Catharanthus roseus extract (L.) G. Don (Pavunraj et al. ingredients available to a specified target at concentrations 2017) and juniper oil (Athanassiou et al. 2013). Nanode- and durations designed to accomplish the intended effect livery systems for pheromones (Bhagat et al. 2013; Hell- by maintenance of the fullest biological efficacy and mann et al. 2011; Trematerra et al. 2013) and various plant reduction of various harmful effects (Ghormade et al. extracts also have been proposed (e.g., capsaicin from chili 2011). Controlled delivery is particularly important to peppers, Bohua and Ziyong 2011; Lansiumamide B extract provide optimized release of necessary and sufficient from the seeds of Clausena lansium (Lour.) Skeels, Yin amounts of pesticides over a period of time to obtain the et al. 2012). maximum biological efficacy and to minimize potential Nanoporous materials particularly possess organized harmful effects (Tsuji 2001). The advantage of using NPs pore distributions and increased surface areas which as nanocarriers is in their ability to have high effective enhance the capacity of sorbents and enable incorporation loading due to the larger surface area, easy attachment of of functionality. This property provides better sensitivity in single and several different pesticide molecules, and a detection methods, and improved selectivity and yield in reasonably fast mass transfer to the target, i.e., insects’ catalyst-based synthesis (Appell and Jackson 2013). body. Pesticides, when encapsulated, are likely to have a Nanoencapsulation is another very important technique more gradual release over time, which requires their which can be utilized for safer handling of pesticides with application less often as compared with very highly con- less exposure to the environment. Carbon nanotubes were centrated and perhaps toxic initial applications followed by discovered in 1991. These are only a few nanometers in repeated applications. At the same time, NPs delay the loss diameter, but they can conduct electricity better than cop- in efficacy due to degradation. per and they are 100 times stronger than steel but only one- Several different concepts for loading of active pesticide sixth of its weight. This is one good example of the benefits molecules on NPs may include adsorption, covalent of nanomaterial application (Lok 2010). Among the vari- attachment mediated by different ligands, encapsulation, ous NPs available, silica-based NPs have generated interest and entrapment inside NP (Fig. 1). Controlled and slow as potential delivery agents of agrochemicals in plants. release of the active molecules can be achieved based on This is mainly due to their structural flexibility in forming degradation properties of the nanocarrier (e.g., polymer), NPs of various sizes and shapes, and also their ability to bonding of the ingredients to the material, and the envi- form pores for loading biomolecules (Campbell et al. 2011; ronmental conditions. The most attractive NPs that are Jang et al. 2013; Athanassiou et al. 2013). Two types of considered as carriers for delivery of pesticides are based engineered silica NPs have been described: solid and on polymers (soft NPs), synthetic silica, titania, alumina, mesoporous silica NPs (MSN) (Slomberg and Schoenfisch Ag, Cu, and natural minerals/clays with nanoscale dimen- 2012; Wanyika et al. 2012). MSNs are formed by a matrix sions (inorganic or solid NPs). Some common paradigms of well-ordered pores that allow high loading capacity of of insecticides explored using this nanotechnology molecules like proteins (Popat et al. 2011). Also, it is approach are essential oils, including neem oil (Anjali et al. possible to modify the surfaces of MSNs, which permits 2010; Xu et al. 2010; Jerobin et al. 2012); garlic essential the NP to be customized to specific experimental needs oil (Yang et al. 2009); Artemisia arborescens L. (Asterales: (Trewyn et al. 2007). MSNs also were used in the slow Asteraceae) essential oil (Lai et al. 2006); Lippia sidoides release of urea as a fertilizer in soil and water (Wanyika

