Review

Botanical insecticides inspired by

plant–herbivore chemical interactions
Saber Miresmailli1 and Murray B. Isman2
1
Center for Teaching, Learning and Technology, University of British Columbia, 1961 East Mall, Vancouver, BC, V6T1Z4, Canada
2
Faculty of Land and Food Systems, University of British Columbia, 2357 Main Mall, Vancouver, BC, V6T1Z4, Canada

Plants have evolved a plethora of secondary chemicals to In this review, we focus on botanical insecticides that
protect themselves against herbivores and pathogens, are inspired by plant–insect chemical interactions. We
some of which have been used historically for pest man- briefly look at the phytochemicals that have been used
agement. The extraction methods used by industry ren- for pest management and compare these with conventional
der many phytochemicals ineffective as insecticides (synthetic) pesticides and examine the different ways that
despite their bioactivity in the natural context. In this plants use their secondary chemicals in nature in contrast
review, we examine how plants use their secondary che- to how we use them for pest management. We also discuss
micals in nature and compare this with how they are used the practical challenges of producing commercial botanical
as insecticides to understand why the efficacy of botanical insecticides and examine certain assumptions behind com-
insecticides can be so variable. If the commercial produc- mercial botanical insecticides that are available on the
tion of botanical insecticides is to become a viable pest market.
management option, factors such as production cost,
resource availability, and extraction and formulation Botanical insecticides
techniques need be considered alongside innovative ap- All living organisms share certain chemicals and biochem-
plication technologies to ensure consistent efficacy of ical reactions that constitute their basic metabolism: for
botanical insecticides. example, nucleic acids, proteins, and particular carbohy-
drates. In addition to the substances that participate in
Phytochemicals this primary metabolism, plants have also evolved diverse
Although plants are sessile organisms and cannot escape secondary metabolic pathways that produce a plethora of
danger in the way that animals do, they are not completely novel substances. Most secondary metabolites are pro-
defenseless. Plants have different forms of defense, rang- duced from universally present precursors and, therefore,
ing from structural traits [1] and barriers [2] to physiologi- they are often classified based on their biosynthetic path-
cal [3] and chemical defensive mechanisms [4]. For ways [17]. Using a simplified classification, they can be
decades, researchers have been studying the defensive classified as nitrogen-containing compounds, phenolics,
mechanisms that plants use against different enemies, polyacetates, and terpenoids (Box 1).
the variety of defensive responses, and the evolution and Pesticidal compounds exist within almost all classes of
ecological impact of those responses [5–9]. Although the secondary metabolite. For example, the alkaloids nicotine
evolutionary raison d’être of those traits is to protect plants [which is found in the nightshade (Solanaceae) family of
from herbivores and pathogens in nature, humans have plants] and strychnine (which is found in the seeds of
also found many uses for them. Plant secondary chemicals Strychnos spp.) have been historically used as pesticides
are of particular interest because they can be used as [18]. However, the only new botanical pesticides that have
medicines [10], food- and beverage-flavoring agents, fra- come on the North American market over the past 20 years
grances, textile dyes, hygiene products [11], and pest and are those based on the terpenoid azadirachtin [a limonoid
disease management tools [12]. Plants produce a wide found in seeds of the Indian neem tree (Azadirachta indica;
spectrum of chemicals in various tissues above and below Meliaceae)], which has been used traditionally to control
ground that are used not only to defend themselves against pests and diseases [19], and those based on plant essential
biotic or abiotic stressors [13,14], but also to communicate oils [20], which are used as contact toxicants, fumigants,
with other plants [15] and organisms [16] (Box 1). attractants, and repellents to control agricultural pests (i.e.,
two-spotted spider mite, green peach aphid, and greenhouse
whitefly), urban pests (i.e., housefly, bedbug, cockroaches,
Corresponding author: Isman, M.B. ([Link]@[Link]). and ants), medical pests (i.e., mosquitoes, ticks, and lice) and
Keywords: botanical pesticides; herbivore–plant interactions; pesticide formulation. veterinary pests (i.e., fleas and horseflies).
1360-1385/$ – see front matter
ß 2013 Elsevier Ltd. All rights reserved. [Link] Production of botanical insecticides versus synthetic
002
pesticides
Botanical insecticides are generally complex mixtures of
several, often closely related secondary metabolites that
may or may not have an important role in the toxicity of the
Trends in Plant Science, January 2014, Vol. 19, No. 1 29
Review Trends in Plant Science January 2014, Vol. 19, No. 1

