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Botanical Insecticides, Deterrents, And Repellents In

Modern Agriculture And An Increasingly Regulated
World

Article in Annual Review of Entomology · February 2006

DOI: 10.1146/[Link].51.110104.151146 · Source: PubMed

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10.1146/[Link].51.110104.151146

Annu. Rev. Entomol. 2006. 51:45–66

doi: 10.1146/[Link].51.110104.151146
Copyright
c 2006 by Annual Reviews. All rights reserved
First published online as a Review in Advance on July 11, 2005

BOTANICAL INSECTICIDES, DETERRENTS, AND

REPELLENTS IN MODERN AGRICULTURE AND
AN INCREASINGLY REGULATED WORLD
by Jawaharlal Nehru Centre For Advanced Scientific Research on 08/31/10. For personal use only.

Murray B. Isman
Faculty of Land and Food Systems, University of British Columbia,
Annu. Rev. Entomol. 2006.51:45-66. Downloaded from [Link]

Vancouver, British Columbia, V6T 1Z4, Canada; email: [Link]@[Link]

Key Words pyrethrum, neem, essential oils, antifeedants, commercialization

■ Abstract Botanical insecticides have long been touted as attractive alternatives
to synthetic chemical insecticides for pest management because botanicals reputedly
pose little threat to the environment or to human health. The body of scientific literature
documenting bioactivity of plant derivatives to arthropod pests continues to expand,
yet only a handful of botanicals are currently used in agriculture in the industrialized
world, and there are few prospects for commercial development of new botanical prod-
ucts. Pyrethrum and neem are well established commercially, pesticides based on plant
essential oils have recently entered the marketplace, and the use of rotenone appears
to be waning. A number of plant substances have been considered for use as insect
antifeedants or repellents, but apart from some natural mosquito repellents, little com-
mercial success has ensued for plant substances that modify arthropod behavior. Several
factors appear to limit the success of botanicals, most notably regulatory barriers and
the availability of competing products (newer synthetics, fermentation products, mi-
crobials) that are cost-effective and relatively safe compared with their predecessors. In
the context of agricultural pest management, botanical insecticides are best suited for
use in organic food production in industrialized countries but can play a much greater
role in the production and postharvest protection of food in developing countries.

INTRODUCTION
The practice of using plant derivatives, or botanical insecticides as we now know
them, in agriculture dates back at least two millennia in ancient China, Egypt,
Greece, and India (86, 89). Even in Europe and North America, the documented
use of botanicals extends back more than 150 years, dramatically predating discov-
eries of the major classes of synthetic chemical insecticides (e.g., organochlorines,
organophosphates, carbamates, and pyrethroids) in the mid-1930s to 1950s. What
is clear from recent history is that synthetic insecticides effectively relegated botan-
icals from an important role in agriculture to an essentially trivial position in the
marketplace among crop protectants. However, history also shows that overzealous
0066-4170/06/0107-0045$20.00 45
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46 ISMAN

use of synthetic insecticides led to numerous problems unforeseen at the time of

their introduction: acute and chronic poisoning of applicators, farmworkers, and
even consumers; destruction of fish, birds, and other wildlife; disruption of natural
biological control and pollination; extensive groundwater contamination, poten-
tially threatening human and environmental health; and the evolution of resistance
to pesticides in pest populations (35, 63, 70, 72).
Governments responded to these problems with regulatory action, banning or
severely restricting the most damaging products and creating policies to replace
chemicals of concern with those demonstrated to pose fewer or lesser risks to hu-
by Jawaharlal Nehru Centre For Advanced Scientific Research on 08/31/10. For personal use only.