123 J Pest Sci (2018) 91:1–15 5 et al. 2012). Gold plating of MSN surfaces increased NP nanocarriers is their protective function for application of density and, subsequently, the ability to pass through the phytochemicals (secondary metabolites) and essential oils plant cell wall upon bombardment, thus improving their which have stability problems, so this can increase their performance (Martin-Ortigosa et al. 2012b). The uptake cost effectiveness. In the case of essential oils, their and phytotoxicity of non-porous silica NPs in the seedlings chemical instability in the presence of air, light, moisture, of rice and roots of Arabidopsis also has been demonstrated and high temperatures that causes rapid evaporation and (Nair et al. 2011; Slomberg and Schoenfisch 2012). In this degradation of some active components is a major concern, regard, calcinated non-porous silica NPs could be trans- and their incorporation into a controlled release nanocarrier ported into roots of Arabidopsis thaliana (L.) Heynh. will prevent rapid evaporation and degradation, enhance (Brassicales: Brassicaceae) without causing any phytotoxic stability, and maintain the minimum effective dosage/ap- effects (Slomberg and Schoenfisch 2012). plication (Ghormade et al. 2011). NPs are important gene carriers in various types of Many types of polymers have been evaluated for plants, and they can be further utilized to effectively designing polymer NP formulations, which are similar to overcome transgenic silencing via controlling the copies those used in the pharmaceutical or cosmetic sectors, and function of DNA (Kumar et al. 2016). Also, NPs can consisting mainly of polyesters (e.g., poly-e-caprolactone mediate multigene transformation without involving the and polyethylene glycol (PEG)), polysaccharides (e.g., traditional building method of a complex carrier (Fu et al. chitosan, alginates, and starch), and recently biodegradable 2012; Martin-Ortigosa et al. 2012a). Torney et al. (2007) materials of biological origin such as beeswax, corn oil, or reported the efficient delivery of DNA and chemicals lecithin or cashew gum (Abreu et al. 2012; Nguyen et al. through silica NPs internalized in plant cells, with no 2012). Among them, polyethylene glycol-based amphi- specialized equipment. A 3-nm mesoporous silica NP philic copolymers are so far most attractive due to their (MSN) was successfully utilized for delivering DNA and biodegradability, easy processing, and well-explored chemicals into isolated plant cells (Barron 2007; Galbraith properties (Torchilin 2006; Shakil et al. 2010). 2007). DNA was introduced successfully in tobacco and The release studies of series of plant protection mole- corn plants using this technology (Torney et al. 2007). cules (mainly pesticides) from PEG polymer nanoformu- Green synthesis of protein-lipid conjugated Ag NPs using lations in water have shown significantly slower release Sterculia foetida L. (Malvales: Sterculiaceae) seed extract (several weeks) compared to commercial formulations, and its anti-proliferative activity against HeLa cancer cell including imidacloprid (Adak et al. 2012), thiamethoxam lines showed their biocompatibility and translocation into (Sarkar et al. 2012), carbofuran (Pankaj et al. 2012), thiram the HeLa cells (Rajasekharreddy and Usha Rani 2014a). (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- Polymer nanoparticles as nanocarriers cial products for the control of insects and nematodes (Loha et al. 2012; Pankaj et al. 2012). Yang et al. (2009) Polymer nanocarriers are based on polymer NPs, and they used essential oil from garlic loaded on polymer NPs include polymeric nanospheres and nanocapsules. Their coated with PEG for control of adults of the red flour attractiveness is based on flexibility to design a complex beetle, Tribolium castaneum (Herbst) (Coleoptera: Tene- drug delivery system including multiple pesticides with brionidae), with very good results. In fact, in that study, different mode of actions, scalable preparation, biocom- efficacy remained over 80% after 5 months due to the patibility, and biodegradability. The active molecules in controlled slow release of the active components, in com- polymer nanospheres are randomly distributed in a poly- parison with free garlic essential oil (11%). This indicated mer matrix in nanocapsules with a core–shell structure that the feasibility of PEG-coated NPs loaded with garlic can act as a reservoir for encapsulation of a hydrophobic essential oil for control of stored-product pests. drug (Torchilin 2006). Polymer nanocapsules, also known It is important to note that the greater efficacy of these as polymer micelles, provide advantages over larger cap- nanoformulations relative to the commercial formulations sules by having better stability of the spraying solution, was generally only noticeable over a relatively long period increased uptake, increased spraying surface, and reduced (i.e., 30 days) which is likely due to their slower release phytotoxicity owing to a more homogeneous distribution rather than to an increased uptake of the released pesticide that provides them with better protection. In both cases, by the target organisms. Some disadvantages of polymer- polymer NPs serve as a protective reservoir and diffusion- based nanoformulations are their very slow release (in controlled release carrier which can be controlled some cases), reduced environmental stability, higher pro- depending on degradation and permeability properties of duction cost, and high-energy preparation methods the polymer. Another important feature of polymer (Torchilin 2006). 123 6 J Pest Sci (2018) 91:1–15

