Journal of Environmental Management xxx (2016) 1e13

Contents lists available at ScienceDirect

Journal of Environmental Management

journal homepage: www.elsevier.com/locate/jenvman

Review

Budding trends in integrated pest management using advanced

micro- and nano-materials: Challenges and perspectives
Neha Khandelwal a, Ranjit S. Barbole a, Shashwat S. Banerjee b, Govind P. Chate b,
Ankush V. Biradar c, Jayant J. Khandare b, d, **, Ashok P. Giri a, *
a
Plant Molecular Biology, Biochemical Sciences Division, CSIR-National Chemical Laboratory, Pune 411008, Maharashtra, India
b
Maharashtra Institute of Medical Education and Research (MIMER) Medical College, Talegaon Dabhade, Dist Pune 410507, India
c
Inorganic Material and Catalysis Division, CSIR-Central Salt and Marine Chemical Research Institute, Bhavnagar 364002, Gujarat, India
d
Maharashtra Institute of Pharmacy, MIT Campus, Pune 411038, Maharashtra, India

a r t i c l e i n f o a b s t r a c t

Article history: One of the most vital supports to sustain human life on the planet earth is the agriculture system that has
Received 5 July 2016 been constantly challenged in terms of yield. Crop losses due to insect pest attack even after excessive
Received in revised form use of chemical pesticides, are major concerns for humanity and environment protection. By the virtue of
15 September 2016
unique properties possessed by micro and nano-structures, their implementation in Agri-biotechnology
Accepted 21 September 2016
Available online xxx
is largely anticipated. Hence, traditional pest management strategies are now forestalling the potential of
micro and nanotechnology as an effective and viable approach to alleviate problems pertaining to pest
control. These technological innovations hold promise to contribute enhanced productivity by providing
Keywords:
Micro and nanotechnology
novel agrochemical agents and delivery systems. Application of these systems engages to achieve: i)
Pest management control release of agrochemicals, ii) site-targeted delivery of active ingredients to manage specific pests,
Bioactives iii) reduced pesticide use, iv) detection of chemical residues, v) pesticide degradation, vi) nucleic acid
Biopesticides delivery and vii) to mitigate post-harvest damage. Applications of micro and nano-technology are still
Controlled delivery marginal owing to the perception of low economic returns, stringent regulatory issues involving safety
Formulations assessment and public awareness over their uses. In this review, we highlight the potential application of
micro and nano-materials with a major focus on effective pest management strategies including safe
handling of pesticides.
© 2016 Elsevier Ltd. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
2. Interaction of NPs with insect physiological status: an essential and important aspect remained unexplored . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
3. Rationales for micro and nano-biotechnological approach inpest management . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
3.1. Microbe-derived bioactives . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
3.2. Plant derived products and their application . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
3.3. Nucleic acid delivery . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
4. Reinforcing nano or micro based pesticides: techniques and applications . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
4.1. Micro/nanoemulsion formulations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
4.2. Nanoparticles as advanced delivery systems . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
4.3. Delivery via adsorption/immobilization . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
4.4. Delivery via encapsulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00

* Corresponding author. Plant Molecular Biology, Biochemical Sciences Division,

CSIR-National Chemical Laboratory, Pune 411008, Maharashtra, India.
** Corresponding author. Maharashtra Institute of Medical Education and
Research (MIMER) Medical College, Talegaon Dabhade, Dist Pune 410507, India.
E-mail addresses: jayant.khandare@mippune.edu.in (J.J. Khandare), ap.giri@ncl.
res.in (A.P. Giri).

http://dx.doi.org/10.1016/j.jenvman.2016.09.071
0301-4797/© 2016 Elsevier Ltd. All rights reserved.

Please cite this article in press as: Khandelwal, N., et al., Budding trends in integrated pest management using advanced micro- and nano-
materials: Challenges and perspectives, Journal of Environmental Management (2016), http://dx.doi.org/10.1016/j.jenvman.2016.09.071
2 N. Khandelwal et al. / Journal of Environmental Management xxx (2016) 1e13

4.5. Interaction via surface functionalization . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00

4.6. Inorganic micro and nano-pesticide delivery systems . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
4.7. Advance polymeric delivery systems in pest management . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
5. Other applications . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
5.1. Detection of pesticide residue . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
5.2. Pesticide degradation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
6. Conclusions and future perspective . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00

1. Introduction adsorption or conjugation. This shall also provide benefits of safe

handling of chemical pesticides by achieving precise and targeted
A significant proportion of a nation's economy relies on its delivery. Application of insect controlling active agents in the field
agriculture and also vitally contributes to the world's food basket. suffers from fast evaporation, runoff, and UV degradation. Towards
Constantly expanding population coupled with changing environ- this, identification of MNP based delivery systems are the key as
mental conditions exerts pressure on agriculture to augment food they can offer: (i) enhanced activity against a wide spectrum of
production in order to satiate a greater demand of food supply pests, (ii) greater stability and retention in external environmental
(Godfray et al., 2010; McClung, 2014). The advent of synthetic condition and (iii) improved uptake (Glare et al., 2012). Further-
pesticides and fertilizers, the major contributors to the green rev- more, these tools are anticipated to enhance the field conditions by
olution, has indeed brought about transformational change in the reducing pest burden and mediating ‘smart’ delivery of active in-
agriculture sector. These strategies have paved their way in modern gredients in terms of targeted and controlled release of agro-
agriculture due to the lack of sufficient inherent quality of the crop chemicals and biological agents. Other advantages include their use
plants in sustaining environmental stresses, e.g. pest invasion. as nanosensors-sensing chemical residues, as nanocides, in
Since 1940 synthetic pesticides provided an effective solution to reducing pesticide use, facilitating pesticide degradation, and assist
control pest populations on crop plants. Losses due to the insect nucleic acid transfer targeted against insects (Fig. 2). Taken
pests are estimated to be 27e42% on crops after application of together, implementing sustainable biotechnological approaches
synthetic pesticides, as opposed to >83% losses in the untreated with the application of novel materials anticipates a paradigm shift
crops (Oerke and Dehne, 2004). However, in the due course of time, in global crop protection.
several insects have developed resistance to numerous pesticides In the following sections, we focus on cataloguing developments
(Dawkar et al., 2013). Further, excessive use of chemical pesticides in advanced micro and nano-based pest management strategies
(>2 million tons/year) has caused detrimental effects on the that may be suited for agronomical applications. In addition, our
ecosystem raising concerns to safeguard crops in an eco-friendly attempt was to cite challenges and recent advances in the bur-
manner (Ko € hler and Tribskorn, 2013; Van Den Bosch et al., 2011). geoning use of active ingredients by exploiting unique properties of
Thus to address these challenges, ‘integrated biotechnological ap- novel materials towards pest control. For the interest of the readers,
proaches’ and ‘sustainable intensification techniques’ are being a brief section on the application of nanoparticles as residue
explored (Tilman et al., 2011). An adaptation of biotechnological detection and pesticide degradation have also been included from
approaches to suppress pest populations involves modification of the perspective of environmental concern.
the living organisms and their bioactives. Towards this, transgenic
plants expressing insecticidal compounds have captured significant 2. Interaction of NPs with insect physiological status: an
attention around the globe. A classical example is the genetically essential and important aspect remained unexplored
engineered crop plants expressing cry toxin(s) of Bacillus thur-
ingiensis (Romeis et al., 2006). Development of transgenic plants In line with the focus of the review, control of agricultural pests
further offers gene-pyramiding by expressing proteins with a by nano-biotechnological means offer unprecedented advantages.
different mode of actions or by domain swapping to maximize ef- Most of the devastating agricultural pests belong to two major
ficacy on the target insect pests (Dunse et al., 2010; Carrie re et al., classes named Lepidoptera and Coleoptera, responsible for major
2015). Although, genetic manipulation imparts an excellent op- losses of field crops and stored grains. Herbivore insects depending
portunity to develop improved biopesticides, its application has on their feeding spectrum are divided into ‘generalists’ that feed on
been limited due to the stringent regulatory guidelines and public a variety of plants belonging to different families and ‘specialists’
acceptance over their use. In addition, various natural compounds that are confined to a single species of plant. In this way different
have been identified as potent deterrents, growth inhibitors, and insects have evolved distinct feeding habits which further deter-
toxins against insect pests in vitro. But substantial studies related to mine their physiological status that varies with the diet composi-
their field applications are lacking due to various environmental tion. Studies have revealed that a particular insect possesses the
and other constraints. This has generated an immediate require- capability to modify its biochemical composition when fed on
ment to harness an alternative technology that can offer eco- different diets that enables them to detoxify plant defensive com-
friendly, cost-effective, and sustainable solutions towards pest pounds while providing better opportunity for the utilization of
control. nutrients (Dawkar et al., 2013; Stam et al., 2014). This presents a
Advancements in material science has offered flexible processes challenging prospect to devise a sustainable and targeted strategy
to design varying size of micro and nanostructures yielding desired for the control of particular pest population in the different envi-
features (Fig. 1). Industrial application of these materials reveals ronment and crops.
their innumerable advantages in various facets of science including Applied technology of MNPs in the pest management has been
agriculture. Micro and nanoparticles (MNPs) if applied prudently gathering attention across the globe for their wide spectrum of
can help to leverage biotechnological expedients via encapsulation, tunable physico-chemical properties. Despite the advantages

