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Botanical Pesticides and Their Mode of Action

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DOI: 10.1007/s10343-013-0308-3

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Botanical Pesticides and Their Mode of
Action

Nabil E. El-Wakeil

Gesunde Pflanzen
Pflanzenschutz - Verbraucherschutz -
Umweltschutz

ISSN 0367-4223
Volume 65
Number 4

Gesunde Pflanzen (2013) 65:125-149

DOI 10.1007/s10343-013-0308-3

1 23
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1 23
Gesunde Pflanzen (2013) 65:125–149
DOI 10.1007/s10343-013-0308-3

R e v i e w A rt i c l e

Botanical Pesticides and Their Mode of Action

Nabil E. El-Wakeil

Received: 26 August 2013 / Accepted: 1 October 2013 / Published online: 3 November 2013
© Springer-Verlag Berlin Heidelberg 2013

Abstract  Pest management is facing economic and eco- use in organic food production in industrialized countries
logical challenge worldwide due to human and environ- but can play a much greater role in the production and
mental hazards caused by majority of the synthetic pesti- postharvest protection of food in developing countries.
cide chemicals. Identification of novel effective insecticid- Botanicals have been in use for a long time for pest con-
al compounds is essential to combat increasing resistance trol. The compounds offer many environmental advantag-
rates. Botanical pesticides have long been touted as attrac- es. However, their uses during the 20th century have been
tive alternatives to synthetic chemical pesticides for pest rather marginal compared with other bio-control methods
management because botanicals reputedly pose little threat of pests and pathogens. Improvement in the understanding
to the environment or to human health. The body of scien- of plant allelochemical mechanisms of activity offer new
tific literature documenting bioactivity of plant derivatives prospects for using these substances in crop protection. I’m
to arthropod pests continues to expand, yet only a hand- trying in this article to present different kinds of botanical
ful of botanicals are currently used in agriculture in the pesticides came from different recourses and their mode
industrialized world, and there are few prospects for com- of actions as well as I will try to examine the reasons be-
mercial development of new botanical products. Pyrethrum hind their limited use (disadvantages) and the actual crop
and neem are well established commercially, pesticides protection developments involving biopesticides of plant
based on plant essential oils have entered the marketplace, origin for organic or traditional agricultures to keep our
and the use of rotenone appears to be waning. A number environment clean and safer for humankind and animals.
of plant substances have been considered for use as pest
antifeedants, repellents and toxicants, but apart from some Keywords  Plant-biopesticide · Pyrethrum · Neem ·
natural mosquito repellents, a little commercial success has Essential oils · Antifeedants · Repellents
ensued for plant substances that modify arthropod behav-
ior. Several factors appear to limit the success of botani-
cals, most notably regulatory barriers and the availability Botanische Pestizide und ihre Wirkmechanismen
of competing products (newer synthetics and fermentation
products) that are cost-effective and relatively safe com- Zusammenfassung  Die Schädlingsbekämpfung mit che-
pared with their predecessors. In the context of agricultural misch-synthetischen Pestiziden steht weltweit vor wirt-
pest management, botanical pesticides are best suited for schaftlichen und ökologischen Herausforderungen. Die
Identifizierung neuer effektiver insektizider Verbindungen
ist wichtig, um die zunehmend auftretenden Resistenzen zu
N. E. El-Wakeil ()
Pests and Plant Protection Department, bekämpfen. Botanische Pestizide sind seit langem als at-
National Research Centre, Dokki, Cairo, Egypt traktive Alternativen zu chemisch-synthetischen Pestiziden
e-mail: [email protected] zur Schädlingsbekämpfung angekündigt worden, weil Pes-
tizide aus pflanzlicher Herkunft weniger Gefahren für die
N. E. El-Wakeil
Institute of Agricultural and Nutritional Sciences, Umwelt und/oder die menschliche Gesundheit birgen. Die
Martin Luther-University Halle-Wittenberg, Germany wissenschaftliche Literatur dokumentiert eine Vielzahl von

13
126 N. E. El-Wakeil

Untersuchungen zur Bioaktivität pflanzlichen Stoffe deren

Derivate geeignet sind, gegen Arthropoden als Schädlinge
eingesetzt zu werden. Aktuell werden aber nur eine Hand-
voll pflanzlicher Stoffe in der Landwirtschaft in den Indus-
trieländern verwendet. Es gibt nur wenige Hinweise auf
eine wirtschaftliche Entwicklung der neuen botanischen
Produkte. Zum Beispiel sind die Wirkstoffe Pyrethrum und
Neem kommerziell gut etabliert und auch Pestizide auf Ba-
sis pflanzlicher ätherischer Ölen sind am Markt zu finden.
Der Einsatz von Rotenon scheint aufgrund von Nebenwir-
kungen zu schwinden. Eine Reihe von pflanzlichen Subs- Fig. 1  Pest resistance increases with repeated exposure products from
tanzen sind interessant für den Einsatz als Fraßhemmer, the same chemical family (cited from Gilkeson and Adams 2000)
und als Repellents, aber abgesehen von einigen natürlichen
Insektenschutzmitteln gibt es kaum kommerziellen Einsatz botanicals from an important role in agriculture to an essen-
für die pflanzlichen Substanzen. Mehrere Faktoren begren- tially trivial position in the marketplace among crop protec-
zen den Erfolg von pflanzlichen Stoffen, hier sind zum tants. However, history also shows that overzealous use of
Beispiel regulatorische Barrieren zu nennen. synthetic pesticides led to numerous problems unforeseen at
Im Zusammenhang mit der landwirtschaftlichen Schäd- the time of their introduction: acute and chronic poisoning
lingsbekämpfung, sind botanische Pestizide bestens für den of applicators, farmworkers, and even consumers; destruc-
Einsatz in der ökologischen Bio-Produktion in den Indust- tion of fish, birds, and other wildlife; disruption of natural
rieländern geeignet, sie können aber auch eine größere Rol- biological control and pollination; extensive groundwater
le bei der Begrenzung von Nachernte- und Lagerverlusten contamination, potentially threatening human and environ-
spielen. Die Verbindungen bieten viele Vorteile für die Um- mental health; and the evolution of resistance to pesticides
welt. Allerdings sind ihre Anwendungen im 20. Jahrhundert in pest populations (Casida 1973; McLaughlin 1973; Marco
eher marginal im Vergleich zu anderen Verfahren zur Kont- et al. 1987; Forget et al. 1993; Perry et al. 1998).
rolle von Schädlingen und Krankheitserregern. Die Verbes- Authorities responded to these problems with regulatory
serungen bei der Aufklärung der Mechanismen der Pflanzen action, replacing chemicals of concern with those demon-
mit allelochemischer Aktivität bieten neue Perspektiven für strated to pose fewer or lesser risks to human health and
die Verwendung dieser Stoffe als Pflanzenschutzmitteln. In the environment. In the United States, these policies are
dem vorliegenden Artikel werden verschiedene Wirkme- reflected by the definition of “reduced risk” pesticides by
chanismen von Bio-Pestiziden vorgestellt und Gründe für the Environmental Protection Agency in the early 1990s
den derzeit begrenzten Einsatz genannt. with their favored regulatory status, and by the Food Qual-
ity Protection Act in USA, which, in reappraising safe lev-
Schlusswörter  Biopestizide · Pyrethrum · Neem · els of pesticide residues in foods, is having the net effect
Ätherische Öle · Repellents of removing most synthetic pesticides developed before
1980 from use in agriculture. These changes in the regu-
latory “environment” appeared to heighten the impetus for
Introduction the discovery and development of alternative pest manage-
ment products—those with reduced health and environ-
Pesticides are the cornerstones upon which the pest man- mental impacts—including pesticides derived from plants.
agement practices are based, and are likely to remain so as Indeed, the scientific literature of the past 25 years describes
long as effective and inexpensive chemicals are available hundreds of isolated plant secondary metabolites that show
(Haynes 1988). The practice of using plant derivatives, or feeding deterrent or toxic effects to insects in laboratory
botanical pesticides as we now know them, in agriculture bioassays, and botanical pesticides have been the subject
dates back at least two millennia in ancient Egypt, China, of several recent volumes (Dev and Koul 1997; Hedin
Greece, and India (Ware 1983; Thacker 2002). Even in et al. 1997; Prakash and Rao 1997; Koul and Dhaliwal
Europe and North America, the documented use of botani- 2001; Regnault-Roger et al. 2005) and also it takes several
cals extends back more than 150 years, dramatically predat- steps to get a commercial product as shown in Fig. 2. There
ing discoveries of the major classes of synthetic chemical are many factors determining using the botanical pesticides
pesticides (e. g. organochlorines, organophosphates, carba- for pest control as reported by Deng et al. (2009).
mates, and pyrethroids) in the mid-1930s to 1950s which Botanical pesticides are also used in organic garden-
had caused many environmental problems as insect resis- ers, in some cases, over synthetic organic materials. In
tances Fig.  1. Synthetic pesticides effectively relegated general, they act quickly, degrade rapidly and have, with

13
Botanical Pesticides and Their Mode of Action 127

Fig. 2  Steps and interactions

between stages from discovery of
a biocide to approved field appli-
cation (cited from Brown 2005)

a few exceptions, low mammalian toxicity. Products con- Certain essential plant oils, widely used as fragrances and
taining ingredients derived from plants (Table 1) are consid- flavors in the perfume and food industries, have long been
ered pesticides. However, products containing these active reputed to repel insects. The investigations in several coun-
ingredients must be registered for use by the Environmen- tries confirm that some plant essential oils not only repel
tal Protection Agency (EPA) in USA as well by Ministry of insects, but have contact and fumigant pesticidal actions
Agricultural and Land Reclamation in Egypt. against specific pests, and fungicidal actions against some