Inorganic nanoparticles as nanocarriers slight (if any) increase in efficacy. At the same time, these rates are considered too high for ‘‘real-world’’ applications. Solid inorganic NPs have been intensively studied in the There are several studies that demonstrated the use of last two decades for the formulation of pharmaceuticals, as hollow silica NPs as carriers for the controlled release and they combine the advantages of nanoemulsions, liposomes, UV shielding of avermectin and validamycinis (Li et al. and polymer NPs, while simultaneously avoiding their 2006, 2007; Liu et al. 2006). The rate of release of these disadvantages by providing better stability, more control- molecules was influenced by temperature, pH, and shell lable release, higher loading, and simpler production thickness. The release profile of encapsulated avermectin resulting in lower cost (Dimetry and Hussein 2016; Benelli was shown to have a multistage pattern which was inter- 2016a). Hence, it is not surprising that this trend was used preted as being due to the release of active ingredient located for the development of advanced pesticide delivery sys- in different parts of the particles (i.e., external, in pore tems (Choy et al. 2007; Ghormade et al. 2011; Kim et al. channels, and in the internal core). The absence of phyto- 2012; Kah et al. 2013; Werdin-Gonzalez et al. 2016; Small toxicity was also demonstrated for several plants sprayed et al. 2016; Sujitha et al. 2017). with concentrations up to 3200 mg/l (Park et al. 2006). Silica NPs are among the most attractive inorganic NPs explored as nanocarriers for pesticide delivery, which include insecticides, growth promoters, fungicides, Using nanoparticles alone as pesticides biopesticides, and pheromones (Barik et al. 2008). Silicon has long been known to enhance plant tolerance to various NPs having insecticidal properties can be used not only as abiotic and biotic stresses, and silica NPs have therefore nanocarriers, but also as an active pesticide agent or naturally been suggested as potential candidates for biopesticide (Barik et al. 2008; Elango et al. 2016). Most increasing the control over a range of agricultural pests promising examples are based on amorphous nanosilica (Barik et al. 2008). Novel formulations based on silica NPs obtained from various natural sources like the shell wall of have been proposed recently for the slow release of phytoplankton, epidermis of vegetables, burnt pretreated chlorfenapyr and growth promoters with promising results rice hulls, straw at thermoelectric plants, and volcanic soil; (Mingming et al. 2013; Song et al. 2012). Field tests some of these materials have particle sizes that exceeds demonstrated that the insecticidal activity associated with 1 lm, but they have minute pores that are considerably silica NPs was twice as high as that of chlorfenapyr asso- smaller than 100 nm (Korunic 1998; Athanassiou et al. ciated with microparticles or without particles (Song et al. 2005; Barik et al. 2008). The silica NPs were physio-sor- 2012). The mechanism involved is different from the bed by the cuticular lipids disrupting the protective barrier insecticide formulations that have no NPs, and observed and thereby causing death of insects purely by physical higher efficacy is probably related to the sustained and means with a mode of action similar to that observed for slow release (i.e., over 10–20 weeks) providing high diatom particles used for protection of stored grain localized concentration over a long time. (Korunic 1998; Vayias and Athanassiou 2004; Barik et al. The potential of nanosilica to control insects during 2008; Kavallieratos et al. 2017). Application of NPs on the grain storage has been reported in recent works. For leaf and stem surface did not alter either photosynthesis or example, Debnath et al. (2011) reported higher insect respiration in several groups of horticultural and crop mortality from treatment with silica NPs (15–30 nm) than plants. They did not cause alteration of gene expression in with bulk silica (100–400 nm) confirming that NPs with insect trachea and were, thus, qualified for approval as a smaller size have higher efficacy. Furthermore, a study on nanobiopesticide. Use of amorphous silica as a influence of surface modification of silica NPs using dif- nanobiopesticide is considered safe for humans by World ferent coatings (hydrophobic, hydrophilic, or lipophilic) Health Organization (WHO). Debnath et al. (2011) repor- indicated a mechanical mode of action that could be ted that silica NPs caused 100% mortality in adults of the enhanced for smaller particles. This study indicated that rice weevil, Sitophilus oryzae (L.) (Coleoptera: Cur- silica NPs of the same size coated with 3-mercaptopropy- culionidae). Furthermore, surface charged modified ltriethoxysilane were more efficient than those coated with hydrophobic silica NPs (3–5 nm) were successfully used to hexamethyl disilazane for reasons, however, that are poorly control a range of agricultural insect pests and animal understood (Debnath et al. 2012). Also, in that work, the ectoparasites of veterinary importance (Ulrichs et al. 2006). application rates were generally comparable with those It was successfully applied as a thin film on seeds to recommended for commercially available diatomaceous decrease fungal growth and boost cereal germination earths (0.5–2 g/kg of grain), and hence the additional costs (Robinson and Salejova-Zadrazilova 2010). Therefore, involved in engineering NPs may not be justified by the nanosilica particles have promising applications for control

123 J Pest Sci (2018) 91:1–15 7 of stored grain and household pests, animal parasites, and TNP, mixed as dusts with rice did kill adults of S. fungi, and worms. 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 Silver and other mineral-based nanoparticles 93% adult mortality (Goswami et al. 2010). Still, 2000 ppm should be considered as a high application Like other NP categories, metal-based NPs can be com- concentration. 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. Paradigms of nanoparticle use for pest control 2008; Werdin Gonza´lez et al. 2014; Patil et al. 2016). However, several previous research efforts have been Apart from stored-product pests, nanomaterials have also conducted on various metal nanomaterials that exhibit been tested for control of agricultural pests. For example, insecticidal properties themselves in order to enhance the AgNP dust, stabilized with polyvinyl pyrrolidone, was potential tools for alternative and effective control of applied to R. communis leaves for control of castor semi- agricultural or stored-product pests but also of pests that looper, Achaea janata (L.) (Lepidoptera: Noctuidae), and are related with humans’ and animals’ health. These the oriental leafworm moth, Spodoptera litura (F.) (Lepi- materials have been synthesized either exclusively chemi- doptera: Noctuidae). It was found that AgNPs negatively cally or by involving living organisms (Dubey et al. 2009). influenced the growth (i.e., larval weight and period of Nanomaterials of the former category that have shown development, pupal weight, and adult weight) of both insecticidal efficacy are aluminum oxide (ANP) or nanos- species as a result of the physiological changes in the body tructured alumina (NSA) (Al2O3), zinc oxide (ZNP) (ZnO), of the insects due to the presence of NPs (Yasur and Usha titanium oxide (TNP) (TiO2), and silver NPs (AgNPs). For Rani 2015). There are also several recent paradigms of example, Ki et al. (2007) found almost complete mortality successful implementation of NPs for this use (Patil et al. of the case-bearing clothes moth, Tinea pellionella (L.) 2016; Nayak et al. 2016; Benelli 2016a; Lee et al. 2017). (Lepidoptera: Tineidae), larvae in wool fibers treated with The progress in chemistry, but also consumers’ and 20 ppm of nanosilver colloid (SNSE, sulfur nanosilver environmental concerns or objections to the use of syn- ethanol-based colloid) 14 days after exposure and consid- thetic materials, propelled scientists to find alternative erable reduction of the weight loss of the treated fiber methods of production of nanomaterials, so called ‘‘green compared with the controls. Stadler et al. (2009) reported synthesis’’ of metal NPs (Benelli and Lukehart 2017). The complete mortality of R. dominica and S. oryzae adults in idea of green synthesis is based on the fact that various wheat treated with 1000 ppm of NSA dust after 9 days of organisms are capable of generating non-organic materials exposure and approximately 95% mortality after only (Simkiss and Wilbur 1989). Microorganisms, such as 3 days of exposure. Furthermore, NSA that was produced bacteria, actinomycetes, fungi, yeasts, and viruses, but also by combustion of glycine and aluminum nitrate applied as plant extracts have been used for the synthesis of metal dust on wheat at doses ranging from 62.5 to 1000 ppm (silver, gold, platinum, palladium, titanium, and zirconium) caused[94% mortality of S. oryzae adults after 15 days of NPs (Dubey