man health and the environment. In the United States, these policies are reflected by
the definition of “reduced risk” pesticides by the Environmental Protection Agency
Annu. Rev. Entomol. 2006.51:45-66. Downloaded from [Link]

in the early 1990s with their favored regulatory status, and by the Food Quality
Protection Act (1996), which, in reappraising safe levels of pesticide residues in
foods, is having the net effect of removing most synthetic insecticides developed
before 1980 from use in agriculture. These changes in the regulatory “environment”
appeared to heighten the impetus for the discovery and development of alterna-
tive pest management products—those with reduced health and environmental
impacts—including insecticides derived from plants. Indeed, the scientific litera-
ture of the past 25 years describes hundreds of isolated plant secondary metabolites
that show feeding deterrent or toxic effects to insects in laboratory bioassays, and
botanical insecticides have been the subject of several recent volumes (28, 40, 57,
76, 79).
Yet in spite of the scale of this research enterprise, only a handful of botanical
insecticides are in commercial use on vegetable and fruit crops today, with signif-
icant commercial development of only two new sources of botanicals in the past
20 years. In this chapter I review current botanicals and their trends in use, discuss
the few botanical materials with potential for future commercialization, suggest
why so few botanicals reach the marketplace, and finally suggest in what contexts
botanicals could prove effective in the years to come.

CURRENT BOTANICALS IN USE

At present there are four major types of botanical products used for insect control
(pyrethrum, rotenone, neem, and essential oils), along with three others in limited
use (ryania, nicotine, and sabadilla). Additional plant extracts and oils (e.g., garlic
oil, Capsicum oleoresin) see limited (low volume) regional use in various countries,
but these are not considered here. In discussing the extent to which each of the more
important botanical insecticides is used, I often refer to data published annually
by the State of California’s Department of Pesticide Regulation (18). Although
not necessarily representative of uses in other jurisdictions, total pesticide use (in
terms of active ingredient applied) in California totaled more than 175 million
pounds, or 80,000 tonnes, in 2003. This amount represents approximately 6% of
global pesticide use, of which 91% was used for agriculture. Pesticide use data
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BOTANICAL INSECTICIDES 47

in California are reported by active ingredient and by crop or other use and as
such are perhaps the world’s most accurate and detailed records of pesticide use
available to the general public.

Pyrethrum
Pyrethrum refers to the oleoresin extracted from the dried flowers of the pyrethrum
daisy, Tanacetum cinerariaefolium (Asteraceae). The flowers are ground to a pow-
by Jawaharlal Nehru Centre For Advanced Scientific Research on 08/31/10. For personal use only.

der and then extracted with hexane or a similar nonpolar solvent; removal of the
solvent yields an orange-colored liquid that contains the active principles (21,
37). These are three esters of chrysanthemic acid and three esters of pyrethric
Annu. Rev. Entomol. 2006.51:45-66. Downloaded from [Link]

acid. Among the six esters, those incorporating the alcohol pyrethrolone, namely
pyrethrins I (Figure 1) and II, are the most abundant and account for most of
the insecticidal activity. Technical grade pyrethrum, the resin used in formulating
commercial insecticides, typically contains from 20% to 25% pyrethrins (21).
The insecticidal action of the pyrethrins is characterized by a rapid knockdown
effect, particularly in flying insects, and hyperactivity and convulsions in most
insects. These symptoms are a result of the neurotoxic action of the pyrethrins,
which block voltage-gated sodium channels in nerve axons. As such, the mech-
anism of action of pyrethrins is qualitatively similar to that of DDT and many
synthetic organochlorine insecticides. In purity, pyrethrins are moderately toxic to
mammals (rat oral acute LD50 values range from 350 to 500 mg kg−1 ), but techni-
cal grade pyrethrum is considerably less toxic (∼1500 mg kg−1 ) (21). Pyrethrins
are especially labile in the 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 hours or less (3).
This problem created the impetus for the development of synthetic derivatives
(“pyrethroids”) that are more stable in sunlight. The modern pyrethroids, devel-
oped 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 (18) in 2003 clearly demonstrate the dom-
inance of this material among botanicals: Pyrethrum accounted for 74% of all
botanicals used that year, but only 27% of that amount was used in agriculture
(∼800 kg). Major uses of pyrethrum in California are for structural pest control, in
public health, and for treatment of animal premises. Pyrethrum is the predominant
botanical in use, perhaps accounting for 80% of the global botanical insecticide
market (49).
For many years world production of pyrethrum was led by Kenya, with lesser
quantities produced in Tanzania and Ecuador. In the past five years, Botanical
Resources Australia, with plantings in Tasmania, has become the second largest
producer in the world (∼30% of world production at present). Pyrethrum produced
in Tasmania is qualitatively similar to that produced in East Africa and elsewhere,
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48 ISMAN

but the market share achieved by the Australian producer may not increase owing
to World Bank grants and government subsidies to producers in Kenya and China
(B. Chung, personal communication).