13
128 N. E. El-Wakeil

Table 1  Toxicity of certain botanical pesticides (mg/kg) with potential for future commercialization, suggest why so
Generic name Oral LD50 Dermal LD50 Signal word few botanicals reach the marketplace, and finally suggest in
Nicotine 50–60 50 Danger what contexts botanicals could prove effective in the years
Rotenone 60–1.500a 940–3.000 Caution to come and their distribution on many countries over the
Sabadilla 4.000 – Caution world as appeared in Table 2.
Ryania 750–1.200 4.000 Caution
Pyrethrins 1.200–1.500 > 1.800 Caution
d-Limonene > 5.000 – Caution Definitions
Linalool 2.440–3.180 3.578–8.374 Caution
Neem 13.000 – Caution
Definition of Pesticides
a
Toxicity varies greatly depending on type of solvent used as carrier

Chemical substance designed to kill or retard the growth

Table 2  Botanical insecticides approved for use in specific countries of pests that damage or interfere with the growth of crops,
(Resource (Pesticide Action Network 2004) Pesticide registration by
country) shrubs, trees, timber and other vegetation desired by
Country Pyrethrum Rotenone Nicotine Neema Others humans. Practically all chemical pesticides, however, are
Australia X X – – Citrus oils poisons and pose long-term danger to the environment and
New X X – X humans through their persistence in nature or body tissue.
Zealand Most of the pesticides are non-specific and may kill life
India X X X X Ryania forms that are harmless or useful.
Philippines X – – –
Hungary X – – – Quassia Definition of Botanical Pesticides
Denmark X X – – Lemongrass,
clove, eucalyp-
tus oils Botanical pesticides are naturally occurring chemicals
Egypt X – – X Essential oils, extracted from plants. Natural pesticidal products are avail-
Lemongrass able as an alternative to synthetic chemical formulations but
Germany X – – X they are not necessarily less toxic to humans. Some of the
Nether- X – – – most deadly, fast acting toxins and potent carcinogens occur
lands
naturally (Regnault-Roger et al. 2005; Regnault-Roger and
United X X X –
Kingdom Philogène 2008).
South X – – –
Africa Definition of Mode of Action
Brazil X X – X Garlic
United X X X X Essential oils, Mode of action refers to the specific biochemical interac-
States ryania, sabadilla tion through which a pesticide produces its effect. Usually,
Canada X X X – Specified
the mode of action includes the specific enzyme, protein,
essential oils,
Mexico X X – X Garlic, capsicum or biological step affected. While most other classifica-
X Be present, – Be not present tions are the pests controlled, physical characteristics, or
a
Includes insecticides listing azadirachtin as the active ingredient chemical composition, mode of action specifically refers to
which biological process the pesticide interrupts (Khambay
et al. 2003; Bloomquist et al. 2008).
important plant pathogens (Isman 1999, 2000). As part of an
effort aimed at the development of reduced-risk pesticides Why Mode of Action is Important?
based on plant essential oils, toxic and sublethal effects of
some essential oil terpenes and phenols have been investi- Knowing the mode of action is integral for scientists to
gated using the tobacco cutworm (Spodoptera litura) and improve the quality and sustainability of a product. To
the green peach aphid (Myzus persicae) as model pest spe- understand how pesticides work (their mode of action), it
cies (Weinzierl 2000; Isman 2000, 2006). is necessary to understand how the pests’ targeted systems
So far in spite of the large scale of the research projects, normally function. It is also helpful to understand how
only a handful of botanical pesticides are in commercial use human systems function in order to know similarities and
on vegetable and fruit crops today, with significant com- differences between humans and the pests we try to control.
mercial development of only two new sources of botani- Another reason, it is important to understand the modes of
cals in the past 25 years. In this review, current botanicals action of the pesticides we use is to prevent development
and their trends in use, discuss the few botanical materials of pesticide resistance in the target pest(s). Using pesticides

13
Botanical Pesticides and Their Mode of Action 129

with the same mode of action contributes to this problem phosphates, and carbamates). They were easier to handle
by killing the susceptible pests and leaving only those with and less expensive. This situation continued until the 1960s
resistance to the entire class of pesticides that work through (Alburo and Olofson 1987).
similar mechanisms (Brown 2005). But as a result of the many demonstrations of negative
effects on non-target species and environmental risks result-
Historical Background ing from the massive use of chemical pesticides, there was
renewed interest for botanicals. Even if there were substan-
Having observed that some plants protect themselves better tially more efforts devoted to the search and the development
than others, humans developed the use of plants as pesticides. of new synthesized pesticides, research on biopesticides of
Historically, botanicals were used before other kinds of pes- plant origin was actively pursued throughout the second half
ticides. They are mentioned in Hieroglyph, Chinese, Greek, of the 20th century in order to improve their stability or to
and Roman antiquity and also in India where the use of the discover new molecules and new sources of molecules. This
neem tree (Azadirachta indica Juss.; Meliaceae) was reported is well illustrated by the development of pyrethrinoids, syn-
in the Veda, a body of manuscripts written in archaic Sanskrit thesized molecules derived from pyrethrum, and of neem
dated at least 4,000 years ago (Philogène et al. 2005). It is (Meliaceae), during the entire 20th century.
thus difficult to assess exactly where and when plants or plant
extracts were systematically used in plant protection or, more
generally, in agriculture. In the 18th century, some publica- Factors Affecting Use of Botanical Pesticides
tions dealt with plant-based formulations to control insect
pests (Shepard 1951). At the end of the 19th century, methods 1. Raw material availability
including the use of toxic plants or minerals, oils, tars, sul- 2. Standardization of botanical extracts containing a com-
focalcic sprays, boiling water, and so forth, were commonly plex mixture of active constituents
put into practice (Whittaker and Feeny 1971; Philogène 3. Solvent types, plant species and part of plant
et al. 1984). Integration of empirical and scientific observa- 4. Rapid degradation
tions led to the development of plant extracts. 5. State registration
The first botanicals and allelochemicals to be used as pes- 6. Market opportunities for botanical pesticides
ticides came from easily available products. Pest insects were 7. Weather conditions
targeted more than pathogens because they could be easily
identified. Several recent books and chapters have reviewed There are other factors affecting on synthetic botanical pesti-
biopesticides of plant origin (Copping 2001; Koul and Dhali- cide uses, such as the formulation of the pesticide, the active
wal 2001; Thacker 2002; Regnault-Roger et al. 2005). ingredient, the time of exposure, the direct or indirect con-
The development of botanicals used as pesticides resulted tact, the quantity used the pesticides mixtures, the climate
from two parallel methods: (i) The observation of the tradi- and season of the year when it’s applied, and the person’s
tional uses of plants and extracts for cattle and crop protec- age, amongst others (Henn et al. 1991; Dosemeci et al. 2002).
tion, followed by checking the efficiency of these practices There are environmental indicators, health indicators,
and identification of the active molecules. The activity of and other elements that help determine the exposure risk,
nicotine extracted from tobacco, Nicotiana tabacum and such as the person residence and occupational history, the
rotenone from Leguminosae Lonchocarpus nicou and Der- clinical history, as well as the presence of the pesticides
ris elliptica fall in this category. (ii) A systematic screening studied in drinking water, in the ground, in the atmosphere,
of families of plants collected during prospecting campaigns and in the fresh or processed foods in the region where the
followed by biological tests in order to discover the active studied populations inhabit. The exposure can be increased
molecules. Ryanodine, an alkaloid extracted from Ryania with the daily time dedicated to the activity, as well as the
sp., and marketed in the USA in 1945, is the result of such years of work, the exposure form, the use of protective gear,
prospectings carried out with collaboration between Rutgers and/or the physical proximity of the housing to agricultural
University and Merck in 1940s (Copping 2001). fields (Arcury et al. 2006).
Before the Second World War, four main groups of com-
pounds were in fact commonly used: nicotine and alkaloids,
rotenone and rotenoids, pyrethrum and pyrethrins, and veg- Resources of Botanical Pesticides
etable oils. The use of these substances, because of their
toxicity to nontargeted species (nicotine) or the instability At present there are four major types of botanical products
of molecules (pyrethrum), decreased with the commercial- used for insect control (pyrethrum, rotenone, neem, and
ization of chemically synthesized insecticides developed essential oils), along with three others in limited use (ryania,
during the Second World War (organochlorides, organo- nicotine, and sabadilla). Additional plant extracts and oils

13
130 N. E. El-Wakeil

Table 3  Egyptian medicinal and

aromatic plants, which can be
used as botanical pesticides

(e. g. garlic oil, Capsicum oleoresin) see limited (low vol- Sabadilla, Ryania, Pyrethrum, Plant essential oils; while the
ume) regional use in various countries, but these are not 2nd generation included Synthetic Pyrethroids and Azadi-
considered here, as shown in the following Tables 3 and 4. rachtin, as well Potential New Botanicals as stated by Reg-
nault-Roger et al. (2005) in the book: Biopesticides of plant
Functional and Biological Active Plant Ingredients of origin.
Some Botanical Pesticides
The first Generation of Botanical Pesticides
Functional of botanical pesticides varied from product to
another and from sources to others as appeared in Table 5. Nicotine
Commercial development of pesticides based on plant has been
greatly facilitated by exemption from registration for certain An alkaloid obtained from the foliage of tobacco plants
products commonly used in processed foods (Quarles 1996). (Nicotiana tabacum) and related species, has a long history
This opportunity has spurred the development of botanical as an insecticide. Nicotine (Fig. 3) and two closely related
insecticides, acracides, fungicides, bactericides, nematicides alkaloids, nornicotine and anabasine, are synaptic poisons
and herbicides for agricultural and industrial applications and that mimic the neurotransmitter acetylcholine. As such,
for the consumer market as described by Thibout et al. (1986); they cause symptoms of poisoning similar to those seen
Thibout and Auger (1997); Auger and Thibout (2002). with organophosphate and carbamate insecticides (Hayes
1982; Regnault-Roger and Philogène 2008). Owing to the
extreme toxicity of pure nicotine to mammals (rat oral LD50
Current Botanicals in Use and Their Mode of Action is 50 mg kg−1) and its rapid dermal absorption in humans,
nicotine has seen declining use, primarily as a fumigant
The botanical pesticides could be divided into two gen- in greenhouses against soft-bodied pests. However, there
erations: The 1st generation included Nicotine, Rotenone, remains some interest in preparing stable nicotine fatty acid