et al. 2009; Narayanan and Sakthivel 2010). exposure at 57 and 75% relative humidity (Stadler et al. Recent research efforts point out the potential of the green 2012). Nevertheless, the efficacy of this NSA for control of synthesis of metal NPs, chiefly AgNPs, for use against a R. dominica adults resulted in lower overall mortality wide spectrum of noxious pest species either in the labo- levels than for S. oryzae. Similar results were obtained ratory or in the field. For example, Jayaseelan et al. (2011) when three novel NSA dusts, based on chemical solution reported that AgNPs synthesized by leaf aqueous extract of methods, were applied on wheat for control of R. dominica Tinospora cordifolia (Thunb.) Miers (Ranunculales: and S. oryzae (Buteler et al. 2015). The mode of action of Menispermaceae) caused complete mortality of the head these dusts is based on the absorption of epicuticular lipids louse, P. humanus capitis De Geer (Phthiraptera: Pedicul- through capillarity, causing death due to dehydration idae) adults after 1 h of exposure at 25 mg/l. (Stadler et al. 2012; Buteler et al. 2015). The efficacy of Regarding mosquito control, most of the research has NSAs, however, depends on their individual physical focused on larvicidal and pupicidal activity of NPs against characteristics, i.e., particle size, particle morphology, and the malaria vector Anopheles stephensi Liston (Diptera: surface area, but also on other biotic and abiotic factors Culicidae), the filariasis vector Culex quinquefasciatus Say such as target species, dose, exposure interval, and relative (Diptera: Culicidae), and the arbovirus vectors Aedes humidity (Stadler et al. 2012; Buteler et al. 2015). Contrary aegypti (Linnaeus in Hasselquist) and Aedes albopictus to results for NSA, the application of other NPs, i.e., ZNP (Skuse) (Diptera: Culicidae). In several cases, the NPs’ 123 8 J Pest Sci (2018) 91:1–15 toxicity against neglected mosquito vectors, such as aegypti L. (Diptera: Culicidae) after 48 h of exposure at Anopheles subpictus (Grassi) (Diptera: Culicidae) and 1000 ppm (Suresh et al. 2014). In a field test, Dinesh et al. Culex tritaeniorhynchus Giles (Diptera: Culicidae), has (2015) showed that the AgNPs synthesized by leaf aqueous been also assessed (Govindarajan and Benelli 2016). As a extract of Aloe vera (L.) Burm.f. (Asparagales: Xanthor- general trend, plant-synthesized NPs showed promising rhoeaceae) resulted in an overall reduction of 74.5, 86.6, activity against young instars of mosquito vectors, with the and 97.7% after 24, 48, and 72 h of application in water majority of LC50 values ranging from 1 to 30 ppm. Among reservoirs, respectively, of 1st–4th instar A. stephensi lar- the different tested species, C. quinquefasciatus larvae and vae. Similarly, Suresh et al. (2015) reported 47.6, 76.7 and pupae were the most resistant to the toxic activity of plant- 100% mortality of A. aegypti larvae 24, 48, and 72 h, synthesized NPs (Benelli 2016a). However, there has been respectively, after application of AgNPs synthesized by little effort to shed light on the toxicity mecha- leaf aqueous extract of Phyllanthus niruri L. (Mal- nism(s) leading to larval and pupal death in mosquito lar- pighiales: Phyllanthaceae). Concerning adulticidal toxicity, vae and pupae exposed to green-synthesized NPs. It has only a few records are available. Silver NPs synthesized been hypothesized that the biotoxicity against mosquito using Feronia elephantum Correˆa (Sapindales: Rutaceae) young instars may be related to the ability of NPs to pen- leaf extract were toxic to adults of A. stephensi, A. aegypti, etrate through the exoskeleton. In the intracellular space, and C. quinquefasciatus, with LD50 values ranging from NPs can bind to sulfur from proteins or to phosphorus from 18.041 to 21.798 lg/ml (Veerakumar and Govindarajan DNA, leading to the rapid denaturation of organelles and 2014). Silver NPs biosynthesized using Heliotropium enzymes. Subsequently, the decrease in membrane per- indicum L. (Eudicotidae: Boraginaceae) leaf extract have meability and disturbance in proton motive force may been evaluated for control of adults of A. stephensi, A. cause loss of cellular function and cell death (Subramaniam aegypti, and C. quinquefasciatus, and the maximum effi- et al. 2015). In these studies, the residual toxicity of metal cacy has been observed against A. stephensi ions against mosquito young instars had little role because (LD50 = 26.712 lg/ml) (Veerakumar et al. 2014). Silver UV–Vis spectrophotometry results highlighted peak satu- NPs prepared using neem leaf extract were toxic to C. ration after 60, 120, or 180 min, indicating complete quinquefasciatus adults, with LC50 