Box 1. Major classes of secondary metabolite used in commercial botanical pest management products
Plants have evolved diverse groups of chemicals that act as major specific chemical signals [45,47,79]. They can even respond
barriers to herbivory. Some chemicals are constitutive [39], meaning chemically to herbivore oviposition before feeding damage occurs
that they are always present, whereas others are induced after attack [80,81].
[40]. Many compounds directly affect the herbivore, whereas others The most important botanical pesticides on the market in
attract organisms from other trophic levels [44]. These chemicals can commercial terms are pyrethrum, neem, and essential oil-based
be found in, and are emitted from, all plant tissues above and below products (Figure I). Essential oil-based products are the most
ground: toxic terpenes and volatile infochemicals are emitted from diverse among the three different types. They are complex
the foliage [73,74]; flowers have behavior-modifying floral scents [75]; mixtures of low-molecular-weight, highly volatile secondary
phytotoxic root exudates are exuded from roots [76,77]; and toxic metabolites. Owing to their versatile nature, they have been used
latex is exuded from the stem [78]. in variety of products, from contact toxicants to fumigants and
Plants have the capacity to convey certain information even in behavior-modifier products, such as attractants and
about herbivores to their natural enemies via the emission of repellents.

Major classes of plant compound Examples of botanical pest Modes of applicaon

important for plant chemical management products
interacons
Contact
Nitrogen containing compounds, i.e., Nicone, toxicants
alkaloids, glucosinolates strychnine
Fumigants
Phenolics, i.e., simple phenols, flavonoid Rotenone
Repellents
Terpenoids, i.e., monoterpenes, Neem, pyrethrum, Anfeedants
sesquiterpenes, limonoids essenal oils
Anmicrobial
Polyacetates, i.e., polyacetylenes
Aractants

TRENDS in Plant Science

Figure I. Examples of botanical pest management products based on major classes of plant compound.

mixture. They can exhibit internal interactions in the form to compensate for scarce and/or expensive ingredients that
of synergy or antagonism, which can affect the overall are not readily available to maintain the competitiveness of
toxicity of the mixture [21]. By contrast, synthetic pesti- the product. Thus, the availability of the ingredients in the
cides are generally based on a single active ingredient market dictates the scalability of botanical products. This is
(Table 1). not the case for synthetic pesticides.
The most important difference between the production Botanical extracts and essential oils often comprise
of botanical insecticides and the manufacture of synthetic lipophilic and highly volatile constituents and are known
pesticides is the difficulties associated with standardizing to be susceptible to conversion and degradation reactions,
the active ingredients found in botanical pesticides: there such as oxidative and polymerization processes, which can
can be great variability in the quality and composition of result in loss of quality and of certain properties [29]. The
these toxic plant extracts. The source of this variability stability of these substances is affected when exposed to
might be natural [22–25] or might occur as a result of elements such as air, light, and elevated temperatures [30].
using different harvest or extraction methods [26,27]. The For this reason, the residual effects of botanical insecti-
initial biomass resource is generally outsourced and min- cides can be limited and, in some cases, lacking entirely.
imally monitored, in contrast to quality-control protocols Despite these limitations, the use of botanical insecti-
that exist for synthetic pesticides. The extracts are usu- cides in California between 2006 and 2011 grew by almost
ally specified based on the level of one or two marker 50% ([Link]
compounds (putatively the active principles) even though pdf and [Link]
the presence and level of other constituents in the mix- [Link]), in part because the public perceives natural pro-
ture can significantly influence the overall toxicity and ducts to be safer than synthetic chemicals, despite evidence
efficacy of the extract [21]. As a result of limited chemical to the contrary [31]. To put this in context, botanical
standardization, the efficacy of botanical products may insecticide use represents only 5.2% of biopesticides, and
not be consistent [28]. However, synthetic pesticides do only 0.04% of all pesticide use in California [32]. Biopes-
not have these problems owing to their simpler composi- ticides represent approximately 2% of the US$60 billion
tional structure compared with that of botanical insecti- global pesticide market (2012 estimate), but the segment is
cides, and the degree of control and standards relating to dominated by microbial insecticides led by products based
their manufacture. on Bacillus thuringiensis [33]. The biopesticide segment is
Scalability limitation can also be an issue for manufac- currently growing at 16% per year, compared with conven-
turers of botanical insecticides and depends on natural tional agrochemicals that are growing at a rate of 5.5% per
resource availability. Formulations may have to be changed year [34].
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Review Trends in Plant Science January 2014, Vol. 19, No. 1