13
Botanical Pesticides and Their Mode of Action 131

Table 4  List of plants and their parts used for evaluation of pesticide activities in Thailand (cited from Bussaman et al. 2012a, b)
Scientific name Family Common name Parts
Boesenbergia pandurata Schltr. Zingiberaceae Fingerroot Rhizome
Kaempferia parviflora Wall. Zingiberaceae Belamcanda chinensis Rhizome
Kaempferia pulchra (Ridl.) Ridl Zingiberaceae Peacock ginger, resurrection lily Rhizome
Zingiber zerumbet (L.) Smith. Zingiberaceae Wild ginger, Martinique ginger Rhizome
Zingiber officinale Roscoe. Zingiberaceae Ginger Rhizome
Zingiber montanum (Koenig) Link Zingiberaceae Phlai, cassumunar Rhizome
Alpinia galanga (L.) Swartz. Zingiberaceae Kha, galingale, galangal Rhizome
Curcuma longa Linn. Zingiberaceae Turmeric Rhizome
Curcuma xanthorrhiza Roxb. Zingiberaceae Curcuma Rhizome
Cymbopogon citratus Stapf. Gramineae Takhrai, lemongrass Leaf
Citrus hystrix DC. Rutaceae Leech lime Leaf
Ocimum basilicum Linn. Labiatae Ho-ra-pa, sweet-basil, basil Leaf
Ocimum canum Linn. Labiatae Hairy basil Leaf
Ocimum sanctum Linn. Malvaceae Holy basil, sacred basil Leaf
Moringa oleifera Lam. Moringaceae Horse radish tree Leaf
Annona squamosa Linn. Annonaceae Sugar apple Leaf
Psidium guajava Linn. Myrtaceae Guava Leaf
Eucalyptus camaldulensis Dehnh. Myrtaceae Red river gum, Murray red gum Leaf
Artocarpus heterophyllus Lam. Moraceae Jackfruit tree Leaf
Piper sarmentosum Roxb. Piperaceae Cha-plu Leaf
Murraya paniculata (L.) Jack. Rutaceae Orange jessamine, satin-wood Leaf
Melissa officinalis L. Lamiaceae Kitchen mint, marsh mint Leaf
Cassia siamea (Lam.) Fabaceae Kassod tree, siamese senna Leaf

Table 5  Examples of functional and/or biologically active plant ingredients (Bakkali et al. 2008)
Ingredient type/function Examples
Antioxidants Lycopene, resveratrol, α-carotene, β-carotene, catechins, vitamin C, vitamin E, green tea, soy
isoflavones, curcumin, pomegranate extracts (anthocyanins, delphinidin, cyaniding, pelargonidin),
grape seed extracts, polyphenols, essential oils, kojic acid
Anticarcinogens Resveratrol, lycopene, green tea, genistein, pycnogenol, curcumin, lycopene, pomegranate seed
oils, polypodium extracts, vitamin E, silymarin
Antiinflammatory/anti-irritant Vitamin C, pycnogenol, oatmeal, curcumin, avenanthramides, salicylic acid, polyphenols
Natural colorants Henna, lawsone, indigo, camomille, lycopene, crocin, carmine, anthocyanidins, carotenoids
Fragrances Essential oils terpenes, terpenoides, aldehydes, alcohols, esters, ketones, phenols, methoxyphenols
Preservatives, antiseptics Saponins, essential oils, benzoic/salicylic acids and derivatives, organic acids and esters, phenols,
usnic acid, thymol, bacteriocins
Hydration/moisturizing Silymarin, lipids, sterols, omega-3 fatty acids
Surfactants Saponins, phospholipids
Thickening agents Carrageenan, starches, carbohydrates
Skin whitening Kojic acid, arbutin, soy proteins, aloesin, vitamin C
Anti-ageing/free radical scavenging Lycopene, genistein, vitamin C, vitamin E, pomegranate extracts, grape seed extract, silymarin, soy
proteins, anthocyanins, green tea extracts, Polypodium leucotomos extract, polyphenols, resveratrol,
curcumin, pomegranate seed oils, soy isoflavones
Photo-protection Pomegranate seed oils, genistein, green tea extracts, Polypodium leucotomos extract, polyphenols,
avenanthramides

soaps, presumably with reduced bioavailability and toxicity acetylcholine, the major neurotransmitter, by bonding
to humans (Casanova et al. 2002). Furthermore, alkaloids of to acetylcholine receptors at nerve synapses and caus-
Haloxylon salicornicum and Stemona japonica are known ing uncontrolled nerve firing. This disruption of normal
be strong agonists at nicotinic acetylcholine receptors (El- nerve impulse activity results in rapid failure of those body
Shazly et al. 2005). systems that depend on nervous input for proper function-
ing. In insects, the action of nicotine is fairly selective, and
Mode of Action In both insects and mammals, nicotine only certain types of insects are affected.
is an extremely fast-acting nerve toxin. It competes with

13
132 N. E. El-Wakeil

Fig. 3  Chemical structure of nicotine and nicotian plants

Fig. 4  Chemical structure of rotenone and Derris and Lonchocarpus
plants
Rotenone

As a pesticide, rotenone has been in use for more than 150 is 4 days, and at harvest residue levels were above the tol-
years, but its use as a fish poison dates back even further erance limit (Cabras et al. 2002). Moreover, residues were
(Shepard 1951). Rotenone is one of several isoflavonoids concentrated in oil obtained from the olives. As an agricul-
produced in the roots or rhizomes of the tropical legumes tural pesticide, use of rotenone is limited to organic food
Derris, Lonchocarpus, and Tephrosia. Most rotenone used production. In California, about 200kg are used annually,
at present comes from Lonchocarpus grown in Venezuela mostly on lettuce and tomato crops (Isman 2006).
and Peru and is often called cubè root. Extraction of the root
with organic solvents yields resins containing as much as Mode of Action  Rotenone is a powerful inhibitor of cellular
45 % total rotenoids; studies indicate that the major con- respiration, the process that converts nutrient compounds
stituents are rotenone (44 %) (Fig.  4) and deguelin (22 %) into energy at the cellular level. In insects rotenone exerts
(Fang and Casida 1998; Cabizza et al. 2004). Rotenone is its toxic effects primarily on nerve and muscle cells, causing
commonly sold as a dust containing 1 to 5 % active ingredi- rapid cessation of feeding. Death occurs several hours to a
ents for home and garden use, but liquid formulations used few days after exposure. Rotenone is extremely toxic to fish,
in organic agriculture can contain as much as 8 % rotenone and is often used as a fish poison (piscicide) in water man-
and 15 % total rotenoids. Rotenone is a mitochondrial poi- agement programs. It is effectively synergized by piperonyl
son, which blocks the electron transport chain and prevents butoxide (PBO) or MGK 264.
energy production (Hollingworth et al. 1994). As a pesti-
cide it is considered a stomach poison because it must be Sabadilla
ingested to be effective. Pure rotenone is comparable to
DDT and other synthetic pesticides in terms of its acute tox- Sabadilla is a botanical pesticide obtained from the seeds of
icity to mammals (rat oral LD50 is 132 mg kg−1), although it the South American lily Schoenocaulon officinale. In purity,
is much less toxic at the levels seen in formulated products. the active principles, cevadine-type alkaloids, are extremely
Safety of rotenone has recently been called into question toxic to mammals (rat oral LD50 is ca. 13 mg kg−1), but com-
because of (a) controversial reports that acute exposure in mercial preparations typically contain less than 1 % active
rats produces brain lesions consistent with those observed ingredient, providing a margin of safety (Fig. 5). These alka-
in humans and animals with Parkinson’s disease (Betarbet loids are remarkably similar to that of the pyrethrins, despite
et al. 2000), and (b) the persistence of rotenone on food their lack of structural similarity. Sabadilla is used primarily
crops after treatment. A study of rotenone residues on olives by organic growers; in California about 100 kg is used annu-
conducted in Italy determined that the halflife of rotenone ally, primarily on citrus crops and avocado (Isman 2006).

13
Botanical Pesticides and Their Mode of Action 133

it does cause insects to stop feeding soon after ingesting

it. Little has been published concerning its exact mode of
action in insect systems. Ryania is effectively synergized by
PBO and is reported to be most effective in hot weather.