of 0.53 ppm calculated reduction of metal ions (Murugan et al. 2015a). after 4 h of exposure (Soni and Prakash 2014). Phyllanthus Furthermore, plant-synthesized NPs showed promising niruri-synthesized silver NPs tested against A. aegypti activity as ovicides and adulticides. In experiments con- adults resulted in an LC50 of 6.68 (Suresh et al. 2015). ducted with A. stephensi, A. aegypti, and C. quinquefas- Mimusops elengi L. (Ericales: Sapotaceae)-synthesized ciatus, egg hatchability was reduced by 100% after a single silver NPs resulted in LC50 values of 13.7 ppm against A. exposure to 30 ppm of Sargassum muticum-synthesized stephensi and 14.7 ppm against A. albopictus (Subrama- silver NPs (Madhiyazhagan et al. 2015). The toxicity niam et al. 2015). Recently, it has been reported that a mechanism(s) exerted by silver NPs on mosquito eggs is single exposure to doses ranging from 100 to 500 ppm of currently unknown. Similar results were obtained when Hypnea musciformis (Wolfen) (Ericales: Cystocloniaceae)- larvae of the mosquitoes A. subpictus and C. quinquefas- fabricated silver NPs greatly reduced A. aegypti longevity ciatus were exposed in 20 mg/l AgNP solution for 24 h. in both sexes, as well as female fecundity (Roni et al. Also, 100% larval mortality of A. subpictus and C. quin- 2015). Another common pest that is associated with public quefasciatus was recorded after 24 h of exposure to AgNPs health issues, the housefly, Musca domestica L. (Diptera: synthesized by leaf aqueous extract of Mimosa pudica L. Muscidae), was treated at the adult stage with 10 ml/l of (Fabales: Fabaceae) at 25 mg/l (Marimuthu et al. 2011). In AgNPs synthesized by leaf aqueous extract of Manilkara the same study, it was found that 89% of the exposed zapota (L.) P. Royen (Ericales: Sapotaceae) and was larvae of the tick Rhipicephalus microplus Canestrini completely suppressed after 4 h of exposure (Kamaraj (Acari: Ixodidae) were dead when exposed for 24 h in et al. 2012). The cotton bollworm, Helicoverpa armigera 20 mg/l of the same solution. Similarly, AgNPs synthe- (Hu¨bner) (Lepidoptera: Noctuidae), was found to be very sized by leaf aqueous extract of Annona squamosa L. susceptible to AgNPs synthesized by leaf aqueous extract (Magnoliales: Annonaceae) resulted in 100% mortality of of Euphorbia hirta L. (Malpighiales: Euphorbiaceae) since pupae or 1st–4th instar larvae of C. quinquefasciatus and all larval instars and pupae exhibited high mortality levels 100, 98, and 89% mortality of 1st–3rd instar larvae, 4th (C80%) after only 4 days exposure in cotton, Gossypium instar larvae, and pupae of Anopheles stephensi Liston hirsutum L. (Malvales: Malvaceae), leaves that had been (Diptera: Culicidae), respectively, at 10 ppm (Arjunan treated with the NPs at 10 ppm (Durga Devi et al. 2014). et al. 2012). AgNPs synthesized by root aqueous extract of Apart from terrestrial plants, marine plants have been used Delphinium denudatum Wall (Ranunculales: Ranuncu- for the synthesis of metal NPs for control of insect pest laceae) caused 100% mortality of 2nd instar larvae of A. species that impact public health or agriculture. For 123 J Pest Sci (2018) 91:1–15 9 example, Vinayaga Moorthi et al. (2015) reported that measures, treatment, or preservation of the harvested AgNPs synthesized by aqueous extract of Sargassum product. muticum (Yendo) Fensholt (Fucales: Sargassaceae), origi- One of the recent popular controlled releases of agro- nally collected from the Gulf of Mannar (India), caused chemicals is the use of silica-based materials. Wen et al. physiological and anatomical abnormalities in the body of (2005) employed porous hollow silica NPs (PHSN) as 4th instar larvae of the common castor, Ariadne merione pesticide carriers to study the controlled release behavior of (Cramer) (Lepidoptera: Nymphalidae). Similarly, Murugan avermectin pesticide. The PHSN carriers markedly delayed et al. (2015c) showed that AgNPs synthesized by aqueous the release of the pesticide, and they concluded that PHSNs extract of Caulerpa scalpelliformis (R. Brown ex Turner) could be exploited in controlled pesticide delivery appli- C. Agardh (Bryopsidales: Caulerpaceae) were highly toxic cation. As NPs have large surface areas, they can absorb to 1st–4th instar larvae of C. quinquefasciatus causing and bond other compounds easily, circulate more easily in C80% mortality at 10 ppm. In the same study, the authors lepidopteran systems, and potentially be exploited for suggested that C. scalpelliformis AgNPs exhibit synergistic pesticide development (Barik et al. 2008). Many terpene effect with Mesocyclops longisetus (Thie´baud) (Cy- compounds are reported to have antifeedant activity and clopoida: Cyclopidae) as a novel biological control strat- are highly volatile in nature. Formulations using certain egy against larvae of C. quinquefasciatus. The plant extracts in combination with nanosilica greatly mycosynthesis of metal NPs has also revealed interesting enhanced insecticidal activity and shelf life of the extracts prospects for the management of certain insect pest species (Madhusudhanamurthy et al. 2013). Similar formulations (Amerasan et al. 2016). According to Salunkhe et al. made with a-pinene and linalool combined with nanosilica (2011), AgNPs synthesized by the filamentous fungus not only enhanced bioactivity of the plant pure chemicals Cochliobolus lunatus R. R. Nelson and Haasis (Pleospo- but also the stability of the formulation with higher zeta rales: Pleosporaceae) resulted in complete mortality of potential, controlled release of the botanical compound, 2nd–4th instar larvae of A. aegypti and A. stephensi at 5 or and enhanced shelf life of the isolated botanicals (Mad- 10 ppm after 24 h of exposure. Another fungus, husudhanamurthy et al. 2013). These formulations showed Chrysosporium tropicum J. W. Carmich. (Onygenales: good antifeedant activity against S. litura and A. janata Onygenaceae), has been used for the synthesis of AgNPs (Madhusudhanamurthy et al. 2013; Usha Rani et al. 2014). and gold NPs (AuNPs) which were highly toxic, causing These nanoformulations are easily dispersible, which was 100% mortality, to the 2nd instar after 1 h of exposure and confirmed from the dispersion studies. Shelf-life analysis the 1st instar after 24 h of exposure, respectively (Soni and of nanoformulations with the above terpenes did not affect Prakash 2012). AgNPs synthesized by extracellular filtrate the dispersion, size, zeta potential, or bioactivity of the of the entomopathogenic fungus Trichoderma harzianum nanoformulations in up to 6 months of storage (Mad- Rifai (Hypocreales: Hypocreaceae) resulted in 92, 96, and husudhanamurthy et al. 2013; Usha Rani et al. 2014). The 100% mortality of 1st, 2nd, and 3rd–4th instar larvae or controlled release property of the formulation was affected pupae of A. aegypti, respectively, at 0.25% concentration only when the compounds were stored for more than after 24 h of exposure (Sundaravadivelan and Padmanab- 6 months. han 2014). 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- Nanopesticide formulations rounding solvent sequestering the hydrophobic single-tail regions in the micelle center, and they can consist of There is great interest in the use of technologies such as organic ingredients (e.g., a.i., polymers) and/or inorganic encapsulation and controlled release methods for the use of ingredients (e.g., metal oxides). Nanoformulations are pesticides. The scope for applying NPs and nanocapsules to like other common pesticide formulations, and they aid in plants for agricultural use has been stressed by several increasing the apparent solubility of a poorly soluble researchers (Pavel et al. 1999; Cotae and Creanga 2005; active ingredient or in releasing the active ingredient in a Pavel and Creanga 2005; Joseph and Morrison 2006). The slow or targeted manner, thus protecting the active formulations that contain NPs within the 100–250 nm size ingredient against premature degradation. They are range are made by numerous companies. A few employ expected to have significant impacts on the fate of active suspensions of nanoscale particles (nanoemulsions), which ingredients. The existing knowledge of nanopesticides can be either water or oil-based, and contain uniform does not allow us to fairly assess the advantages and suspensions of pesticidal NPs in the range of 200–400 nm. disadvantages of their use. The emulsions can be easily incorporated into gels, creams, A new delivery system for pesticides in the form of liquids, and have multiple applications for preventative nanoformulation comprising the incorporation of A. 123 10 J Pest Sci (2018) 91:1–15 arborescens essential oil into solid lipid NPs (SLN) with environmental and human impacts of these materials. the high-pressure homogenization technique using Com- Nevertheless, despite the extensive research on plant-me- pritol 888 ATO as lipid and Poloxamer 188 or Miranol diated synthesis of NPs for arthropod control, there is a gap Ultra C32 as surfactants has become popular (Lai et al. between theory and practical applications, especially on a 2006). It was found that the average diameter of A. large-scale (Benelli 2015; Murugan et al. 2015b, c, d). arborescens essential oil-loaded SLN did not change dur- The process of nanomaterial synthesis is also important, ing storage and increased slightly after spraying the SLN and the changes in