Table 1. Commercial botanical pesticides versus conventional synthetic pesticides

Differentiators Botanical pesticides Synthetic pesticides Refs
Active ingredients Mixture of several secondary metabolites with various Usually one or two active ingredients with specific mode [21,82]
modes of actions. Concentration of active ingredients in of action, for example neurotoxins. Usually small
the final product must be at certain level (usually higher amount of active ingredient is needed in the final
than synthetic pesticides) to be effective product for effective control
Manufacturing Simple extraction methods and blending; enzymatic Multistep synthesis of active ingredients; various [83,84]
alterations of some secondary products by enzymes formulations; in-house production
such as peroxidases and polyphenol oxidase may occur
during extraction; materials are usually outsourced;
various formulations
Scalability Limited, depending on availability of biomass; limited Scalable for mass production; rigorous standards in
chemical standardization place
Shelf life Limited, can breakdown and/or change over time Relatively stable and/or long shelf life [30]
Production cost Variable, depending on biomass availability and/or Generally lower than commercial botanical pesticides,
market price especially off-patent
Application Limited applications in urban, medical, stored products, Various applications in almost all pest management [28]
forestry, and large-scale agriculture sectors
Regulatory hurdles Exemptions in some jurisdictions, certain products still Require full registration
require full registration
Social hurdles Generally considered safe Generally considered harmful
Marketing channels Mostly retail and limited agriculture Retail and large-scale agriculture, aviation, and military

Regulatory exemptions such as that provided by List when needed [for example, dhurrin, a cyanogenic glyco-
25(b) of the Federal Insecticide, Fungicide, and Rodenti- side, in sorghum (Sorghum bicolor) can produce hydrogen
cide Act (FIFRA) of the US Environmental Protection cyanide upon herbivore damage as a result of enzymatic
Agency (EPA), which allows certain essential oils and inert degradation] or, (ii) store the toxic chemicals in specific
materials to be used as pesticide active ingredients without protected cell compartments, such as vacuoles to prevent
regulatory review, has facilitated the commercialization of self-toxicity [for example, in white melilot (Melilotus alba),
some essential oil-based pesticides in the USA over the the tonoplast and the plasmalemma separate glucosino-
past decade. Many of the essential oils and their products lates from enzymes that can produce toxic mustard oil]
are included in the Generally Recognized as Safe (GRAS) [41]. Plants have also evolved special anatomical features
list, which have been approved by the US Food and Drug to release toxic chemicals. For example, some plants have
Administration (FDA) and the US Environmental Protec- evolved glandular trichomes that contain highly special-
tion Agency (EPA) for food and beverage consumption. ized secretory cells that synthesize and accumulate a
However, to determine whether we are benefiting from variety of secondary metabolites. The glandular trichomes
the full potential of these natural substances, we believe of some plants can continuously exude secretions, for
that we need to look at their source and see how they are example, capitate trichomes, such as those of tobacco
used in their natural context. (Nicotiana tabacum.), whereas others are touch sensitive
and release the toxic materials, when ruptured, to trap and
Secondary metabolites: use in pesticides versus use by kill small arthropods, for example, peltate trichomes of the
plants Lamiaceae (mint family) [42,43].
Millions of years before humans became the dominant In the case of induced chemical responses, plants exhibit
species on the planet, plants started to evolve sophisticated a strong degree of specification and control. Plants can
defensive mechanisms. The diversification of flowering respond differentially to different types of herbivore [44]
plants during the Cretaceous period (circa 145 million– and through those responses, change the behavior of pred-
66 million years ago) is associated with a sudden burst of atory and parasitic arthropods that use those chemicals as
speciation and adaptive radiation of insects that acted as a cues to find their prey [45]. Plants can also use their
major selective force in plant evolution, and led to selection volatile chemicals to signal pest density, location of pests
of plants that had defensive adaptations [35]. Plant–insect in the canopy, and the duration of damage [46–48]. Fur-
coevolution has been the subject of several studies thermore, plants can control the composition and emission
[1,5,6,36–38] and several defensive traits have been iden- rates of their volatile chemicals [49–51].
tified that plants coevolved as a result of interacting with Destructive extraction of these chemicals from plant
coevolving insect herbivores [2,4]. For the purpose of this tissues negates most of these traits. Simply put, we render
review, we only explore traits and features that plants use millions of years of plant evolution, chemical specification,
specifically for chemical defense (Figure 1). compartmentalization, and structural development use-
Chemical defenses in plants can be constitutive, mean- less by crudely combining all the extractable phytochem-
ing that the toxic chemicals are always present [39], or icals together. To take better advantage of the attributes of
specifically induced after herbivore attack [40]. Some these secondary metabolites in the production of bio-in-
plants have evolved specific ways of storing toxic chemicals spired botanical insecticides, we must first closely examine
to protect themselves from their harmful effects by follow- the underlying assumptions that are made when develop-
ing two different strategies. Plants either (i) store less-toxic ing these products and then address the practical chal-
precursors, which are transformed into active toxins only lenges and limitations.
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 Review Trends in Plant Science January 2014, Vol. 19, No. 1