Pyrethrum

Pyrethrum is the powdered, dried flower head of the pyre-

thrum is daisy, Chrysanthemum cinerariaefolium (Astera-
ceae). Most of the world’s pyrethrum crop is grown in
Kenya. The term “pyrethrum” is the name for the crude
flower dust itself, and the term “pyrethrins” refers to the
six related insecticidal compounds that occur naturally in
the crude material, the pyrethrum flowers. The flowers are
ground to a powder and then extracted with hexane or a
Fig. 5  Cevadine-type alkaloids and Schoenocaulon officinale plant similar nonpolar solvent; removal of the solvent yields an
orange-colored liquid that contains the active principles
Mode of Action  In insects, sabadilla’s toxic alkaloids affect (Casida and Quistad 1995; Glynne-Jones 2001). These are
nerve cell membrane action, causing loss of nerve cell mem- three esters of chrysanthemic acid and three esters of pyre-
brane action, causing loss of nerve function, paralysis and thric acid. Among the six esters, those incorporating the
death. Sabadilla kills insects of some species immediately, alcohol pyrethrolone, namely pyrethrins I and II, are the
while others may survive in a state of paralysis for several most abundant and account for most of the pesticidal activ-
days before dying. Sabadilla is effectively synergized by ity (Fig.  7). Technical grade pyrethrum, the resin used in
PBO or MGK 264. formulating commercial pesticides, typically contains from
20 to 25 % pyrethrins (Casida and Quistad 1995; Isman
Ryania 2006).
The insecticidal action of the pyrethrins is character-
Another botanical in declining use is ryania, obtained by ized by a rapid knockdown effect, particularly in flying
grinding the wood of the Caribbean shrub Ryania speciosa insects, and hyperactivity and convulsions in most insects.
(Flacourtiaceae). The powdered wood contains < 1 % ryano- These symptoms are a result of the neurotoxic action of
dine (Fig. 6), an alkaloid that interferes with calcium release the pyrethrins, which block voltage-gated sodium channels
in muscle tissue (National Research Council 2000). It is in nerve axons. As such, the mechanism of action of pyre-
used to a limited extent by organic apple growers for con- thrins is qualitatively similar to that of DDT and many syn-
trol of the codling moth, Cydia pomonella. More informa- thetic organochlorine pesticides. In purity, pyrethrins are
tion on sabadilla and ryania can be found in the two reviews moderately toxic to mammals (rat oral acute LD50 values
(Weinzierl 2000; Isman 2006). range from 350 to 500 mg kg−1), but technical grade pyre-
thrum is considerably less toxic (ca. 1,500 mg kg−1) (Casida
Mode of Action Ryania is a slow-acting stomach poison. and Quistad 1995). Pyrethrins are especially labile in the
Although it does not produce rapid knockdown paralysis, presence of the UV component of sunlight, a fact that has
greatly limited their use outdoors. A recent study indicated
that the half-lives of pyrethrins on field-grown tomato and
bell pepper fruits were 2 h or less (Antonious 2004). This
problem created the impetus for the development of syn-
thetic derivatives (“pyrethroids”) that are more stable in
sunlight. The modern pyrethroids, developed in the 1970s
and 1980s, have been highly successful and represent one
of the rare examples of synthetic pesticide chemistry based
on a natural product model. However, note that the modern
pyrethroids bear little structural resemblance to the natural
pyrethrins, and their molecular mechanism of action differs
as well. Pyrethrum use data from California (CDPR 2005)
Fig. 6  Chemical structure of ryanodine and Ryania speciosa plant in 2003 clearly demonstrate the dominance of this material

13
134 N. E. El-Wakeil

Fig. 7  Chemical structure of

different pyrethrum products and
Chrysanthemum flowers

among botanicals: Pyrethrum accounted for 74 % of all Plant Essential Oils
botanicals used that year, but only 27 % of that amount
was used in agriculture (ca. 800 kg). Major uses of pyre- Steam distillation of aromatic plants yields essential oils,
thrum in California are for structural pest control, in public long used as fragrances and flavorings in the perfume and
health, and for treatment of animal premises. Pyrethrum food industries, respectively, and more recently for aro-
is the predominant botanical in use, perhaps accounting matherapy and as herbal medicines (Salama et al. 1970;
for 80 % of the global botanical insecticide market (Isman Sharaby 1988; Coppen 1995; Abd El-Aziz and Sharaby
2005, 2006). 1997; Abd El-Aziz and El-Hawary 1997; Buckle 2003).
As I reported above, by 1860, the natural pesticides Plant essential oils are produced commercially from several
were used in Europe and the United States (Casida 1973; botanical sources, many of which are members of the mint
McLaughlin 1973). The organic solvent extract of the flow- family (Lamiaceae). The oils are generally composed of
ers was tenned pyrethrum, and it possessed many favorable complex mixtures of monoterpenes, biogenetically related
properties. Its safety for mammals and rapid photo degrada- phenols, and sesquiterpenes. Examples include 1,8-cineole,
tion led to many ses in situations that required low mamma- the major constituent of oils from rosemary (Rosmarinus
lian toxicity and no residue problems (dairies, vegetables). officinale) and eucalyptus (Eucalyptus globus); eugenol
This combination of desirable characteristics fueled numer- from clove oil (Syzygium aromaticum); thymol from garden
ous attempts to develop synthetic analogues that would be thyme (Thymus vulgaris); and menthol from various species
more widely available and perhaps more potent; the syn- of mint (Mentha species) (Isman 1999) (Fig. 8). A number
thetic pyrethroids will be presented in the second genera- of the source plants have been traditionally used for pro-
tion products of the botanical pesticides. tection of stored commodities, especially in the Mediterra-
nean region and in southern Asia, but interest in the oils was
Mode of Action  Pyrethrins exert their toxic effects by dis- renewed with emerging demonstration of their fumigant
rupting the sodium and potassium ion exchange process in and contact insecticidal activities to a wide range of pests
insect nerve fibers and interrupting the normal transmission (Abdallah et al. 2004). The rapid action against some pests
of nerve impulses. Pyrethrins insecticides are extremely is indicative of a neurotoxic mode of action, and there is evi-
fast acting and cause an immediate “knockdown” paralysis dence for interference with the neuromodulator octopamine
in insects. Despite their rapid toxic action, however, many (Enan 2001; Kostyukovsky et al. 2002) by some oils and
insects are able to metabolize (break down) pyrethrins with GABA-gated chloride channels by others (Priestley
quickly. After a brief period of paralysis, these insects may et al. 2003; El-Hosary 2011).
recover rather than die. To prevent insects from metabo- Some of the purified terpenoid constituents of essential
lizing pyrethrins and recovering from poisoning, most oils are moderately toxic to mammals, but, with few excep-
products containing pyrethrins also contain the synergist, tions, other oils had molluscicidal effects for snails (Hussein
piperonyl butoxide (PBO) (Rattan 2010). 2005; Abdelgaleil 2010). The oils themselves or products

13
Botanical Pesticides and Their Mode of Action 135

Fig. 8  The chemical structures

of monoterpenes and Rosmarinus
and Thymus plants

based on oils are mostly nontoxic to mammals, birds, and extensive worldwide use as fragrances and flavorings. In
fish (Stroh et al. 1998; Isman 2000, 2006). However, as contrast, pyrethrum and neem are used primarily for pesti-
broad-spectrum pesticides, both pollinators and natural cide production (Khater 2012). On the other hand, plant oils
enemies are vulnerable to poisoning by products based have harmless effects on the predacious mites as reported
on essential oils. Owing to their volatility, essential oils by Amer and Momen (2002, 2005), who studied effects of
have limited persistence under field conditions; therefore, some essential oils on Amblyseius swirskii.
although natural enemies are susceptible via direct contact,
predators and parasitoids reinvading a treated crop one or Mode of Action  Contact and fumigant insecticidal actions
more days after treatment are unlikely to be poisoned by of plant essential oils have been well demonstrated against
residue contact with pesticides (Dimetry et al. 1993; Ismail stored product pests (Acanthoscelides obtectus) (Regnault-
et al. 2004; El-Sebai et al. 2005). Roger et al. 1993). Knockdown activity and lethal toxicity
In the United States, commercial development of pesti- via contact has been demonstrated in the American cock-
cides based on plant essential oils has been greatly facilitated roach (Periplaneta americana) (Ngoh et al. 1998), the
by exemption from registration for certain oils commonly German cockroach (Blattella germanica) and the housefly
used in processed foods and beverages (Quarles 1996). (Musca domestica) (Coats et al. 1991; Rice and Coats 1994).
This opportunity has spurred the development of essential These studies latter pointed to an obvious neurotoxic site-
oil-based insecticides, fungicides, and herbicides for agri- of-action. Certain essential oil monoterpenes are competi-
cultural and industrial applications and for the consumer tive inhibitors of acetylcholinesterase in vitro (Grundy and
market, using rosemary oil, clove oil, and thyme oil as Still 1985; Miyazawa et al. 1997), but this action may not be
active ingredients. Interest in these products has been con- correlated with toxicity to insects in vivo. However, system-
siderable, particularly for control of greenhouse pests and atic investigation of the antifungal activities of essential oils
diseases and for control of domestic and veterinary pests, and their constituents predate those of the pesticidal proper-
with several private companies (e. g. EcoSMART Technolo- ties (Kurita et al. 1981).
gies, Inc., United States) moving toward or into the market- El-Hawary and Sammour (2006) studied the bioactiv-
place (Khater 2012). Another factor favoring development ity and mechanism of action of some wild plant extracts on
of botanical pesticides based on plant essential oils is the Aphis craccivora. As well Adel et al. (2010) have several
relatively low cost of the active ingredients, a result of their studies on physiological, biochemical and histopathological