Please cite this article in press as: Khandelwal, N., et al., Budding trends in integrated pest management using advanced micro- and nano-
materials: Challenges and perspectives, Journal of Environmental Management (2016), http://dx.doi.org/10.1016/j.jenvman.2016.09.071
 N. Khandelwal et al. / Journal of Environmental Management xxx (2016) 1e13 3

Fig. 1. Representation of size range of different types of micro and nanoparticles.

reducing condition of the gut environment. Ingestion of plant

allelochemicals that generates reactive oxygen species can induce
oxidative stress in the insects upon feeding. However, insects have
developed mechanism to evade the plant defense system for
instance, Manduca sexta can maintain reducing condition in midgut
by the secretion of antioxidants (Chapman et al., 2013).
The exposure of nanoparticles (NPs) to oxidation-reduction
state may challenge their stability and of immobilized protein,
which in principle may impact the protein-protein interaction and
hence efficacy in the feeding insects. Metallic NPs such as Silver
(Ag) or Gold (Au) are considered as redox species requiring the
evaluation of their redox properties and reactivity in physiological
conditions. Exposure of insects to Ag Nps has shown to induce
oxidative stress, which was thwarted by the enhanced production
of antioxidant enzymes such as superoxide dismutase, peroxidases
and catalases (Yasur and Rani, 2015). Thus, to determine the insect
response upon exposing it to varied nanostructures require a
Fig. 2. Applications and advantages of micro/nano systems in integrated pest
management.
careful examination to devise an effective strategy for the pro-
longed stability and effectivity of particulate materials.
NPs have the tendency to adsorb a dense layer of proteins which
posessed by nano-based pest control, their extensive application in are highly dynamic in nature forming a ‘corona’ like structure.
the field has remained elusive. Before manoeuvring into applica- Proteins that are abundantly present are known to adsorb on NPs,
tion, it is imperative that multitude of physical parameters needs to which can be replaced by the proteins present in low amount but
be critically evaluated viz. light, temperature, humidity, and bio- has high affinityto the NP surface (Nel et al., 2009). Interestingly,
logical factors such as insect feeding habits, motility, detoxification several reports are available on the interaction of corona proteins
strategies by insects and phytotoxicity. The translocation of par- with nanosurface influencing translocation, uptake and fate of the
ticulate materials and their interaction with insect body fluids have NPs in the biological system. It can be assumed that entry of par-
not been much investigated, exploring which may facilitate precise ticles through feeding exposes it to distinct biochemical composi-
selection of materials and their selective engineering. Hence, the tion present in the mouth parts and in the gut environment of the
studies determining the transport, release and fate of NPs with insect. However, the interactions of the NPs with proteins, native to
respect to insect physiology remain scarce. With relevance to the the insect system, are still obscure. Lepidopteran insects predomi-
invertebrate system, gut pH of herbivores ranges from 6 to 11 which nantly contain serine proteases which are active at alkaline pH, but
seek for the selection of particles exhibiting ‘smart’ pH-responsive several coleopteran insect digestive system is dominant with
properties to overcome such challenge. Furthermore, targeted cysteine proteases that are active at a slightly acidic pH. Interaction
release of the nano-encapsulated bioactive in the specific pH milieu of NPs with proteins in a distinct physicochemical environment
has to cross the barrier of pH gradient which it receives while affects release, retention and efficacy. Furthermore, the properties
passing from the plant surface to the insect gut system. We recently viz., size, shape, charges, hydrophobicity and surface chemistry of
demonstrated the unloading of defensive protein immobilized on the particles determines the selectivity and specificity of their
silica nanospheres to target insect digestive system exhibiting interaction. The role of these features in governing the efficacy and
alkaline pH (Khandelwal et al., 2015). Engineering of such materials applicability of nanomaterials towards insect growth or survival is
to make it acceptable for a desired condition is plausible and readily the subject of research. We propose that studying these factors will
achievable owing to the advancement in chemical and biological be useful for designing micro or nano strategy for effective control
molecular knowledge. Furthermore, several insect display varia- of pests in an eco-friendly way. This will also bring light in evalu-
tions in redox potential which is an indicative of oxidizing or ating the retention of nanoparticles from the view of

Please cite this article in press as: Khandelwal, N., et al., Budding trends in integrated pest management using advanced micro- and nano-
materials: Challenges and perspectives, Journal of Environmental Management (2016), http://dx.doi.org/10.1016/j.jenvman.2016.09.071
4 N. Khandelwal et al. / Journal of Environmental Management xxx (2016) 1e13