Ready mix Specific structure

Storage Release
Compartmentalized Emission control

Environmental condions Constuve

Locaon on canopy
Induced
Density

Stressor characteriscs Stressor type

Damage duraon Different responses

Plant developmental stage

TRENDS in Plant Science

Figure 1. Factors affecting the elicitation of different secondary metabolites in plants. Plants have evolved specific traits that enable them to control and use their chemical
arsenal robustly. They have perfected these traits over millions of years of evolution. However, most of these traits are destroyed by crude extraction techniques.

Practical challenges and opportunities traders significantly process these products by, for exam-
Developing standards, addressing chemical variation, ple, blending and filtration. This issue might also be a
blending and fortification: what is natural? concern for regulatory agencies. At this point, there is no
Botanical extracts and plant essential oils comprise sever- official definition or criteria as to what constitutes a natu-
al potentially bioactive constituents. Rosemary (Rosmar- ral essential oil despite the variability in their composition.
inus officinalis) oil for instance, comprises more than 50 By creating standard criteria for botanical product compo-
different constituents, of which approximately ten are sition, extraction methods, blending, or fortification, it
considered major compounds that determine specific char- might be possible to achieve greater uniformity in pestici-
acteristics of the oil. In addition to these major compounds, dal efficacy.
minute amounts of other compounds may also be present in
the mixture and these can have an active role in the Stability and formulation methods
bioactivity of the total mixture [21]. The composition of Compared with synthetic pesticides, botanical insecticides
plant essential oils is influenced by, for example, season, are relatively unstable and breakdown significantly faster
geography, harvest time, species chemotype, and extrac- when exposed to the elements, such as light, temperature,
tion methods [22–27]. Plants can also actively change the and air [30]. Constituents of botanical extracts originate
composition of their volatile organic compounds in re- from different biosynthetic pathways. Aromatic phenylpro-
sponse to minute changes in their microclimate [49]. Most panoids are formed via the shikimic acid pathway resulting
botanical insecticide manufacturers outsource their essen- in phenylalanine, whereas terpenoids are derived from the
tial oils and usually screen for one or two marker com- C5 building blocks isopentenyl diphosphate (IPP) and its
pounds to determine the quality. To compensate for isomer dimethylallyl diphosphate (DMAPP) [53–55]. Once
variability in the composition of essential oils and to create plant chemicals have been removed from their protective
a uniform mixture with a known level of key compounds, compartments as a result of destructive extraction meth-
essential oil traders and botanical pesticides manufac- ods, their constituents are prone to oxidative damage,
turers resort to blending essential oils of different origin chemical transformations, or polymerization reactions.
to obtain the desired mixture. A greater understanding of Furthermore, as plant extracts age, their quality declines
the role of each constituent in the overall bioactivity of the further. Over time, they might lose some of their attri-
mixture could enable manufacturers to create more effec- butes, such as odor, flavor, color, and consistency [56,57].
tive blends and mixtures with relatively consistent efficacy The compositional diversity of the botanical extracts and
[52]. the instability of their constituents can make botanical
It is also possible to fortify essential oils and botanical insecticides unsuitable for applications where residual
extracts with certain compounds that naturally occur in effects over long periods of time are desirable.
these mixtures to maintain a desired overall composition. To overcome the instability of botanical extracts and
However, can fortified mixtures be considered natural? essential oils when used as pesticides, several formulation
This might be a concern for consumers that perceive techniques and methods have been developed and deployed
‘natural products’ to be ‘pure, unadulterated substances’ in recent years. Microencapsulation, for example, is a meth-
even though large-scale essential oil and botanical product od that is used to protect sensitive materials that can easily
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Review Trends in Plant Science January 2014, Vol. 19, No. 1