13
136 N. E. El-Wakeil

effects of Artemisia monosperma against the cotton leaf-

worm, Spodoptera littoralis in Egypt. Sammour et al. (2011)
had comparative studies on the efficacy of neemix and basil
oil formulations on the cowpea aphid Aphis craccivora in
laboratory in Egypt. On the other side, Dimetry and El-
Hawary (1997) conducted some experiments to enhance the
synergistic effects of some additives on the biological activ-
ity and toxicity of Nem-based formulations against cowpea
aphids.
The modes of action of limonene and linalool in insects
are not fully understood. Limonene is thought to cause
an increase in the spontaneous activity of sensory nerves.
This heightened activity sends spurious information to
motor nerves and results in twitching, lack of coordination,
and convulsions. The central nervous system may also be
affected, resulting in additional stimulation of motor nerves.
Massive over stimulation of motor nerves leads to rapid
knockdown paralysis. Adult fleas and other insects may
recover from knockdown, however, unless limonene is syn-
ergized by PBO. Linalool is also synergized by PBO. Little
has been published regarding the mode of action of linalool
in insects (Abdelgaleil and El-Aswad 2005; Abdelgaleil
et al. 2008; Rattan 2010). Fig. 9 Different products of synthetic pyrethroids and their LD50
values
The Second Generation
theses and purifications now can generate the most potent
Synthetic Pyrethroids individual stereoisomers for production.
Although the majority of studies have demonstrated
The earliest synthetic pyrethroids retained most of the ben- favorable selectivity ratios for synthetic pyrethroids, a few
eficial proper ties. Allethrin varied from pyrethrin I only in effects have been reported in mammals. A transitory tin-
the three carbon length of the side chain on the cyclopen- gling of the skin can occur during occupational exposures
tenone ring. Replacement of that photolabile ring with the (Cagen et al. 1984). Permethrin caused increases in tumors
furan ring and the photo stable benzene ring generated pyre- in mice, but they were benign tumors. The EPA does not
throids (e. g. resmethrin) with slightly more residual time fol- consider this chemical to present a significant health hazard
lowing their application (Davies 1985). In the 1970s, great to humans. A metabolite formed from cholesterol and the
strides were made in the United Kingdom and Japan toward chlorophenyl isovaleric acid portion of the R, S-isomer of
enhancing insecticidal potency, increasing photostability, fen valerate reportedly caused a liver granuloma condition
and improving the chemistry to achieve a host of commer- in rats (Okuna et al. 1986).
cially viable synthetic pyrethroid pesticides. The evolution From an environmental perspective, the pyrethroids
of this class of compounds has since yielded a vast array of represent improvements in many ways over the previously
molecules, some with greater lipophilicity, extremely low used classes. The widely used pyrethoids seem to pres-
water solubility, and considerable persistence because of the ent no problem to birds or other wildlife. Bees, important
use of single or multiple halogen atoms (Coats 1990, 1994). non-target arthropods, are only affected if sprayed directly;
Mammalian and avian studies on the toxicity of the syn- otherwise, the pyrethroids effectively repel them from for-
thetic pyrethroids have demonstrated, in general, retention aging in fields that have been sprayed. Aquatic arthropods
of safety for warm blooded species. The LD50 S of many are generally very susceptible to these compounds, but the
of the photostable analogues were more than 100 or even bioavailability of them depends on suspended solids in the
1,000 mg/kg in mammals, and were even greater in birds. water (Coats et al. 1989).
However, some of the most powerful compounds, e.g.
lambda cyhalothrin, deltamethrin, tefluthrin and flucythri- Mode of Action  Synthetic pyrethroids are generally recog-
nate (Bradbury and Coats 1989) as shown in Fig  9, have nized as neurotoxicants that act directly on excitable mem-
different LD50 values in rats and mice. Stereoselective syn- branes. These compounds induce intense repetitive activity
in sense organs and in myelinated nerve fibers. In the lat-

13
Botanical Pesticides and Their Mode of Action 137

eral-line sense organ this repetitive activity increases with and release of molting hormones (ecdysteroids) from the
cooling, a phenomenon that may be related to the negative prothoracic gland, leading to incomplete ecdysis in imma-
temperature coefficient of toxicity of pyrethroids in insects. ture insects. In adult female insects, a similar mechanism
Pyrethroids are also known to cause prolongation of the of action leads to sterility. In addition, azadirachtin is a
sodium current together with repetitive activity in nerve potent antifeedant to many insects. The discovery of neem
fibers of invertebrates (Henk et al. 1982). It has been sug- by western science is attributed to Schmutterer (1990), who
gested that the sodium channel in the nerve membrane is the observed that swarming desert locusts in Sudan defoliated
major target site of pyrethroids. Other results showed that almost all local flora except for some introduced neem trees
these compounds modify sodium channel gating in a strik- (National Research Council 1992). Indeed, azadirachtin was
ingly similar way and reduce selectively the rate of closing first isolated based on its exceptional antifeedant activity in
of the activation gate (Narahashi 1976). the desert locust, and this substance remains the most potent
locust antifeedant discovered to date. Unlike pyrethrins,
Neem Products (Azadirachtin) azadirachtin has defied total synthesis to this point. In USA,
Neem rapidly became the modern paradigm for develop-
Two types of botanical pesticides can be obtained from ment of botanical pesticides (Weinzierl 2000).
seeds of the Indian neem tree, Azadirachta indica (Melia- Enthusiasm for neem was fostered by several interna-
ceae) (Schmutterer 1990, 2002). Neem oil, obtained by tional conferences in the 1980s and 1990s, and several vol-
cold-pressing seeds, can be effective against soft-bodied umes dedicated to neem and neem insecticides have been
insects and mites but is also useful in the management of published (Jacobson 1989; National Research Council
phytopathogens. Apart from the physical effects of neem oil 1992; Schmutterer 2002). Unfortunately, neem’s commer-
on pests and fungi, disulfides in the oil likely contribute to cial success has fallen well short of the initial hype fueled
the bioactivity of this material (Dimetry et al. 2010; Dim- by the explosive scientific literature surrounding it. In part
etry 2012). More highly valued than neem oil are medium- this is due to the relatively high cost of the refined product
polarity extracts of the seed residue after removal of the oil, (Isman 2004) and the relatively slow action on pest insects.
as these extracts contain the complex triterpene azadirachtin Nonetheless, several azadirachtin based pesticides are sold
(Fig. 10). Neem seeds actually contain more than a dozen in the United States and at least two such products in the
azadirachtin analogs, but the major form is azadirachtin European Union. In California, azadirachtin-based insecti-
and the remaining minor analogs likely contribute little to cides constituted about one third of the botanicals used in
overall efficacy of the extract. Seed extracts include con- agriculture in 2003 (ca. 600  kg). In practice, reliable effi-
siderable quantities of other triterpenoids, notably salan- cacy is linked to the physiological action of azadirachtin as
nin, nimbin, and derivatives thereof. The role of these other an insect growth regulator; the antifeedant effect, which is
natural substances has been controversial (El-Sayed 1982– spectacular in the desert locust, is highly variable among
1983a, b), but most evidence points to azadirachtin as the pest species, and even those species initially deterred are
most important active principle (Isman et al. 1996). Neem often capable of rapid desensitization to azadirachtin (Bom-
seeds typically contain 0.2–0.6 % azadirachtin by weight, so ford and Isman 1996). What is clear is that azadirachtin
solvent partitions or other chemical processes are required is considered nontoxic to mammals (rat oral acute LD50 is
to concentrate this active ingredient to level 10–50 % seen in > 5,000  mg kg−1), fish (Wan et al. 1996), and pollinators
the technical grade material used to produce their products (Naumann and Isman 1996). The influence of azadirachtin
(Sallena 1989; Schmutterer 1990). on natural enemies is highly variable (Lowery and Isman
Azadirachtin has two profound effects on insects. At 1995; Spollen and Isman 1996). Like the pyrethrins, aza-
the physiological level, azadirachtin blocks the synthesis dirachtin is rapidly degraded by sunlight. For example,
on olives growing in Italy, azadirachtin has a half-life of
approximately 20 h (Caboni et al. 2002). Azadirachtin has
systemic action in certain crop plants, greatly enhancing its
efficacy and field persistence (Schmutterer 2002). On the
other hand, El-Wakeil et al. (2006, 2013) mentioned further
that NeemAzal-T/S had reduced the parasitism rates, to 40,
55.4, 77.8 and 81.3 % (at 2, 1, 0.5, 0.25 % cons.), respec-
tively, compared to 93.3 % on control plants.

Fig. 10  Active constituents of neem (Azadirachtin) and neem tree

13
138 N. E. El-Wakeil

Fig. 13  Active constituents

of some botanical insecticides
(volkensin)

reported to be a stomach poison for chewing insects (Chiu

1988). Later studies suggest that this substance acts pri-
Fig. 11 Active constituents of 1-cinnamoyl-3-feruoyl-11-hydro­
- marily as a feeding deterrent but can also serve as a syner-
xy­melia­carpin
gist for conventional insecticides (Chen et al. 1995; Feng
et al. 1995). Although relatively nontoxic to mammals, it
Melia Extracts is unclear whether this material remains in production or
whether it is sufficiently efficacious as a stand-alone crop
The remarkable bioactivity of azadirachtin from the Indian protectant.
neem tree (Azadirachta indica) led to the search for natural When M. toosendan came under scientific scrutiny,
pesticides in the most closely related genus, Melia. Seeds investigation of the east African M. volkensii demonstrated
from the chinaberry tree, Melia azedarach, contain a num- bioactivity in insects from seed extracts of this species. The
ber of triterpenoids, the meliacarpins (Fig. 11), that are simi- active principles in M. volkensii include the triterpenoid
lar but not identical to the azadirachtins, and these also have salannin, also a major constituent of neem seed extracts,
insect growth regulating bioactivities (Kraus 2002). But in and some novel triterpenoids such as volkensin (Fig.  13).
spite of the abundance of chinaberry trees in Asia and other Collectively these function as feeding deterrents and
tropical and subtropical areas to which they were introduced, stomach poisons with moderate efficacy against chewing
development of commercial pesticides has not paralleled insects and as a mosquito larvicide. Although a standard-
that of the neem pesticides. The main reason is the pres- ized seed extract has been made in quantities sufficient for
ence, in chinaberry seeds, of additional triterpenoids, the research (Rembold and Mwangi 2002), commercial pro-
meliatoxins, that have demonstrated toxicity to mammals duction appears unlikely owing to a lack of infrastructure
(Ascher et al. 2002). However the chemistry of chinaberry for harvesting seeds in addition to regulatory impediments
varies considerably across its natural and introduced range, (Weinzierl 2000; Isman 2006).
and seeds of M. azedarach growing in Argentina lack melia-
toxins but produce triterpenoids (most notably meliartenin) Mode of Action Neem products are complex mixtures
that are strong feeding deterrents to insect pests and could of biologically active materials, and they are difficult to
prove useful for pest management (Carpinella et al. 2003). pinpoint the exact modes of action of various extracts or
Similar results have been obtained from South Africa using preparations. In insects, neem is most active as a feeding
aqueous extracts of chinaberry leaves, presumably lacking deterrent, but in various forms it also serves as a repellent,
meliatoxins but efficacious against the diamondback moth growth regulator, oviposition (egg deposition) suppressant,
(Charleston 2004). sterilant, or toxin. As a repellent, neem prevents insects from
In the early 1990s a botanical insecticide produced in initiating feeding. As a feeding deterrent, it causes insects to
China was based on an extract of bark of Melia toosen- stop feeding. As a feeding, either immediately after the first
dan, a tree considered by most taxonomists to be synony- “taste” (due to the presence of deterrent taste factors) (Sal-
mous with M. azedarach. The extract contains a number of ama and Sharaby 1988), or at some point soon after ingest-
triterpenoids based on toosendanin (Fig.  12), a substance ing the food (due to secondary hormonal or physiological
effects of the deterrent substance). As a growth regulator,
neem is thought to disrupt normal development interfering
Fig. 12 Active constituents with chitin synthesis. Susceptibility to the various effects of
of some botanical insecticides
neem differs by species.
(toosendanin)