environmental concerns. Till date, though reports have demon- industries and the public sector are continuing to grow. Simulta-
strated the efficacy of NPs in regard to insect management, these neously, recent research interventions have advanced our knowl-
parameters have been overlooked which needs a critical viewpoint edge in various solid and liquid based formulation technologies to
in order to successfully commercialize the micro or nano-pest expand biopesticide applicability. Magnetic immobilization of mi-
control strategies for their application in the agriculture fields. crobial cells onto a hybrid product generated from the amalgam of
gellan gum polymer and Fe3O4 nanoparticle has endowed them
3. Rationales for micro and nano-biotechnological approach with the higher degradation ability of organic contaminant,
inpest management carbazole (Wang et al., 2007). For efficient and controlled delivery
of bioactives various surface modifications and combination of
Past few decades have witnessed the increasing use of methods materials have also been explored. Double-shelled microcapsules
involving biological means for controlling pests. Towards this, of avermectin, a microbial-based insecticide was prepared by
modest research support was aimed at screening attributes of coating chitosan over surface functionalized silica shell. Shell
living organisms, plants and microbes and their products to form thickness of nanoparticles provided UV and thermal protection li-
biopesticides. The commercial success of any biopesticides is aises with controlled release of avermectin (He et al., 2013a, b).
largely determined by its efficacy, safe handling, cost effective, Noteworthy, use of Bt biopesticides in insect control is escalating
longer shelf life and non-target safety along with displaying no with a mounting interest in exploring novelties to further its
phytotoxic effects. These features can be addressed by designing effective utilization. Potential of nanoparticles in pest eradication/
robust materials exhibiting stability under environmental condi- suppression have received a recent recommendation to develop
tions and contribute to maintaining the effectiveness of bioactive Btnanopesticides providing protection to high-value crops
agents. By combining these materials with biological ingredients to (Mahadeva Swamy and Asokan, 2013).
form a formulation is expected to endow with consistent responses
at field level. Biopesticide formulations often exert a synergistic 3.2. Plant derived products and their application
effect with multiple modes of actions, reducing the danger of
developing resistance to pests as opposed to synthetic pesticides Over the past decades, plant-derived compounds and extracts
typically having a single mode of action (Hubbard et al., 2014). have been investigated for their capability to control insect pests.
Inherent plant protection from pests is governed by the action of
3.1. Microbe-derived bioactives defensive traits through the production of secondary metabolites
such as alkaloids, benzoxazinoids, cyanogenic glucosides, pheno-
Microbial agents like bacteria, protozoa, fungus, viruses and lics, and terpenoids (Mishra et al., 2015). This arsenal of structurally
nematodes have been investigated and successfully used either and functionally diverse natural molecules exhibit repellant, toxic
alone or in combinations as biocontrol agents. Several industries or antinutritive effects on insects (Ibanez et al., 2012). Our recent
are exploiting the features of bacteria and fungi in reducing or studies have shown enhanced insecticidal effects portrayed by
managing pest populations due to their narrow host range. Ex- Ocimum species by increased levels of metabolites such as camphor,
amples include the use of several species of Trichoderma, Neo- limonene and b-caryophyllene against H. armigera (Singh et al.,
typhodium, Beauveria, Metarhizium in agriculture. Several species of 2014). In vivo studies have also demonstrated the potential of caf-
Neotyphodium endophytes have potent insecticidal properties and feic acid in deterring growth and development of lepidopteran pest
are commercially available (Glare et al., 2012). In addition, various (Joshi et al., 2014). Furthermore, wound inducible plant proteinase
registered products include microbe-derived bioactives that exert inhibitors, a well-studied class of defensive proteins, was found to
deleterious effects on the insect pests and are optimized for large interfere with insect protein digestion, resulting in the arrested
scale production. Selection of microbes requires high throughput growth, lowered fecundity and fertility of H. armigera (Tamhane
screening among thousands of isolates. Genetic engineering of et al., 2005, 2007; Mishra et al., 2010). Despite the intensive
microbes has made it feasible to modulate sub-optimal features of research demonstrating the biological efficacy of plant metabolites,
pesticidal microbes such as efficacy, stability and virulence by only a limited number of plant-based products are registered
overproduction of bioactives with enhanced activity or introducing (Table 1). Products such as neem (Azadirachta indica) seed extract,
insecticidal genes that are obtained from other living organisms (St azadirachtins, pyrethrin, and limonene are amongst the widely
Leger and Wang, 2010; St Leger et al., 1996). Bacillus thuringiensis accepted botanical insecticides (Isman et al., 1990). Azadirachtin, a
based biopesticides have dominated the marketplace since half triterpenoid isolated from neem, interferes with the embryonic
century and have been genetically mutated to produce strains with development of Spodoptera frugiperda (Correia et al., 2013). Heli-
novel insecticidal proteins (Glare et al., 2012). Maintaining the ef- coverpa armigera have also shown to be highly susceptible to the
ficacy of microbial agents in the field is the utmost prerequisite, neem seed extract (Bhushan et al., 2011; Nigam et al., 1994;
which can be achieved by selecting diverse complement of adju- Weinzierl, 2000).
vants and blend it with target agents/molecules to augment efficacy Pesticides based on the plant essential oils (EOs) and plant-
and environmental compatibility. Though data on recipe prepara- derived compounds hold special status of ‘exempted active in-
tion for the commercial microbial formulation is limited, its com- gredients’. They have reduced risk to the environment and are
ponents should provide advantageous properties viz. improved exempted from registration along with extensive toxicological and
uptake, enhanced spread, reduced evaporation and desiccation environmental tests. A few examples are: cinnamon, citronella,
along with providing protection from harsh environmental condi- lemon grass, garlic, thyme, pure compounds like eugenol and citric
tions such as UV radiation and rainfastness (Hynes and Boyetchko, acid (Cantrell et al., 2012). Though many of them act as natural
2006). For example, the addition of Tinopal LPW to the virus sus- repellents against various arthropods, our focus here is on those
pensions contributed to reducing LD50 in target pest Spodoptera compounds that are efficient in controlling the menace of crop
exigua (Lepidopteran) (Murillo et al., 2003). pests. Various formulations of azadiractin have been developed in
Despite the global realization of effective pest control, the the form of emulsion, nanocapsules, and MNPs, achieving greater
commercial success of biopesticides is still facing challenges due to stability and efficacy against pests such as Plutella xylostella, Zab-
biological, ecological, and regulatory constraints. Nevertheless, rotes subfasciatus (Forim et al., 2013; da Costa et al., 2014). In an
improvements in the pesticide research and their acceptance by another example, a citrus extract consisting d-limonene was

Please cite this article in press as: Khandelwal, N., et al., Budding trends in integrated pest management using advanced micro- and nano-
materials: Challenges and perspectives, Journal of Environmental Management (2016), http://dx.doi.org/10.1016/j.jenvman.2016.09.071
 N. Khandelwal et al. / Journal of Environmental Management xxx (2016) 1e13 5

Table 1
Selected examples of plant defensive compounds applied through conjugation on nanoparticles or prepared as formulations against insect pests.

Class Plant Mode of action Details of formulations Effective against References

insecticidal
compounds

Monoterpenoids a-pinene Antifeedant Adsorb on silica nanoparticle Spodoptera litura, Rani et al., 2014;
linalool Achaea janata
(Lepidopterans)
Limonene Neurotoxic Emulsion 1% limonene, 0.75% APSA-80, 0.1% Silwet L-77 Pseudococcus Hollingsworth,
longispinus Aleurodicus 2005
disperses
(Hemipterans)
Tetranortriterpenoids Azadirachtin Molt Nanoformulation in colloidal suspension neem oil 2% (w/v), neem Plutella xylostella Forim et al., 2013
disruptantAntifeedant extract 0.5% (w/v), Span60 0.5% (w/v), polymer (poly(e- (Lepidoptera)
caprolactone))0.5% (w/v), and Tween80 0.5% (w/v)
Alkaloids Nicotine Neurotoxic mode of Nicotine dispersions (3 wt % sodium caseinate, 20 vol % nicotine Aphids (Hemiptera) Casanova et al.,
action, blocks caþþ ion oleate) 2002
channels
Wound inducible Proteinase Digestive enzyme Water: isopropanol: butanol (55:35:10); Loaded on Silica Helicoverpa armigera Tamhane et al.,
Pin-II inhibitor inhibitionAntibiosis nanospheres (Lepidoptera) 2012,
Khandelwal et al.,
2015
Essential oils Garlic Antifeedant Microencapsulation in PEG coated nanoparticles Tribolium castaneum Yang et al., 2009