suffer degradation [58]. Encapsulation techniques can be mixtures. Sophisticated extraction methods based on phys-
divided into three classes: (i) chemical processes, such as ical [67], biological [68], and chemical [69] techniques allow
molecular inclusion or interfacial polymerization [59]; (ii) greater control over the composition of plant extracts and
physicochemical techniques, such as coacervation and lipo- provide opportunities for selective extraction of specific
some encapsulation [60]; and (iii) physical processes, such as bioactive compounds [70]. However, because of their com-
spray drying, spray chilling or cooling, co-crystallization, plexity and cost, these methods have not yet been adopted
extrusion, or fluidized bed coating [61,62]. Microencapsula- for the mass production of plant extracts by most botanical
tion techniques are generally used to prepare pesticide product producers. For example, traditional steam distil-
nanoemulsions that provide some level of controlled release lation is still a preferred method for obtaining essential oils
of the botanical active ingredient [63]. in many countries that mass-produce essential oils [12].
These microencapsulation techniques generally slow Further research is needed to develop advanced extraction
down the release or decay of the entire mixture that is methods that are simple and economically viable yet pro-
obtained by the destructive extraction of plant tissues; vide adequate levels of control of the composition of botan-
however, no specific attention is paid to the behavior of ical extracts.
individual constituents of the mixture. By contrast, plants The second area relates to novel formulation methods
rely on specific structural features, cellular compartments, that mimic the chemical compartmentalization and storage
and chemical pathways to control proactively the produc- capacity of plants. Compartmentalization of drug substrates
tion, storage, and release of individual compounds within to prevent unwanted reactions is a common practice in the
their defensive chemical arsenal [50,51,54,55]. Novel tech- development of pharmaceuticals [71]. The compartments
nologies that consider the behavior and control level of can be formed in various sizes from a visible to a nano-scale
individual constituents of botanical insecticides are paving [63,72]. The same techniques that have been successfully
the way for a new generation of botanical insecticides that used in pharmaceuticals can be used for enhancing pesticide
are applied in a manner that is closer to the natural formulations. The main challenge for incorporating these
defense methods used by plants against herbivores [64]. techniques for industrial botanical insecticide production is
again, cost and complexity. Although the effectiveness and
Botanical insecticides: stand-alone solutions or innovative aspects of a product are well regarded in certain
complementary supplements? societies, cost and economic viability are still the primary
The defensive arsenal of plants extends beyond chemical factors that determine the commercial success of a product;
barriers [2,3,5]. Phytochemicals often work in harmony therefore, more research is needed to find economical solu-
with other means of defense to protect plants from herbi- tions and novel formulation methods that address the
vores. However, does maximizing the efficacy of botanical compartmentalization issue yet maintain commercial com-
insecticides by producing more potent versions of phyto- petitiveness of botanical insecticides.
chemical mixtures via blending and fortification, despite The third area is the development of advanced technol-
the higher cost, provide a better option than integrating ogies and delivery methods that provide qualitative and
botanical products with other methods of pest manage- quantitative release control at the level of individual con-
ment? Botanical insecticides have been successfully used stituents. In recent years, micro- and nanoencapsulation
in combination or rotation with synthetic pesticides [20] techniques have been investigated as means of providing
and biological control agents [65,66]. Owing to their insta- controlled release of botanical insecticides [58–62]. These
bility and lack of residual toxicity, botanical pesticides can technologies can extend the efficacy of botanical insecti-
be easily incorporated into integrated pest management cides over longer periods of time. Despite these formulation
programs along with biological control agents. A closer look advances, the controlled release remained at the whole
at the role of phytochemicals in plant–insect interactions formula mixture level without addressing differences in
across different trophic layers could inspire further devel- volatilization and biological characteristics of individual
opment of effective integrated solutions. Considering the constituents of botanical materials used in production of
relatively higher cost of botanical insecticides and their botanical insecticides. A better understanding of the be-
scalability limitations, the integrated use of botanical havior and bioactivity of individual components of botani-
insecticides with other control measures could be a more cal insecticides coupled with more advanced methods of
economically viable option both for consumers and pest compartmentalization and formulation will allow greater
management solution providers. degrees of control over the availability and activity of
individual components of complex botanical mixtures
Concluding remarks and outlook and, consequently, should enhance the efficacy of botanical
Most botanical insecticides are based on toxic chemicals insecticides.
that plants generate as part of their constitutive defensive
arsenal. Many phytochemicals are induced by herbivore Disclaimer statement
attack on demand when needed; however, our strategies S.M. was formerly the executive science officer and is a shareholder at
for using commercial pesticides do not emulate this partic- Sumatics, LLC based in New York, NY, USA. Through Sumatics, Saber
ular type of defensive behavior. Miresmailli filed a patent on ‘‘Apparatus and method for controlled release
We have identified three important areas for future of botanical fumigant pesticides’’ which is still under revision at the US
patent office. Prior to that, S.M. was a member of the Scientific Advisory
research to improve the efficacy of botanical insecticides. Panel for EcoSMART Technologies Inc., based in Roswell, GA, USA,
The first is improved extraction methods with specific providing consultation and scientific advise on the development of novel
attention to preserving the integrity of phytochemical botanical pesticides. In collaboration with Scientific Animations Without