Neem
Two types of botanical insecticides can be obtained from seeds of the Indian neem
tree, Azadirachta indica (Meliaceae) (81). Neem oil, obtained by cold-pressing
by Jawaharlal Nehru Centre For Advanced Scientific Research on 08/31/10. For personal use only.

seeds, can be effective against soft-bodied insects and mites but is also useful
in the management of phytopathogens. Apart from the physical effects of neem
oil on pests and fungi, disulfides in the oil likely contribute to the bioactivity of
Annu. Rev. Entomol. 2006.51:45-66. Downloaded from [Link]

this material. More highly valued than neem oil are medium-polarity extracts of
the seed residue after removal of the oil, as these extracts contain the complex
triterpene azadirachtin (Figure 2). Neem seeds actually contain more than a dozen
azadirachtin analogs, but the major form is azadirachtin and the remaining mi-
nor analogs likely contribute little to overall efficacy of the extract. Seed extracts
include considerable quantities of other triterpenoids, notably salannin, nimbin,
and derivatives thereof. The role of these other natural substances has been con-
troversial, but most evidence points to azadirachtin as the most important active
principle (50). Neem seeds typically contain 0.2% to 0.6% azadirachtin by weight,
so solvent partitions or other chemical processes are required to concentrate this
active ingredient to the level of 10% to 50% seen in the technical grade material
used to produce commercial products.
Azadirachtin has two profound effects on insects. At the physiological level,
azadirachtin blocks the synthesis and release of molting hormones (ecdysteroids)
from the prothoracic gland, leading to incomplete ecdysis in immature insects. In
adult female insects, a similar mechanism of action leads to sterility. In addition,
azadirachtin is a potent antifeedant to many insects. The discovery of neem by
western science is attributed to Heinrich Schmutterer, who observed that swarming
desert locusts in Sudan defoliated almost all local flora except for some introduced
neem trees (69). Indeed, azadirachtin was first isolated based on its exceptional
antifeedant activity in the desert locust, and this substance remains the most potent
locust antifeedant discovered to date. Unlike pyrethrins, azadirachtin has defied
total synthesis to this point. Promoted in the United States by Robert Larson (with
assistance from the U.S. Department of Agriculture), neem rapidly became the
modern paradigm for development of botanical insecticides.
Enthusiasm for neem was fostered by several international conferences in the
1980s and 1990s, and several volumes dedicated to neem and neem insecticides
have been published (51, 69, 81). Unfortunately, neem’s commercial success has
fallen well short of the initial hype fueled by the explosive scientific literature sur-
rounding it. In part this is due to the relatively high cost of the refined product (48)
and the relatively slow action on pest insects. Nonetheless, several azadirachtin-
based insecticides are sold in the United States and at least two such products
in the European Union. In California, azadirachtin-based insecticides constituted
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BOTANICAL INSECTICIDES 49

about one third of the botanicals used in agriculture in 2003 (∼600 kg). In practice,
reliable efficacy is linked to the physiological action of azadirachtin as an insect
growth regulator; the antifeedant effect, which is spectacular in the desert locust,
is highly variable among pest species, and even those species initially deterred are
often capable of rapid desensitization to azadirachtin (13).
What is clear is that azadirachtin is considered nontoxic to mammals (rat oral
acute LD50 is >5000 mg kg−1 ), fish (88), and pollinators (71). The influence of
azadirachtin on natural enemies is highly variable (62, 83). Like the pyrethrins,
azadirachtin is rapidly degraded by sunlight. For example, on olives growing in
by Jawaharlal Nehru Centre For Advanced Scientific Research on 08/31/10. For personal use only.