formulated as an emulsion that demonstrated up to 100% mortality 3.3. Nucleic acid delivery
to mealybug and scale insects (Hollingsworth, 2005). Formulation
of botanicals in an appropriate media is imperative in the view of RNA interference technology is a new tactic for insect control.
overcoming limitations pertaining to field application as well as for This method relies on post-transcriptional silencing by double-
enhanced bioactivity. stranded RNA (dsRNA) mediated downregulation of specific
Repellant and antifeedant activities of plant secondary com- gene(s) by degrading respective messenger RNA (mRNA)(s). dsRNA
pounds, a-pinene and linalool were elevated to 25% against Spo- upon encounter with endonuclease called “dicers”, produce small
doptera litura and Achaea janata when formulated with silica NPs. interfering RNA (siRNA), one strand of which is responsible for
Nanoformulation granted improved shelf life to these terpenes for target degradation (Gordon and Waterhouse, 2007). So far, the
the purpose of their long-term use in the field (Rani et al., 2014). potential of dsRNA to control insects has been evaluated by
Among conventional pesticides, synthetic pyrethroid derived from microinjection into the insect gut, oral feeding assays and trans-
a plant (Chrysanthemum species) holds an essential component, genic expression (Price and Gatehouse, 2008). Studies have sug-
which can control a wide range of insects. Historically, pyrethrum is gested that the efficient delivery of dsRNA in an insect is an
recognized as a potent killer of insects. However, it is highly un- important factor to achieve efficacy. For instance, microinjection of
stable when exposed to light and UV radiation. Thus, the synthetic dsRNA in the insect hemocoel efficiently downregulated the
derivatives are formed by chemical modifications to render stability midgut aminopeptidase-N gene of Spodoptera litura, but feeding
to pyrethrin in order to maintain its efficacy (Clark, 1997). Similarly, the dsRNA construct to the insect did not result in downregulation
the neonicotinoid class of insecticides containing plant-derived of this gene (Rajagopal et al., 2002). This differential response is
nicotine has captured a significant portion of the insecticide mar- assumed due to the complexity of insect physiology that exists in
ket. However, considering the environmental toxicity posed by different species and respond differently to oral uptake and injec-
these synthetic pesticides, it is essential that use of formulations ted RNA (Price and Gatehouse, 2008).
implicate non-toxic effect on non-target insects and safety towards The efficiency of introducing RNAi in insects suffers challenge of
humans by guarded pesticide handling. In a study, nicotine-based lower solubility, poor delivery, and uptake as well as degradation by
formulation was prepared using sodium caseinate as a stabilizing nucleases. Hence, it is projected to use an advanced nano or micro
agent. Dispersion of increasing concentration of nicotine oleate delivery system, such as an encapsulated or conjugated dsRNA to
sought three formulation systems in the form of emulsion, suspo- achieve exceptional results. Advanced materials including cationic
emulsion and suspension. This study revealed greater bioactivity polymers, dendrimers, and functionalized nanoparticles are
and stability of formulation majorly in the form of emulsion and considered as an effective gene delivery materials (He et al., 2013a,
suspension (Casanova et al., 2002). b). In a study, fluorescent nanoparticles were developed containing
Thus, to achieve substantial stability and biological activity, a dye in the center, poly (phenylene) dendrimers form the inner
appropriate liquid and solid formulations can be designed that layer, whereas the outer layer is composed of a cationic polymer.
propound promising opportunities for pest control in an environ- The inner layer of dendrimers assists in preventing the aggregation
mentally benign way. Botanical insecticides pose a narrow range of of dye in water milieu whereas amino group functionalized
stability under environmental conditions, including thermal outermost polymers shells aid in enhanced aqueous solubility. This
degradation, product inactivation and rapid evaporation (de structure comprised of positively charged polymer shell to facilitate
Oliveira et al., 2014). Furthermore, commercial level of success binding of negatively charged DNA or dsRNA. In vitro analysis
also depends on properties such as controlled release of the active revealed efficient uptake of genetic materials while exhibiting low
compound, improved physicochemical stability, greater retention cytotoxicity (Liu et al., 2015).
and better uptake. This has enabled researchers to explore delivery Application of NPs conjugated RNA for the disruption of target
mechanisms by exploiting MNPs or emulsions and polymeric gene activity in the insect may exert negative consequences on its
nanoparticles that are depicted to hold beneficial characteristics biological function. However, the knockdown efficiency varies with
than their bulk counterparts. the type of NP used along with the ratio of NP-dsRNA conjugated

Please cite this article in press as: Khandelwal, N., et al., Budding trends in integrated pest management using advanced micro- and nano-
materials: Challenges and perspectives, Journal of Environmental Management (2016), http://dx.doi.org/10.1016/j.jenvman.2016.09.071
6 N. Khandelwal et al. / Journal of Environmental Management xxx (2016) 1e13

complex and require optimization. In an interesting study, three used to form a micro-suspension and then a nano-milling process
different types of NPs i.e. carbon quantum dots, chitosan and using Zirconium oxide beads provided the second milling step.
amine-functionalized silica NPs were used to conjugate the same Formation of nanosuspension concentrates containing pesticide
amount of dsRNA. Though the loading efficiency in all the cases was imparted enhanced dissolution of poorly soluble insecticides, (e.g.
reported to be 100%, their efficiency in gene suppression varied carbofuran) along with increased stability. Evaluations of its bio-
with carbon quantum dots showing the efficient suppression of logical activity against diamond black moth was shown to be highly
Aedes aegypti gene (Das et al., 2015). This demonstrates that the oral efficient at low effective concentration (Chin et al., 2011). This study
route of delivering genetic materials conjugated with MNPs in in- represented the high efficacy of nanosuspension as compared to
sects for the gene suppression offers a non-toxic and economically microsuspension. Development of such novel processes can be
viable approach. It also offers an easy method for controlling insects extended to address other problems faced by poor bioavailability or
by avoiding a tedious process of generating plant transgenics. stability of biological or chemical pesticides for their safe and tar-
However, before administration, a detailed assessment of the use of geted use in contrasting environments. Further potential advan-
RNAi delivery systems is required for its successful administration tages of the use of MNTs and mode of delivery of active ingredients
and protection in the field conditions. in IPM have been provided in the subsequent subsections.

4. Reinforcing nano or micro based pesticides: techniques 4.1. Micro/nanoemulsion formulations

and applications
Due to the differential solubility of active ingredients, emulsions
Small materials comprising various sizes of MNPs has a pro- are prepared by dispersing liquid droplets (as a dispersed phase)
found impact on their functionality in medical and agricultural into another fluid as a continuous phase (e.g. oil/water or water/oil
applications. Nanotechnology refers to a technique involving syn- emulsion). This system could be further stabilized by adding
thesis, engineering, modification and implementation of materials surface-active ingredients (Sathishkumar et al., 2008). Such for-
or solutions having particles or droplet size ideally below 100 nm mulations are routinely used with certain modifications depending
(Fig. 1) (Khandare et al., 2012). Small sized NPs such as carbon on the environment, crop, target insect pests and their feeding
nanotubes, dendrimers or quantum dots have been explored well habits. Currently, development of formulation is focused with an
for drug delivery purposes but is still in its infancy in the delivery of objective of high loading of active ingredients and for wide spec-
agrochemicals. The size of the NPs largely influences the binding of trum applications, resulting in greater efficacy and applicability
active ingredients such as protein/peptide or DNA/RNA and loading against target insect pests. Towards this, micro/nanoemulsions may
efficiency. Especially, for agricultural application, efficient loading achieve this crux in delivering a high payload of bioactives.
of bioactives are desirable. In addition to size, surface chemistry and Micro/nanoemulsion-based pesticide formulations have
particle composition has a crucial importance in pesticide delivery advantage over the conventional pesticidal emulsions due to their
and particle uptake. long-term thermodynamic stability and small droplet size (Wang
Use of nano or micro based pesticides applied through nano/ et al., 2007). Altogether, these systems boasts wide range of solu-
micro-emulsions, nanocapsules or MNPs offers unparalleled ad- bilizing ability allowing loading of different polar and non-polar
vantages over the conventional delivery systems. They propose to compounds in an acceptable range (Sathishkumar et al., 2008).
provide a wide range of solubility, thermal stability, biodegrad- Thus, it is possible to develop microemulsions complementary to
ability, large surface area and permeability (Bergeson, 2010; the chemical bio-actives with desirable features. A microemulsion-
Bouwmeester et al., 2009). For the successful application of bio- based formulation carrying plant proteinase inhibitor (PI) protein
actives, it is desirable that the pesticide formulations must were developed and was evaluated for safety and efficacy when
include the following traits, viz. (i) improved activity, (ii) increased applied to the plant surfaces (Tamhane et al., 2012). PI formulation
spreading and retention ability on plant surfaces, (iii) stability in composed of water: isopropanol: butanol (WIB) microemulsion
the external environmental milieu and (iv) ease of handling (Mollet was found to be effective against H. armigera and caused no adverse
and Grubenmann, 2001). Formulations are prepared in different effect on the plants as compared to the other microemulsions in the
ways by assessing various physicochemical properties of bioactive study. Interestingly, WIB microemulsion was found to increase the
agents. In several instances, there is a practical difficulty in applying retention of PI protein on leaf by possibly endowing the property of
or spreading the active ingredients directly for effective insect penetration (Tamhane et al., 2012). Despite providing advantageous
control. Furthermore, the active ingredients may be chemically properties microemulsion systems in agronomical application are
unstable, difficult to handle and may have a short shelf life. Thus, very limited. A few examples include, developing novel formula-
‘active ingredients’ are generally formulated using excipients which tions by incorporating cyhalothrin, an organic pesticide in the
provide a protective shield and may act as adjuvants. Generally, microemulsion system (Zhao et al., 2009). Similarly, water insol-
these formulations are differentiated by physical classes, e.g. uble agrochemical, b-cypermethrin formulations were developed
emulsions, ready to use aerosols, smoke or fog generators, micro- by incorporating it into the microemulsion concentrate. Dilution of
encapsulated materials, pastes, gels and other injectable baits. this concentrate with a large amount of water forms a stable
Pesticide formulation may consist of; (i) pesticidal active in- nanoemulsion system displaying enhanced wetting, spreading and
gredients that control the target pest, (ii) the vehicle, e.g. organic penetrating properties (Wang et al., 2007). This suggests that such
solvent or mineral clay, (iii) surface-active ingredients including systems can be efficiently utilized and modified to contain bio-
stickers and spreaders (e.g. emulsifiable concentrates) and (iv) logically or chemically active ingredients and might prove to be a
other ingredients, such as stabilizers, dyes, and chemicals to promising system for hydrophilic or hydrophobic compounds. Such
enhance the pest control activity. microemulsions can have immense potential in the agriculture
Water insoluble pesticides can be formulated using microen- industry owing to its increased dispersion over larger contact area,
capsulation and nanoemulsion formulation methods to enhance improved wettability and enhanced penetration properties (Paul
their bioavailability in aqueous environment (Tsuji, 2001; Wang and Moulik, 2001). While bio-formulations intend to cause no
et al., 2007). A pesticide delivery system was developed contain- harmful effect on the environment, the possibility of the phytotoxic
ing pesticide, surfactant, and water by two-step milling process effect on the target crops after multiple applications must be
(Chin et al., 2011). In this formulation, a general milling process was recognized and needs to be tested over extended period to develop