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Review Trends in Plant Science January 2014, Vol. 19, No. 1

Boarders (SAWBO- University of Illinois at Urbana-Champaign), using 23 Duarte, A.R. et al. (2009) Seasonal influence on the essential oil
funds from EcoSMART Technologies, S.M. produced educational anima- variability of Eugenia dysenterica. J. Braz. Chem. Soc. 20, 967–974
tions promoting safe botanical pesticides and the correct way of using, 24 Sáez, F. (1995) Essential oil variability of Thymus zygis growing wild in
handling, and storing insecticides. M.B.I. formerly served as a member of southeastern Spain. Phytochemistry 40, 819–825
the Scientific Advisory Panel for EcoSMART Technologies Inc. He has 25 Azevedo, N.R. et al. (2001) Chemical variability in the essential oil of
conducted research on botanical insecticides for over 30 years, supported Hyptis suaveolens. Phytochemistry 57, 733–736
by EcoSMART Technologies, BC Chemicals Ltd., Safer Ltd., Arbokem Inc., 26 Rohloff, J. et al. (2005) Effect of harvest time and drying method on
and PheroTech Inc. in addition to several government-funding agencies. biomass production, essential oil yield, and quality of peppermint
He currently receives support from SemiosBIO Technologies Inc. and is a (Mentha  piperita L.). J. Agri. Food Chem. 53, 4143–4148
consultant to DE Laboratories Inc. He is currently consulting on the 27 Djouahri, A. et al. (2013) Effect of extraction method on chemical
development of essential oil-based insecticides for a university in China composition, antioxidant and anti-inflammatory activities of
and a Government institute in Cuba and serves as an international advisor essential oil from the leaves of Algerian Tetraclinis articulata (Vahl)
to an European Union-funded project on the utilization of plant pesticides Masters. Ind. Crop Prod. 44, 32–36
for several countries in sub-Saharan Africa. 28 Isman, M.B. (2005) Problems and opportunities for the
commercialization of botanical insecticides. In Biopesticides of Plant
Acknowledgments Origin (Regnault-Roger, C. et al., eds), pp. 283–291, Intercept Ltd.
This work was supported by a Natural Sciences and Engineering 29 Sell, C. (2010) Chemistry of essential oils. In Handbook of Essential
Research Council of Canada Discovery grant (11-2729) to M.B.I. Oils. Science, Technology, and Applications (Baser, K.H. et al., eds), pp.
121–150, CRC Press
30 Turek, C. and Stintzing, F.C. (2013) Stability of essential oils: a review.
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