Potential new Botanicals

Annonaceous Acetogenins

Botanical pesticides have been traditionally prepared from

the seeds of tropical Annona species, members of the cus-

13
Botanical Pesticides and Their Mode of Action 139

Fig. 14  Active constituents of

Annona species (asimicin) and
Annona squamosa plant

tard apple family (Annonaceae). These include the sweetsop (Nature’s Sunshine Products, Inc., United States). Annona
(A. squamosa) and soursop (A. muricata), important sources seed extracts may prove more useful in tropical countries
of fruit juices in Southeast Asia. Detailed investigations in where the fruits are commonly consumed or used to pro-
the 1980s led to the isolation of a number of long-chain duce fruit juice, in which case the seeds are a waste prod-
fatty acid derivatives, termed acetogenins, responsible for uct. For example, Leatemia and Isman (2004a, b) recently
the insecticidal bioactivity. The major acetogenin obtained demonstrated that crude ethanolic extracts or even aqueous
from seeds of A. squamosa is annonin I, or squamocin, and extracts of seeds from A. squamosa collected at several sites
a similar compound, asimicin (Fig. 14), was isolated from in eastern Indonesia are effective against the diamondback
the bark of the American pawpaw tree, Asimina triloba moth (Plutella xylostella) (Isman 2006).
(McLaughlin et al. 1997; Johnson et al. 2000). Mikolajc-
zak et al. (1988) hold a US patent on insecticides ased on The Insecticidal Mode of Action of Asimicin It reduced
acetogenins from A. triloba; Bayer AG (Germany) holds a the rate of oxygen consumption by fourth instar Ostrinia
similar patent based on Annona acetogenins for Moeschler nubilalis as measured with a constant volume manometer.
et al. (1987). These compounds are slow acting stomach Further examination of the respiratory effect of asimicin
poisons, particularly effective against chewing insects such was carried out on mitochondria isolated from the midguts
as lepidopterans and the Colorado potato beetle (Leptino- of fifth instar O. nubilalis and in which O2 was measured
tarsa decemlineata). polarographically. The results of these studies indicate a
Further investigations revealed that the acetogenins have significant reduction in state 3 respiration using malate and
a mode of action identical to that of rotenone, i. e., they pyruvate as substrate, caused by asimicin (concentration
block energy production in mitochondria in both insects and for 50 % inhibition = 0.55  nmol/mg protein) (Lewis et al.
mammals (Londershausen et al. 1991). In purity certain ace- 1993).
togenins are toxic to mammals (LD50 is < 20 mg kg−1), an
impediment to regulatory approval, even though standard- Sucrose Esters
ized extracts from Annona seeds and Asimina bark are much
less toxic. In the early 1990s scientists at the US Department of Agri-
Johnson et al. (2000) have isolated hundreds of aceto- culture discovered that sugar esters naturally occurring in
genins from the Annonaceae, and for many their potential the foliage of wild tobacco (Nicotiana gossei) were pesti-
as anticancer agents exceeds their value as pesticides. In cidal to certain soft-bodied insects and mites. Although pat-
spite of the patents based on the insecticidal activities of ented (Pittarelli et al. 1993), extraction of these substances
these materials, no commercial development has proceeded on a commercial scale from plant biomass proved impracti-
with the exception of a head lice shampoo that contains a cal, leading to the development of sucrose esters manufac-
standardized pawpaw extract among its active ingredients tured from sugar and fatty acids obtained from vegetable

Fig. 15  Chemical structure of

sucrose esters obtained from
wild tobacco (N. gossei)

13
140 N. E. El-Wakeil

Table 6  Mechanism of action of pesticides of plant origin (modified from Rattan 2010)
System Mechanism of action Compound Plant source References
Cholinergic system Inhibition of acetylecholinestrase Essential oils Azadirachtina indica, Mentha Grundy and Still (1985);
(AChE) spp., Lavendula spp. Ryan and Byrne (1988);
Miyazawa et al. (1997);
Keane and Ryan (1999)
Cholinergic acetylcholine nicotinic Nicotine Nicotiana spp., Haloxylon sali- Richards and Cutkomp
receptor Agonist/antagonist cornicum, Stemona Japonicum (1945); Kukel and Jen-
nings (1994)
GABA system GABA-gated chloride channel Thymol, Thymus vulgaris Ratra and Casida (2001);
Silphinenes Priestley et al. (2003);
Bloomquist et al. (2008)
Mitochondrial Sodium and potassium ion exchange Pyrethrin Crysanthemum cinerariaefolium Casida (1973)
system disruption
Inhibitor of cellular Rotenone Lonchocarpus spp. Yamamoto and Kuroka-
respiration(mitochondrial complex I wa (1970); Ware (1988);
electron transport inhibitor (METI) Khambay et al. (2003)
Affect calcium channels Ryanodine Ryania spp. Copping and Menn
(2000)
Affect nerve cell membrane action Sabadilla Schoenocaulon officinale Bloomquist (1996, 2003)
Octopaminergic Octopaminergic receptors Essential oils Cedrus spp., Pinus spp., Citro- Nathanson et al. (1993);
system nella spp., Eucalyptus spp. Kostyukovsky et al.
(2002); Enan (2005a)
Block octopamine receptors by Thymol Thymus vulgaris Enan (2005a, b)
working through tyramine receptors
cascade
Miscellaneous Hormonal balance disruption Azadirachtin Azadiractina indica Copping and Menn
(2000)

oils. AVA Chemical Ventures (United States) has patented Summary of Different Mode of Actions
and registered an insecticide/miticide based on C8 and C10
fatty acid mono-, di-, and triesters of sucrose octanoate and Botanical pesticides can be grouped according to their mode
sucrose dioctanoate (Farone et al. 2002) (Fig. 15). The prod- of action or the way a pesticide destroys or controls the tar-
uct, first registered in 2002, contains 40 % active ingredient. get pest. This is also referred to the primary site of action.
The major isomers are composed of an acetyl group (R3) For example, one insecticide may affect insect nerves,
and three 3-methylvaleryl groups (R1, R2, R4) esterified to while another may affect moulting. There are many mode
three hydroxyl groups of sucrose. Extensive studies have of actions for various botanical pesticides shown in Table 6.
shown that the glandular trichomes of wild tobacco contain
complexes of either glucose or sucrose esters (sometimes Efficiency of Botanical Pesticides on Pests
both). These leaf surface lipids have biological activity
against insects and microorganisms. Compounds of this Antifeedants
type have been synthesized in a search for a new class of
bioinsecticides (Matsuzaki et al. 1991). The possibility of using nontoxic deterrents and repellents
as crop protectants is intuitively attractive. The concept
Mode of Action  Functionally, this product appears to dif- of using insect antifeedants (= feeding deterrents) gained
fer little from the pesticidal soaps based on fatty acid salts strength in the 1970s and 1980s with the demonstration of
developed in the 1980s, particularly potassium oleate. This the potent feeding deterrent effect of azadirachtin and neem
product is contact pesticide that kills small insects and mites seed extracts to a large number of pest species. Indeed, con-
through suffocation (by blocking the spiracles) or disrup- siderable literature, scientific and otherwise, touts neem as
tion of cuticular waxes and membranes in the integument a successful demonstration of the antifeedant concept. In
as recorded by Buta et al. (1993), leading to desiccation reality, it is the physiological actions of azadirachtin that
(Isman 2006). Although useful in garden products and in appear most reliably linked to field efficacy of neem pesti-
greenhouse production, the utility of these materials for cides (Immaraju 1998); although purely behavioral effects
agriculture remains to be seen. cannot be ruled out, there is hardly any irrefutable evidence