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 N. Khandelwal et al. / Journal of Environmental Management xxx (2016) 1e13 7

a suitable and anecologically acceptable system. 4.3. Delivery via adsorption/immobilization

The property of NPs to adsorb proteins and revealing their

interaction has been the subject of intensive research in nano-
4.2. Nanoparticles as advanced delivery systems toxicology or nanomedicine applications. Due to small size and
large surface area they serve as an excellent template for the
Nanoscience and its transformation into nanotechnology plat- adsorption of the large number of proteins and other biomolecules
forms are anticipated to offer better solutions for targeted delivery. involving hydrogen bonds or through hydrophobic interactions
Towards this, both organic and inorganic components have been (Dastkhoon et al., 2015). Interestingly, the process and properties
widely explored in fabricating nano-sized systems, deliberating the can be exploited to adsorb bioactive compounds on the nanosur-
prudent applications in engineering and biomedical sciences. face for the targeted delivery of the active ingredients in agricul-
In general, nanosystems offer several tasks in parallel including tural applications. Application of silica NPs, described in the later
loading of cargo molecules, either small or large, through the section, has unique advantages pertaining to surface functionali-
conjugation process (Khandare et al., 2012). Therefore, the nano- zation, surface area and particle size. Mesoporous silica nano-
systems are typically prepared using biologically relevant bio- structures with varied pore diameters, and structures were
polymers (e.g. sodium alginate, chitosan etc.) and hard matters (e.g. synthesized to evaluate the factors important in the adsorption and
Zeolites, iron oxide, nanoporous silica, etc.) that suggest numerous release of synthetic insecticide imidacloprid, an insect neurotoxin.
applications. Furthermore, additional complexities are chemically The adsorption isotherm study revealed that particle with larger
tuned by adding multifunctional components, thus, leading to surface area shows higher adsorption by accumulating large
robust chemical diversities. Methods such as encapsulation, cova- number of imidacloprid particles. After adsorption, strong reduc-
lent bonding, adherence, and adsorption, render significant impact tion in the particle surface area or pore diameter was obsereved as
on the ‘smart’ delivery approach to achieve controlled payload compared to other structures with lesser surface area (Popat et al.,
release (Ghormade et al., 2011). (Fig. 3). Most of the approaches that 2012). Loading of natural or chemical agrochemicals occurs through
have been developed to fabricate the multicomponent nano- physical interaction at the nano-bio interface that may cause sig-
systems rely upon the adsorption of molecules on their surfaces nificant conformational changes leading to a possibility of disrup-
(Asfaram et al., 2015; Khandelwal et al., 2015). Conversely, the tion or enhanced activity of bioactives. Studies suggest that
chemical conjugation methods can considerably affect the effi- parameters like hydrophobicity and particle size are the vital de-
ciency of the delivery system. Multiple agents may compete for the terminants for maintaining the native structure of proteins (Mahon
same surface binding sites and thus may alter the efficacy of both et al., 2012). Owing to the plasticity of the particle size and surface
agents. Depending upon the biological significance and chemical area fine tuned with desired surface chemistry modifications, it is
properties of the bioactives, selection of suitable materials is crit- plausible to control the surface hydrophobicity and surface curva-
ical. This further relies on the interaction of bioactives with nano ture leading to high adsorption and enhanced stability of proteins
structures that can affect their delivery and hence efficacy.

Fig. 3. Schematic representation of nanomaterials and their interaction with active ingredients. Bioactive delivery by encapsulation, adsorption, binding on the surface through
ligands and entrapment in the polymer are shown. Different biologicals or chemical pesticides along with nanocides can be formulated appropriately for their controlled delivery on
plants in managing pest infestation. The figure shows examples of each class of pesticides such as Azadirachtin, cholopyrifos and silica NP.

Please cite this article in press as: Khandelwal, N., et al., Budding trends in integrated pest management using advanced micro- and nano-
materials: Challenges and perspectives, Journal of Environmental Management (2016), http://dx.doi.org/10.1016/j.jenvman.2016.09.071
8 N. Khandelwal et al. / Journal of Environmental Management xxx (2016) 1e13