method of synthesis may cause changes in dispersions. Interestingly, the rapid evaporation of the dimensions and shape, as well as in the risks associated with essential oil was reduced due to SLN and indicates that the the use of such materials. Therefore, risk assessment studies SLN formulations are suitable carriers in agriculture. are essential before the use of such materials, since there are Potential advantages described are the solubilization of no specific guidelines to use these formulations on nano- hydrophobic pesticides/herbicides thereby discounting the materials, so the toxic nature of these compounds to plants use of toxic organic solvents. and insects need to be analyzed. A great deal of work is still It is important that the changes in method of synthesis of needed on nanopesticide formulations before they become NPs may cause changes in dimensions and shape, as well more popular in pest management by combining analytical as in the risks associated with the use of such materials. techniques that can detect, characterize (e.g., through size, There are differences in the activities of biologically or size range, shape or nature, and surface properties), and eco-synthesized NPs and the normal or chemically syn- quantify the active ingredient and adjuvants emanating from thesized NPs and their effects on plants and arthropod the formulations. Nanotechnology will make agriculture pests. There are several advantages of biologically syn- eco-friendly and profitable by reducing the usage of crop thesized NPs over the chemically synthesized ones. Eco- protection chemicals. Smart delivery of fertilizers, pesti- toxicological studies using Daphnia magna Straus cides, and growth regulators, including nanosensors for real- (Cladocera: Daphniidae) showed that the silver NPs time monitoring of soil conditions, crop growth, and pest and biosynthesized from the medicinal and aromatic plant disease attack, are made possible by the development of Piper betle L. (Piperales: Piperaceae) leaf extract showed nanodevices and products. There seems to be a bright future less toxicity than the silver NPs synthesized chemically. for nanotechnology in the agricultural sector, just as in other These results revealed that the biosynthesized AgNPs are areas, though the progress is slow. 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- Author contributions ladium (Pd) and platinum (Pt) NPs biosynthesized with P. betle extracts, indicating their eco-friendly characteristics CGA and ND conceived and designed the paper. CGA, (Rajasekharreddy and Usha Rani 2014b). The application NGK, GB, DL, URP, and ND contributed with different of NPs in mammalian systems is more advanced compared sections on the manuscript. to their use in plants, which is still a relatively new concept (Cifuentes et al. 2010; Wang et al. 2012). 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 Future perspectives supported by PROAPI (PRAF 2015) and University of Pisa, Department of Agriculture, Food and Environment (Grant ID: Number of publications and successfully explored exam- COFIN2015_22). URP expresses here acknowledgments to Jyothsna Yasur for her support while preparing the manuscript and also to the ples show very strong research in this field and consider- Ministry of Earth Sciences, New Delhi for the research grant related able confidence that nanopesticide-based formulations, with NPs. CGA would like to thank the General Secretariat for such as nanoemulsions, nanodispesions, and NPs have a Research and Technology for the Grants GSRT11-ROM-30-2-ET29 bright future and potential for developing safer and more and 1422-BET-2013 and the Research Committee of the University of Thessaly for the Grants ELKE-UTH-4198 and 4975. Funders had no effective chemical pesticide formulations for pest control, role in the study design, data collection and analysis, decision to which potentially could result in revolutionary changes in publish, or preparation of the manuscript. Mention of trade names or this field. However, due to potential toxicity concerns of commercial products in this publication is solely for the purpose of nanomaterials, which are not standardized yet, not well providing specific information and does not imply recommendation or endorsement by the University of Thessaly, Agricultural University of understood, and not explored, this development will likely Athens, University of Pisa, University of Adelaide, CSIR-Indian go through strong scrutiny by international and national Institute of Chemical Technology and French National Institute for safety regulators with requests for more research on Agricultural Research.

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