13
Botanical Pesticides and Their Mode of Action 141

or documentation of field efficacy based on the antifeedant oils as natural alternatives. Some personal repellents in the
effects of neem alone. The antifeedant index (AFI) is calcu- US marketplace contain oils of citronella, eucalyptus, or
lated from the formula: cedar wood as active ingredients; 2-phenethylpropionate, a
constituent of peanut oil, and p-menthane-3,8-diol (obtained
AFI = [ (C − T) (C + T)] × 100 (in %)
from a particular species of mint) (Fig. 8) are also used in
Where: consumer products. All of these materials can provide some
C Consumption of control, protection, but the duration of their effect can be limited
T Consumption of treated disks (Pavela et al. 2008) (often < 1 h) (Fradin and Day 2002). In tropical areas where
mosquito-borne disease is a threat (e.g., yellow fever, den-
As an academic exercise, the discovery and demonstration gue, malaria), DEET probably remains the only reliable
of plant natural products as insect antifeedants has been repellent. Oil of citronella or the constituent citronellal
unquestionably successful. In addition to the neem triter- (Fig. 8) is also used in mosquito coils to repel mosquitoes
penoids, extensive work has been performed on clerodane from outdoor areas. Several veterinary products for flea and
diterpenes from the Lamiaceae (Klein Gebbinck et al. 2002) tick control on domestic pets contain d-limonene (from cit-
and sesquiterpene lactones from the Asteraceae (Gonzalez- rus peels; Fig.  8) as the active ingredient. Other uses for
Coloma et al. 2002). On the other hand, not a single crop repellents under investigation include perimeter treatments
protection product based unequivocally on feeding or ovi- of buildings to exclude termites and the use of essential
position deterrence has been commercialized. Two main oils to repel cockroaches from kitchens and flies from dairy
problems face the use of antifeedants in agriculture (Isman barns (Maistrello et al. 2004). Another important use of
2002). The first is interspecific variation in response even plant essential oil constituents is in fumigation of beehives
closely related species can differ dramatically in behavioral to manage economically important honey bee parasites, the
responses to a substance limiting the range of pests affected Varroa mite (Varroa jacobsoni). In USA, menthol is widely
by a particular antifeedant (Isman 1993). Some substances used for this purpose (Delaplane 1992) and in Europe thy-
that deter feeding by one pest can even serve as attractants mol is most used (Floris et al. 2004). Abdel-Khalek et al.
or stimulants for other pests. The second is the behavioral (2010) studied repellency and toxicity of extract from Fran-
plasticity in insects pests can rapidly habituate to feeding coeria crispa to Eutetranychus orientalis.
deterrents, rendering them ineffective in a matter of hours.
This has been recently demonstrated not only for pure sub- Toxicity of Botanical Pesticides
stances like azadirachtin (Bomford and Isman 1996), but
also for complex mixtures (plant extracts) (Akhtar et al. The botanical pesticides are biodegradable and harmless
2003). Whereas a highly mobile insect may leave a plant to the environment. Furthermore, unlike conventional pes-
upon first encountering an antifeedant, a less mobile one ticides that are based on a single active ingredient, plant-
(larva) may remain on the plant long enough for the deter- derived pesticides comprise an array of chemical compounds
rent response to wane. Such behavioral changes are impor- which act concertedly on both behavioral and physiological
tant in light of the observation that some plant substances processes. One plant species may possess substances with
are initially feeding deterrents but lack toxicity if ingested. a wide range of activities; for example, extracts from the
Azadirachtin is an exception to this rule, as ingestion leads neem tree Azadirachta indica are antifeedant, antioviposi-
to deleterious physiological consequences, but other com- tion, repellent and growth-regulating. In contrast, the toxic-
pounds with demonstrated antifeedant effects lack toxicity ity of conventional synthetic insecticides is mainly restricted
when administered topically (Bernays 1990, 1991). to neuro-muscular function (Ware 1983). Conventional
synthetic insecticides require special safety procedures and
Repellents equipment during production and application because of the
exposure risks for humans, the environment (Schmutterer
For many chemists, an effective alternative to DEET (N, 1990; Childs et al. 2001).
N-diethyl-m-toluamide) for personal protection against
mosquitoes and biting flies is the holy grail. In spite of five
decades of research, no chemical has been found that pro- Summary of Botanicals Used to Control Different
vides the degree of protection against biting mosquitoes or Insect Pests
persistence on human skin afforded by DEET (Peterson and
Coats 2001). Concerns with the safety of DEET, especially Summary of different botanical pesticides and their effects
to children, have resulted in the introduction of several plant on various insect pests is appeared in Table 7.

13
142 N. E. El-Wakeil

Table 7  Botanical pesticides used to control different insect pests

Botanical pesticides Insect pests References
Nicotine Aphids, thrips, caterpillars Casanova et al. (2002)
Rotenone Bugs, aphids, potato beetles, spider mites, carpenter ants Cabras et al. (2002); Cabizza et al. (2004)
Ryania Codling moths, potato aphids, onion thrips, corn earworms, silkworms Copping and Menn (2000); Isman (2006)
Sabadilla Grasshoppers, codling moths, armyworms, aphids, cabbage loopers, Bloomquist (1996, 2003)
squash bugs
Pyrethrum Caterpillars, aphids, leafhoppers, spider mites, bugs, cabbage worms, Casida (1973); Glynne-Jones (2001)
beetles
Essential oils Caterpillars, cabbage worms, aphids, white flies Land sanils Enan (2005a, b); Abdelgaleil (2010)
Neem products Armyworms, cutworms, stemborers, bollworms, leaf miners, caterpil- Dimetry et al. (1993, 2010)
lars, aphids, whiteflies, leafhoppers, psyllids, scales, mites and thrips
Synthetic pyrethroids Caterpillars, aphids, thrips Coats (1990); Sallam et al. (2009)

Vision and Expectation to the crop we wish to protect (Isman 2006). These sorts of
technological advancements seem far more likely now than
Drawbacks and Barriers to Commercialization they did even a decade ago; however, the cost of these tech-
nologies will dictate that the traditional means of obtaining
Isman (1997) identified three main barriers to commer- botanical insecticides, and indeed their minor uses (on small
cialization for botanical insecticides: sustainability of the acreage specialty crops) or uses in developing countries on
botanical resource, standardization of chemically complex lesser value crops will continue for many years to come. For
extracts, and regulatory approval. For each of these there example, neem seed oil had a long history of use in India for
are also important cost considerations. Other drawbacks or the production of soaps and low grade industrial oil. When
limitations are the slow action of many botanicals-growers extraction companies began purchasing neem seeds in bulk
must gain confidence in insecticides that do not produce to produce insecticides, the price of seeds increased 10-fold.
an immediate “knockdown” effect and the lack of residual In contrast, certain plant essential oils have numerous uses
action for most botanicals. as fragrances and flavorings, and the massive volumes
required to satisfy these industries maintain low prices that
Sustainability make their use as insecticides attractive (Weinzierl 2000;
Isman 2006).
To produce a botanical insecticide on a commercial scale,
the source plant biomass must be obtainable on an agricul- Standardization of Botanical Extracts
tural scale and preferably not on a seasonal basis. Unless the
plant in question is extremely abundant in nature, or already An often cited drawback to the adoption of botanical insec-
grown for another purpose (e. g., sweetsop, Annona squa- ticides by growers is the variation in performance of a par-
mosa, grown for its edible fruit; rosemary, Rosmarinus offi- ticular product, even when prepared by the same process.
cinale, as a flavoring), it must be amenable to cultivation. Natural variation in the chemistry of a plant-based commod-
Pyrethrum and neem meet this criterion; the latter has been ity should come as no surprise to anyone who enjoys coffee,
extensively introduced into Africa, Australia, and Latin tea, wine, or chocolate. The investigation of seed extracts
America, more so as a shade tree, windbreak, or source of from sweetsop (A. squamosa) collected in Indonesia dem-
firewood than for its yield of natural medicines or insecti- onstrated both geographical and annual variation in their
cides. Research aimed at producing azadirachtin from neem insecticidal potency (Leatemia and Isman 2004b). For a
tissue culture provided proof of concept, but economic fea- botanical insecticide to provide a reliable level of efficacy to
sibility has yet to be attained (Allan et al. 2002). the user there must be some degree of chemical standardiza-
In the not-too-distant future it may be possible to produce tion, presumably based on the putative active ingredient(s).
botanical insecticides by “phytopharming,” i. e., through This has certainly been achieved with more refined products
genetic engineering of an existing field crop to produce based on pyrethrum, neem, and rotenone, but crude prepara-
high-value natural products originally isolated from a dif- tions often contain low concentrations of active ingredients
ferent botanical source. But as progress in plant biotechnol- without adequate quantitation. To achieve standardization,
ogy continues at a rapid pace, it may prove just as easy to the producer must have an analytical method and the equip-
modify the plants we wish to protect from pests directly, ment necessary for analysis and may need to mix or blend
such that they produce the natural product protectant consti- extracts from different sources, which requires storage facil-
tutively, alleviating the need to obtain the desired botanical ities and is partially dependent on the inherent stability of
product through extraction, formulate it, and then apply it