along with achieving efficient release. In our recent study, we have has not only led to the enhanced stability of the compounds by
utilized the adsorption property of NP to form a single protein allowing controlled release, but reduced volatility haveaugmented
corona by using silica nanospheres and mixing it with protein its bioavailability with minimum active concentration. As a
(proteinase inhibitor). With increasing concentration of protein, its consequence longevity of active ingredients as compared to free
adsorption on the NP surface was obsereved to be greater as essential oils can be accomplished due to slow and consistent
calculated by quantifying the remaining amount of proteins. release. In another example, EO extracted from cumin (Cuminum
Interestingly, the electrostatic interaction at the nano-bio interface cyminum) were entrapped in nanogels formed by the combination
facilitated the adsorption of positively charged proteins on nega- of myristic acid and chitosan to exhibit their fumigant toxicity
tively charged silica surface as measured (Khandelwal et al., 2015). against granary weevil Sitophilus granarius and flour beetle Tribo-
lium confusum. Results indicated enhanced toxicity of nanogel
4.4. Delivery via encapsulation loaded essential oil as compared to free oil which showed an
insecticidal activity loss in 12 days (Ziaee et al., 2014). Thus, overall
In context with field application of bioactives, their protection observations manifest that loading or encapsulation of oils in
from environmental factors such as UV degradation, rain fastness, nanoparticle is preferable to achieve controlled delivery and to
evaporation losses, temperature stability is essential. An ideal maintain stability of sensitive compounds. Encapsulation of EO
encapsulating material for bioactives protects the sensitive com- extracted from Artemisia arborescens, an important medicinal plant
pounds from getting ineffective and facilitates their controlled and was reported. Biological significance of Artemisia EO against
sustained release. The sensitivity of azadirachtin, a potent insecti- various arthropod pests has been well documented.The drawback
cidal compound, to environmental conditions led the researchers due to its physico-chemical degradation has led to the use of solid-
to screen different materials for the preparation of nanoparticles lipid nanoparticles rendering physical stability, enhanced shelf life
that can enhance its stability while obtaining efficient encapsula- and reduced evaporation of the oil (Lai et al., 2006). Its encapsu-
tion and optimized release. Sodium alginate nanocarriers laced lation in alginate beads also exhibited its slow release. These results
with different coating agents such as natural rubber, starch and PEG reinforce the possibility of the extensive use of these nano or micro
showing over 80% encapsulation efficiency (Riyajan and systems in agronomy for control pesticide delivery. The application
Sakdapipanich, 2009; Jerobin et al., 2012). Encapsulating vehicles, of various inorganic and organic material with relevance to insect
in general, may contain a selective material that act as a nanocarrier management are provided in the below sections.
or coating agent and a reticulating agent. Together these materials
control the encapsulation efficiency and release rate for the bio- 4.5. Interaction via surface functionalization
actives in desired environment. Several examples pertaining to
agricultural application of natural compounds have been provided Covalent attachment of structural moieties onto the surface for
in the above sections that make use of encapsulation methods for the adsorption or coupling of the active ingredients is the utmost
their targeted delivery. Such nanoformulations display less toxicity requirement to attain desired results. Surface chemistry of nano-
to non-target insects as compared to their respective commercial or materials grants opportunities to carry out certain modifications
bulk counterparts. that become the primary determinant of their interaction with
Plant derived products or extracts have gained a prominent biomolecules and biological system. For the application of nano-
position in agriculture, especially, in the production of organic materials in insect pest management, suitable surface chemistry
foods. de Oliviera et al. (2014) reviewed application of plant based plays a key role not only in determining its efficacy, but maintaining
insecticidal compounds such as azadirachtin, rotenone, calvacrol, stability and can avoid ecotoxicity by specific conjugation of
thymol, eugenol, including essential oils of garlic, rosemary and chemical moieties. Modulation of surface properties enhances the
citrus plants. Plant-based EOs are the complex mixture of metab- uptake or bioavailability in specific conditions. For instance, prob-
olites that appear to be non-toxic in isolation, but exert a syner- lem pertaining to the distribution of hydrophobic pesticides in in-
gistically antagonistic effect on the pest (Isman et al., 2011). Though sect physiological system can be resolved by entrapping the active
their significance in the protection of stored grains was known ingredient onto carrier with hydrophilic surface moieties medi-
traditionally, re-evaluation of their efficacy in the agricultural sys- ating their effective distribution. Nanocarriers based on dendrimers
tem by combining approaches from nanotechnology envisages were successfully used for entrapping pesticide molecules after
great potential in agronomy. Synthesis of nanocarriers takes into surface functionalizationwith amine groups to enhance their hy-
account the effect of encapsulation efficiency, release profiles and dration (Liu et al., 2015). Silica NPs due to the presence of large
stability of botanicals for their successful development and appli- number of silanol groups on the surface allows it to be readily
cation. Coating of nanoparticles restricts the exposure of active functionalized with various organic groups to carry out desired
ingredient to light and temperature thereby preventing the functions. For instance, surface functionalization of silica particles
degradation by microbes. In addition, it facilitates slow release of with 3-mercaptopropyltriethoxysilane and hexamethyldisilazane
bio-actives as compared to the uncoated nanoparticles. Polymers have shown enhanced efficacy against lepidopetran pest (Debnath
such as PEG, sodium alginate, chitosan or solid-lipid nanoparticles et al., 2012). Modification of surface chemistry also affects release
offer such advantages. For instance, loading of garlic EO on poly profile of bioactives and can circumvent the problems of bioactive
(ethylene glycol) (PEG) coated nanoparticles displayed over 80% outburst thereby rendering sustained release. Use of the selective
efficacy against T. castaneumup to 5 months against free oil showing coating matrix such as PEG function to contain the bioactive
only 11% controlling efficiency (Yang et al., 2009).Nano-carriers encapsulated and facilitate slow release.
with PEG coating does not interfere with the activity of natural
compounds such as enzymes or proteins, exhibits a wide range of 4.6. Inorganic micro and nano-pesticide delivery systems
solubility and are biocompatible thereby ensuring lack of toxicity.
In a study, nanoformulation of PEG was employed for the gradual In the view of increasing concern over an indiscriminate use of
release of plant secondary metabolites, geranium and bergamot pesticides, MNT was suggested to be the potential carrier of pes-
terpenes. It ensured enhanced contact toxicity through disrupting ticides, allowing an optimized level of exposure in the environment
digestive physiology of storage pests Tribolium castaneum and with reduced and effective dose. Inorganic micro and nanoparticle-
Rhizopertha dominica (Gonzalez et al., 2014). PEG polymeric matrix based formulations for pesticide delivery have attracted great

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materials: Challenges and perspectives, Journal of Environmental Management (2016), http://dx.doi.org/10.1016/j.jenvman.2016.09.071
 N. Khandelwal et al. / Journal of Environmental Management xxx (2016) 1e13 9

attention over the last few years as they offer high stability, 2015). The nanosystem based formulation possessed a critical
chemical versatility and biocompatibility (Fig. 4A). Inorganic property of pH-triggered release, thus, offering an advantage of
nanomaterials, e.g. iron oxide, silica, and calcium phosphate controlled release of immobilized proteinase inhibitor peptide.
nanoparticles envisaged unprecedented opportunities in delivering Silica nanoparticles exhibited a high peptide loading capacity ac-
bio-actives (Debnath et al., 2012; Banerjee et al., 2015). For counting for 62%. The interaction of proteinase inhibitor peptide
example, silica nanoparticles have burgeoned to be the most widely with silica nanosphere was driven by the charge and ionic strength
explored material for pesticide delivery as they offer inimitable as evident from the variation in peptide loading at different pH.
advantages (Fig. 4B). They possess markedly different features viz. Additionally, other forces such as particle size, curvature and ag-
physical and chemical stability, tunable pore sizes, high surface area gregation were suggested to play their role at the interface. Inter-
and distinct surface properties, making them superlative for mol- estingly, an in vitro release study showed pH-dependent peptide
ecules of varied sizes, shapes and functionalities (Khandelwal et al., release of 56% at pH 10 and in vivo study demonstrated higher ef-
2015; Torney et al., 2007). In addition, silica nanoparticles provide ficacy for proteinase inhibitor peptide with silica nanoparticle as
stability to bio-active molecules from chemical to physical param- compared to the control.
eters such as temperature, moisture, plant's chemical secretions, It was reported that treating insects with silica NPs (15e30 nm)
soil pH and composition. These characteristics must be considered resulted in higher mortality than when the insect was treated with
in the efficient delivery of many peptide and protein molecules. bulk silica (Debnath et al., 2011; Wen et al., 2005). The possible
Various reports on the utilization of functionalized silica as mode of action of silica particles on insect physiological system is
nanocides or carriers with varying size have been demonstrated for suggested by blocking the cuticular lipid layers for the passage of
their plausible application in pest management. Recently, we water resulting into dehydration of the insect (Barik et al., 2008).
investigated the potential of silica based nanospheres and rods Amorphous nanosilica was also shown to be effective against
immobilized with proteinase inhibitor peptide (Khandelwal et al., storage grain pest and field pest. Surface functionalized silica NPs

Fig. 4. Present and futuristic micro- and nano-formulations and delivery systems exhibiting potential to be used in the insect pest control in agriculture. [A] Currently
explored nanosystems in pest management, e.g. nanoporous silicates, porous zeolites, alginate/chitosan polymers. While, another perspective nano-delivery components such as
carbon allotropes (e.g. CNT, grapheme etc.), dendrimers and calcium phosphates; [B] Properties of silica nanoparticle beneficial for pesticide delivery applications.

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materials: Challenges and perspectives, Journal of Environmental Management (2016), http://dx.doi.org/10.1016/j.jenvman.2016.09.071
10 N. Khandelwal et al. / Journal of Environmental Management xxx (2016) 1e13

possess the advantages of impating desired features to carry spe- physiological fluids is through the sodium-calcium exchange. The
cific functions. A study revealed that surface functionalized silica delivery of pesticidal compound through alginates has also been
nanoparticles i.e., hydrophobic, hydrophilic or lipophilic coatings demonstrated. For example, the delivery of imidacloprid in the
have a differential effect on Sitophilus oryzae mortality (Goswami form of nanoformulation was achieved by utilizing sodium alginate
et al., 2010). Similarly, silica nanoparticles capped with 3- biodegradable polymer (Bhagat et al., 2013). The pesticide entrap-
mercaptopropyltriethoxysilane and hexamethyldisilazane was ment efficiency was observed to be more than 98%, however, the
assessed against S. Litura (Debnath et al., 2012) and found signifi- formulation showed less cytotoxicity in in vitro studies over un-
cantly effective. Silica nanoparticles have also been used for de- formulated pesticide. Also, in vivo studies showed a significant
livery of pesticides with the short half-life. For example, avermectin reduction in leafhopper population on okra leaves after the treat-
an insect chloride channel inhibitor that blocks neurotransmission ment. Calcium alginate is rich in divalent salts and once it is
shows a major problem in the field due to UV inactivation. Li et al. introduced in the environment, the insoluble calcium alginate
investigated porous hollow silica nanoparticles to deliver aver- converts into a soluble alginate. This subsequently results in the
mectin. These nanoparticles not only protected avermectin from solubilization of nanoformulation at alkaline pH and release of the
UV degradation by encapsulation but also controlled its slow pesticide is achieved (Kumar et al., 2014). Entrapment of Chlor-
release. Furthermore, the nano-pesticide formulation exhibited a pyrifos in a polymer based matrix formed by the combination of
sustained-release pattern for nearly 30 days (Li et al., 2007). Under starch and alginate via crosslinking with CaCl2 has produced pes-
similar lines, insecticidal effect of nanostructured alumina was ticidal nanospheres (Baohua, 2013; Roy et al., 2009). Interestingly,
tested against two storage pests, Sitophilus oryzae and Rhyzopertha nano-pesticidal structures are bestowed with greater environ-
dominica (Stadler et al., 2010). Results demonstrates that exploita- mental and economical advantages such as low toxicity to non-
tion of nanosturctures with various functionalizations can impart targets due to release in a controlled manner as compared to bulk
significant effect on controlling pest population and present a scope or commercial formulations. In a recent study, silver NPs were
for further testing their role as nanocides in pest management. employed for nano-encapsulation of dichlorvos and chlorpyrifos,
Other inorganic materials such as clay have also been studied for stabilized by the starch obtained from cassava. While the entrap-
potential use in pesticide delivery. Clay nanoparticles form stacked ment efficiency for the both the pesticides was over 95%, their
platelet-like structure with a nanometer scale dimension of each release profiles exhibited slow and long lasting discharge in a
platelet. Nano-clays provide more interactive surfaces when exfo- buffered medium (Ihegwuagu et al., 2016). This study represents a
liated and dispersed well due to the high aspect ratio (Ghormade facile, rapid and a cost effective method of synthesizing pesticidal
et al., 2011). Singh et al. developed pesticide delivery systems nanostructures in the range of 23e30 nm which can further be
containing neem leaf powder, kaolin, and bentonite. The formula- extended for a large scale production. Application of highly hy-
tion demonstrated controlled and sustained release due to the drophobic pesticides is usually problematic for their low solubility
presence of kaolin and bentonite particles while the release of in aqueous environments and risk to transdermal exposure if
thiram from kaolin-based formulation was found to be greater solubilised in an organic solvent. Efficacy of hydrophobic pesticides
compared to bentonite (Singh et al., 2010). The clay based poly- is largely dependent on their degree of dispersion. Effective
meric beads facilitate safe handling and finally supports efficient dispersion can be achieved by designing an appropriate nano de-
delivery (Roy et al., 2014). livery system to generate stable dispersions. Bifenthrin, largely
Insecticidal effect of silver nanoparticles (AgNP) was investi- used to protect cotton plants from insects, were suspended in a
gated in two lepidopteran insects, castor semilooper (Achaea janata nanoparticle formulation for improved uptake by insects and
L.) and asian armyworm (S.litura F.). Insects displayed delayed enhanced release. For this, flash nanoprecipitation technique was
growth due to the accumulation of silver nanoparticles in their gut applied, which involves rapid mixing in a controlled chamber to
and a larger proportion of AgNP was detected in their fecal matter. achieve high supersaturation of active ingredient leading to rapid
(Yan et al., 2014). More studies are needed to make a reliable nucleation and growth. The growth is restricted by the adsorption
assessment of the benefits and risks of using silver nanoparticles. of amphiphilic polymer on the surface. This technique creates
Further insights in this research are anticipated over the coming nanosized particles of <200 nm with stable dispersions (Liu et al.,
years to address the present knowledge gap, by exploring other 2008). By choosing an appropriate polymer, the efficacy of
attractive inorganic nanosystems such as iron oxide nanoparticles, different hydrophobic compounds can be improved with enhanced
calcium phosphate, etc (Banerjee et al., 2015). bioavailability.Various novel approaches using polymeric gels have
been designed with major emphasis on environment-friendly
4.7. Advance polymeric delivery systems in pest management management of fruit flies. Low molecular mass gelator consisting
nanogels was prepared from a pheromone, methyl eugenol (Bhagat
Many new polymer based systems are being introduced as et al., 2013). The pheromone nanogels showed greater stability
nanocarriers, however, progress is limited due to stringent clinical under all environmental conditions. At the same time, it has
regulations, toxicity profiles, and overall therapeutic efficacy. New controlled and reduced the rate of evaporation of pheromone
polymeric nanocarriers are being designed and explored in vivo, significantly. The nano-gel pheromone demonstrated an effective
and their biocompatibility and delivery capacity is being correlated management of Bactrocera dorsalis, a prevalent pest for a number of
with bioavailability, tissue distribution and its elimination (Yasur fruits e.g. guava. This study demonstrated a practical low-cost
and Rani, 2015). green polymeric delivery strategy for crop protection.
Preparation of pesticidal nanoformulation requires their Dendrimers are hyperbranched polymers and are used in drug
entrapment usually in biodegradable polymers for slow and sus- delivery due to monodispersity, nano size and multiple modifica-
tained release. In general, few natural polymers like chitosan and tions for surface functionalization (Khandare and Minko, 2006).
alginates can serve as important functional nanocarriers for Use of fluorescent dendrimers for synthetic pesticide thiame-
application purposes by encapsulating bio-actives/chemical pesti- thoxam showed promising results (Liu et al., 2015). Nanoparticle-
cides. In particular, sodium alginate, an acid resistant poly mediated gene delivery including dendrimers and cationic poly-
(saccharide) anionic polymer, has been widely explored as a drug mers have received greater attention for delivery of nucleic acids
carrier because of its biocompatibility and non-toxicity. The prime (Jin et al., 2009). Interaction of nucleic acids with cationic polymers
mechanism governing the active ingredient release in the is electrostatically driven which provides the protection from

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materials: Challenges and perspectives, Journal of Environmental Management (2016), http://dx.doi.org/10.1016/j.jenvman.2016.09.071
 N. Khandelwal et al. / Journal of Environmental Management xxx (2016) 1e13 11