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Botanical Pesticides and Their Mode of Action 143

the active principles in the source plant material or extracts 3. The rapid degradation of the active product may be con-
thereof held in storage (Atkinson et al. 2004). venient as it reduces the risk of residues on food.
4. Some of these products may be used shortly before
Regulatory Approval harvesting.
5. Many of these products act very quickly inhibiting in-
Regulatory approval remains the most formidable barrier sect feeding even though long term they do (will?) not
to the commercialization of new botanical insecticides. In cause insect death.
many jurisdictions, no distinction is made between synthetic 6. Since most of these products have a stomach action and
pesticides and biopesticides, including botanicals. Simply are rapidly decomposed they may be more selective to
put, the market for botanicals in industrialized countries insect pests and less aggressive with natural enemies.
based mostly on uses in greenhouse production and organic 7. Most of these compounds are not phytotoxic.
agriculture is too small to generate sufficient profits to offset 8. Resistance to these compounds is not developed as
multimillion dollar regulatory costs. Unfortunately, this sit- quickly as with synthetic pesticides.
uation may prevent many “green” pesticides from reaching
the marketplace in countries where the demand is greatest. Disadvantages
I am not making the case that botanicals should be exempt
from all regulatory scrutiny; as discussed above, nicotine 1. Most of these products are not truly pesticides since
is as toxic and hazardous as many synthetic pesticides, and many are merely insect deterrents and their effect is
strychnine, still used for rodent and insect control in some slow.
regions, is responsible for some human poisonings (Katz 2. They are rapidly degraded by UV light so that their re-
et al. 1996). Natural products can pose risks, and safety sidual action is short.
cannot be assumed (Coats 1994; Trumble 2002). But most 3. Not all plant pesticides are less toxic to other animals
of the botanicals discussed in this review are characterized than the synthetic ones.
by low mammalian toxicity, reduced effects on nontarget 4. They are not necessarily available season long.
organisms, and minimal environmental persistence. 5. Most of them have no established residue tolerances.
As noted, several plant essential oils and their constituents 6. There are no legal registrations establishing their use.
are exempt from registration in the United States, attributed 7. Not all recommendations followed by growers have
to their long use history as food and beverage flavorings or been scientifically verified. 
as culinary spices. This exemption has facilitated the rapid
development and commercialization of pesticides based on Botanical Pesticides: for Richer and Poorer Countries
these materials as active ingredients (Isman 2000). Although
other jurisdictions have yet to follow the lead of the United The botanical pesticides should prove most beneficial in two
States in this regard, there are proposals in some Asian coun- contrasting applications (developed and developing coun-
tries to exempt some types of pesticides from registration tries), one for affluent consumers and the other for farmers
for specific uses in public health, for example, in head lice in developing countries (Isman 2008). Apart from economic
preparations or for cockroach and fly suppression. It seems considerations and potential health benefits, another impor-
that regulatory agencies continue to focus their efforts on tant force driving botanicals into these disparate markets is
protecting the general public from miniscule traces of pesti- the regulatory environment. Regulatory approval in indus-
cides in the food supply rather than focusing on the safety of trial nations has become so costly and time consuming
applicators and farm workers, for whom, arguably, the more that only multinational agrochemical companies have the
demonstrable hazards occur (Isman 2006). resources to satisfy regulatory requirements for their pesti-
cides to see widespread agricultural use (Thacker 2002). As
a consequence, botanicals will only see use on food crops
Advantages and Disadvantages of Botanical Pesticides in niche markets such as certified organic production or in
controlled environments. On the other hand, regulation, or
Advantages at least enforcement of pesticide regulations, in developing
counties is generally more relaxed, particularly for domes-
1. Plants producing the above mentioned compounds are tic food production. While it might appear irresponsible to
known by the farmer because most of the time they advocate the use of unregistered crop protectants for which
grow in the same general area. health hazards have not been rigorously established, there
2. Often these plants also have other uses like household in- is reasonable evidence to suggest that, with few exceptions,
sect repellents or are plants with medicinal applications. crude botanical preparations at worst pose no greater risk to
human health than conventional pesticides and indeed are

13
144 N. E. El-Wakeil

probably of substantially lower risk. Moreover, indigenous et al. 2005). At least one study indicates that these materials
knowledge often extends beyond the potential efficacy of are relatively safe in the forms in which they are used (Bel-
endemic plants as crop protectants to include their toxicity main et al. 2001). Some plant products could even be useful
to users. This may well represent a case where our highly in industrialized countries for the protection of grain from
technological society can learn that long-established agro- storage pests (Fields et al. 2001).
ecological practices have a role to play in food production Many of the plants discussed in this review are tropical in
in the twenty-first century. distribution and theoretically available to growers in devel-
oping countries. However, efficacy against pests is only one
Role of Botanical Pesticides in the Future factor in the adoption of botanicals logistics of production,
preparation, or use of botanicals can mitigate against their
What role can botanical pesticides play in crop protection use (Morse et al. 2002). Perhaps it is time to refocus the
and for other uses in the near future? In industrialized coun- attention of the research community toward the develop-
tries it is hard to imagine botanicals playing a greater role ment and application of known botanicals rather than screen
than at present, except in organic food production. Organic more plants and isolate further novel bioactive substances
production is estimated to be growing by 8 to 15 % per that satisfy our curiosity but are unlikely to be of much
annum in Europe and in North America (National Research utility.
Council 2000), and it is in those marketplaces that botani-
cals face the fewest competitors. Even there, however, Conclusions
microbial insecticides and spinosad have proven efficacious
and cost-effective. Rather than considered as stand-alone In summary, the insecticidal activity of extracts may be due
products, botanicals might be better placed as products in to synergistic effects shown by the phenolic components of
crop protectant rotations, especially in light of the docu- the mixtures in the test system used in this investigation.
mented resistance of the diamondback moth to Bacillus These facts are indicative of the potency of the methanol
thuringiensis and spinosad due to overuse (Tang et al. 1997; extracts. Thus, the effect of compounds on reducing insect
Zhao et al. 2002). In conventional agriculture, botanicals growth, increasing development time, and increasing mor-
face tremendous competition from the newest generation of tality of Spodoptera is similar to that of gedunin and more
“reduced risk” synthetic insecticides such as the neonicoti- potent than the MeOH extract from Cedrela salvadorensis
noids. Between 1998 and 2003, use of reduced risk pesti- (Céspedes et al. 2000, 2006).
cides in California increased more than threefold (from 138 The sites and mode of action of these compounds and
to 483  t), whereas biopesticide use declined (from 652 to extracts are being investigated and probably correspond to
472 t) (CDPR 2005). a combination of antifeedant action as midgut phenol oxi-
Botanicals, constituting less than 1 % of biopesticide use dase, proteinase, AChE, tyrosinase, or other PPOs and cuti-
in California (CDPR 2005), are also in decline. Overall, it cle synthesis inhibition, as well as molting, sclerotization,
is hard not to conclude that the best role for botanicals in toxicity, and nerval system inhibition, as has been found for
the wealthier countries is in public health (mosquito, cock- other phenolics and terpenoids (Miyazawa et al. 1997; Kubo
roach abatement) and for consumer (home and garden) use. 2000) and extracts (Feng et al. 1995). In addition, the pres-
The real benefits of botanical pesticides can be best real- ence of an orcinol or catechol group seems to be important
ized in developing countries, where farmers may not be for these activities as shown for the most potent compounds
able to afford synthetic pesticides and the traditional use of in this article. Furthermore, a great percentage of larvae that
plants and plant derivatives for protection of stored prod- reached pupation decreased with the application of pheno-
ucts is long established. Even where synthetic pesticides are lics in comparison to control, which might be due to the
affordable to growers (e.g., through government subsidies), inhibition by tyrosinase as well or to the accumulation of
limited literacy and a lack of protective equipment result in proteinase inhibitors (Tamayo et al. 2000). The activity of
thousands of accidental poisonings annually (Forget et al. these plants, their metabolites, and MeOH extracts is com-
1993; Isman 2000, 2006). parable to the insect growth regulators gedunin and toosen-
More attention has been paid to traditional plants used in danin, which suggests potential for further development of
West Africa for postharvest protection against insects (Bel- these materials.
main and Stevenson 2001; Boeke et al. 2004a, b). Some of The plant kingdom offers a rich source of a wide range of
the more efficacious plants used have well-known active structural biodiversity of natural secondary metabolites. One
principles (e. g., rotenoids from Tephrosia, nicotine from of the most recent trends in fungal and insect pest control is
Nicotiana, methyl salicylate from Securidaca, and eugenol to reduce heavy reliance on synthetic pesticides and to move
from Ocimum); some of these are volatile and act as natural towards biodegradable substances. Synthetic pesticides of
fumigants that kill adult pests and their progeny (Jayasekara broad spectrum have been widely used as the main tools

13
Botanical Pesticides and Their Mode of Action 145

for controlling weeds, and fungal and insect pest, which generalist herbivore, Trichoplusia ni (Lepidoptera: Noctuidae).
are highly toxic to many living organisms as well as to the J Insect Behav 16:811–831
Alburo R, Olofson H (1987) Agricultural history and the use of bo-
environment. Hence, new biorational and specific trends to tanical insecticides in Argao, Cebu. Philipp Quar Cul & Soc
pest control should be developed. In this article, an update 15:151–172
of findings in the field were presented, those approaches Allan EJ, Eeswara JP, Jarvis AP, Mordue Luntz AJ, Morgan ED, Stuch-
resulting from the studies on inhibition of growth (including bury T (2002) Induction of hairy root cultures of Azadirachta
indica A. Juss. and their production of azadirachtin and other im-
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involved in key processes of insect life, specially modifying Amer SA, Momen FM (2002) Effect of some essential oil on preda-
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Amer SA, Momen FM (2005) Effect of French lavender essential oil
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Shepard H (1951) The chemistry and action of insecticides. McGraw- Dr. Nabil E. El-Wakeil, was born
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insecticide on the commercial biocontrol agents Phytoseiulus per- Department of Entomology, Crop
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J Econ Entomol 89:1379–1386 Germany. The topic of his disser-
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toxicity to juvenile Pacific coho salmon and rainbow trout of some logical control of Helicoverpa
plant essential oils, a formulated product, and the carrier. Bull En- armigera in organic cotton pro-
viron Contam Toxicol 60:923–930 duction”. He had started working
Tamayo MC, Rufat M, Bravo JM, San Segundo B (2000) Accumula- in national research Center (Pests
tion of a maize proteinase inhibitor in response to wounding and and Plant Protection dept.) in
insect feeding and characterization of its activity toward digestive Cairo, Egypt from June 2013 as
proteinases of Spodoptera littoralis larvae. Planta 211:62–71 professor of Biological Control. Actually Dr. Nabil El-Wakeil works as
Tang JD, Gilboa S, Roush RT, Shelton AM (1997) Inheritance, stabil- Post doc fellow at Martin Luther-Halle University.
ity and lack-of-fitness costs of field-selected resistance to Bacil-
lus thuringiensis in diamondback moth (Lepidoptera: Plutellidae)
from Florida. J Econ Entomol 90:732–741

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