degradation and subsequently facilitate cellular uptake. Fluores- signal transducers facilitating facile and direct transfer of electrons
cent nanoparticulate dendrimers were employed to assist their from immobilized electroactive species and the electrode. Their
transfer across the cell membrane. The dsRNA for a chitinase-like application is noticeable in the detection of the potential in-
gene was synthesized, mixed with fluorescent nanoparticles, and secticides namely, methyl parathion, carbaryl, monocrotophos.
fed to the Asian corn borer (Ostriniafurnacalis). The results showed Another electrochemical sensor employing, specific detection
adverse effects on the insects such as small body size and failure to methods such as molecular imprinting for nitroaromatic OPs such
some individuals to molt (He et al., 2013a, b). These studies high- as paraoxon, methyl parathion, and fenitrothion were developed to
light new avenues in the utilization of pesticides based nano- circumvent the use of biomolecules with the benefits of high
systems. Overall, these strategies provide advantages of easy selectivity and improved precision. Zirconia NPs, exhibiting high
synthesis in bulk, flexibility to modifications, environmental sta- affinity to the phosphoric group, was deposited on gold electrode
bility, targeted delivery, and thus reducing the harsh effects of facilitating OPs adsorption for its electrochemical detection. The
chemical pesticides. study suggests the scope of field monitoring of OPs by designing
portable electrochemical sensors and reusable NP printed gold
5. Other applications electrode (Liu and Lin, 2005). Recent studies have reported novel
enzyme-based nano-biosensors for the detection of an OP, para-
5.1. Detection of pesticide residue oxon with the advantage of requiring very low concentration of
starting sample (10e1000 nM) with detection limit close to
One of the important aspects of sustainable agricultural prac- 5  106 mM. The nanomagnet silica core-shell was conjugated to
tices is to apply an effective concentration of pesticides in the crops. OP hydrolase (OPH). Coumarin 1, a competitive inhibitor of OPH
A significant amount of spray pesticide leaches off into the soil and was used as a fluorogenic probe. Upon excitation, nanomagnet
groundwater consequently polluting the environment and silica core-shell caused a mirroring effect to intensify radiations
demanding multiple applications. Furthermore, the persistence of emitting from coumarin. Paraoxon, competing for the enzyme
pesticide residue in the harvested or processed food is of high active site, resulted in the reduction of emission, which is a direct
importance to assess. Detection of pesticide residue in the envi- measure of paraoxon concentration (Khaksarinejad et al., 2015).
ronment needs to be monitored for the risk assessment purposes
and to determine exposure limit (Barry et al., 2009). Several 5.2. Pesticide degradation
immunological assays were developed, though with a detection
limit of one residue per assay thereby requiring several tests for the To reduce the potential exposure of pesticides in the environ-
complex mixture. Also, the lack of quantitative measures for the ment, their removal via nano-based degradation methods were
accurate pesticide detection with minimal cost/resources was explored. As many conventional approaches are time-consuming
another constraint. An upsurge in micro and nano-based techno- and incur a high cost, contaminant removal by nanomaterials
logical innovations suggest advantages of developing advanced promises rapid action with low cost (Asfaram et al., 2016; Ghaedi
microanalytical biosensors (Barry et al., 2009). Application of MNPs et al., 2016). Photocatalytic degradation of hexachlorobenzene,
coupled with the range of biomolecules forms a novel detection cypermethrin and dicofol pesticides using titanium oxide NPs was
system. Such systems offer the benefits of quick and simultaneous demonstrated. At the interface of pesticide and TiO2 NP, a series of
detection of residues in a complex system with greater sensitivity at electron transfer reactions takes place along with the production of
nano-micro scale. Attachment of proteinaceous molecule or oligo- peroxide. Presence of hydroxyl radicals further accelerates photo-
nucleotides on the nanostructures imparts them with the property degradation (Yu et al., 2007). Dispersion of TiO2 over a porous
of biorecognition. By the virtue of target analytes to take part in nanosilica was found to be effective in degradation of commercial
specific chemical reactions upon interacting with biosensors, their pesticidal preparation of imidacloprid and phosphamidon (Sharma
detection becomes feasible by performing tests like colorimetric, et al., 2009). Degradation of various chemical classes was also
fluorometric, conductometric or change in electric potential. evaluated though are not discussed in this review considering its
Biosensors developed for the detection of organophosphates limited scope.
(OPs) and carbamates pesticides are mainly based on their ability to
inhibit cholinesterase enzyme. Cholinesterase (ChE) hydrolyses its 6. Conclusions and future perspective
natural substrate, acetylcholine into choline and acetic acid. Vari-
ation in pH due to the acid formation can be determined by The thrust of MNT in agriculture is expanding at an accelerated
measuring the pH indicating presence of pesticidal components. In rate and reaching almost every sector. In this review, application of
a more sensitive and reliable detection system, ChE and choline MNT to curb the use of chemical pesticides and develop an envi-
oxidase (ChOD) were immobilized on Au-Pt metallic nanoparticles ronmental benign strategy for control of pest populations was
based electrode. Choline being a non-electroactive species was given a major focus. Along with this, safe handling of pesticides and
processed into H2O2 by the action of ChOD for its further oxidation. controlled delivery of agrochemicals using micro and nano-
The combined effect of bimetallic NPs assisted in electron transfer structures are also depicted. With the burgeoning potential of
process by the increased surface area for the potentiometric biopesticides, a comprehensive understanding of natural com-
detection of pesticidal residue (Sassolas et al., 2012). In another pounds and their properties is imperative. Understanding the po-
highly sensitive method, polyvinyl pyrrolidone capped cadmium tential of natural compounds and their utilization has been
sulfide (CdS) quantum dots nanostructures were used for the demonstrated in various studies for their effective role in control-
detection of trichlorfon, based on the principle of inhibition of ChE. ling insect pest attack on plants. However, more studies of these
Enzymatically produced thiocholine from an artificial substrate compounds in the field are needed. Advances in MNTs have
acetylthiocholine was electrochemically distinguished (Li et al., contributed to the successful development of nano or micro based
2006). Similarly, carbon nanotubes were developed for the identi- formulations by achieving effective delivery, imparting enhanced
fication of carbaryl with a detection limit of 4.9  1015 M. Gold NPs activity, greater stability of the compounds and biodegradability.
(Au-NPs) hold intriguing properties for the preparation of bio- Importantly, choosing an ideal nanomaterial or formulation for
sensors and also providing a favorable microenvironment for the field application is critical. Materials that are biocompatible,
immobilization of the biomolecules. Furthermore, Au-NPs act as nontoxic and biodegradable are preferable and should be

Please cite this article in press as: Khandelwal, N., et al., Budding trends in integrated pest management using advanced micro- and nano-
materials: Challenges and perspectives, Journal of Environmental Management (2016), http://dx.doi.org/10.1016/j.jenvman.2016.09.071
12 N. Khandelwal et al. / Journal of Environmental Management xxx (2016) 1e13

investigated. It is critical to study both the short-term and long- Agarwal, S., Gupta, V.K., 2015. Ultrasound assisted adsorption of malachite
green dye onto ZnS: Cu-NP-AC: equilibrium isotherms and kinetic stud-
term effects of the formulations on plant physiology to avoid
ieseresponse surface optimization. Sep. Purif. Technol. 156, 780e788.
adverse effects. Moreover, by integrating current agricultural Dawkar, V.V., Chikate, Y.R., Lomate, P.R., Dholakia, B.B., Gupta, V.S., Giri, A.P., 2013.
technology with advancements in nanotechnology, improved crop Molecular insights into resistance mechanisms of lepidopteran insect pests
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de Oliveira, J.L., Campos, E.V.R., Bakshi, M., Abhilash, P., Fraceto, L.F., 2014. Appli-
ronmental and human health effects. cation of nanotechnology for the encapsulation of botanical insecticides for
sustainable agriculture: prospects and promises. Biotechnol. Adv. 32,
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Entomotoxic effect of silica nanoparticles against Sitophilus oryzae (L.). J. Pest
NK thank the Council of Scientific and Industrial Research (CSIR), Sci. 84, 99e105.
Debnath, N., Mitra, S., Das, S., Goswami, A., 2012. Synthesis of surface functionalized
Government of India, New Delhi for Senior Research Fellowship. silica nanoparticles and their use as entomotoxic nanocides. Powder Technol.
Project funding under CSIR network programs in XII plan (BSC0107 221, 252e256.
and BSC0120) to National Chemical Laboratory is greatly Dunse, K.M., Stevens, J.A., Lay, F.T., Gaspar, Y.M., Heath, R.L., Anderson, M.A., 2010.
Coexpression of potato type I and II proteinase inhibitors gives cotton plants
acknowledged. JK would like to acknowledge financial support
protection against insect damage in the field. Proc. Natl. Acad. Sci. U. S. A. 107,
Department of Biotechnology, Government of India, New Delhi. 15011e15015.
AVB acknowledges the Director CSIR-NCL and CSMCRI for allowing Forim, M.R., Costa, E.S., da Silva, M.F.D.F., Fernandes, J.B., Mondego, J.M., Boica, A.L.,
to publish this work and Science and Engineering Research Board, 2013. Development of a new method to prepare nano-/microparticles loaded
with extracts of Azadirachta indica, their characterization and use in controlling
Department of Science and Technology, Government of India for Plutella xylostella. J. Agric. Food Chem. 61, 9131e9139.
funding. We thank Dr. Bhushan Dholakia, for editorial assistance. Ghaedi, M., Khafri, H.Z., Asfaram, A., Goudarzi, A., 2016. Response surface meth-
odology approach for optimization of adsorption of Janus Green B from aqueous
solution onto ZnO/Zn (OH) 2-NP-AC: kinetic and isotherm study. Spectrochim.
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Please cite this article in press as: Khandelwal, N., et al., Budding trends in integrated pest management using advanced micro- and nano-
materials: Challenges and perspectives, Journal of Environmental Management (2016), http://dx.doi.org/10.1016/j.jenvman.2016.09.071