Italy, azadirachtin has a half-life of approximately 20 h (16). On the other hand,

azadirachtin has systemic action in certain crop plants, greatly enhancing its effi-
Annu. Rev. Entomol. 2006.51:45-66. Downloaded from [Link]

cacy and field persistence (81).

Plant Essential Oils

Steam distillation of aromatic plants yields essential oils, long used as fragrances
and flavorings in the perfume and food industries, respectively, and more recently
for aromatherapy and as herbal medicines (14, 26). Plant essential oils are produced
commercially from several botanical sources, many of which are members of the
mint family (Lamiaceae). The oils are generally composed of complex mixtures
of monoterpenes, biogenetically related phenols, and sesquiterpenes. Examples
include 1,8-cineole, the major constituent of oils from rosemary (Rosmarinus
officinale) and eucalyptus (Eucalyptus globus); eugenol from clove oil (Syzygium
aromaticum); thymol from garden thyme (Thymus vulgaris); and menthol from
various species of mint (Mentha species) (45) (Figure 2). A number of the source
plants have been traditionally used for protection of stored commodities, especially
in the Mediterranean region and in southern Asia, but interest in the oils was
renewed with emerging demonstration of their fumigant and contact insecticidal
activities to a wide range of pests in the 1990s (46). The rapid action against
some pests is indicative of a neurotoxic mode of action, and there is evidence for
interference with the neuromodulator octopamine (29, 56) by some oils and with
GABA-gated chloride channels by others (77).
Some of the purified terpenoid constituents of essential oils are moderately
toxic to mammals, but, with few exceptions, the oils themselves or products based
on oils are mostly nontoxic to mammals, birds, and fish (46, 84). However, as
broad-spectrum insecticides, both pollinators and natural enemies are vulnerable
to poisoning by products based on essential oils. Owing to their volatility, essential
oils have limited persistence under field conditions; therefore, although natural
enemies are susceptible via direct contact, predators and parasitoids reinvading
a treated crop one or more days after treatment are unlikely to be poisoned by
residue contact as often occurs with conventional insecticides.
In the United States, commercial development of insecticides based on plant
essential oils has been greatly facilitated by exemption from registration for certain
oils commonly used in processed foods and beverages (78). This opportunity
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50 ISMAN
by Jawaharlal Nehru Centre For Advanced Scientific Research on 08/31/10. For personal use only.
Annu. Rev. Entomol. 2006.51:45-66. Downloaded from [Link]

Figure 1 Active constituents of some botanical insecticides from various plant sources
discussed in this review. (a) Nicotine, (b) pyrethrin I, (c) rotenone, (d ) cevadine, (e) ryan-
odine, and ( f ) asimicin.
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BOTANICAL INSECTICIDES 51
by Jawaharlal Nehru Centre For Advanced Scientific Research on 08/31/10. For personal use only.
Annu. Rev. Entomol. 2006.51:45-66. Downloaded from [Link]

Figure 2 Active constituents of some botanical insecticides from neem (a), Melia species
(b–d ), and selected plant essential oils (e–k). (a) Azadirachtin, (b) toosendanin, (c) 1-
cinnamoyl-3-feruoyl-11-hydroxymeliacarpin, (d ) volkensin, (e) d-limonene, ( f ) menthol,
(g) 1,8-cineole, (h) citronellal, (i) eugenol, ( j) p-menthane-3,8-diol, and (k) thymol.
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52 ISMAN

has spurred the development of essential oil-based insecticides, fungicides, and

herbicides for agricultural and industrial applications and for the consumer market,
using rosemary oil, clove oil, and thyme oil as active ingredients. Interest in these
products has been considerable, particularly for control of greenhouse pests and
diseases and for control of domestic and veterinary pests, with several private
companies (e.g., EcoSMART Technologies, Inc., United States) moving toward or
into the marketplace. Another factor favoring development of botanical insecticides
based on plant essential oils is the relatively low cost of the active ingredients, a
result of their extensive worldwide use as fragrances and flavorings. In contrast,
by Jawaharlal Nehru Centre For Advanced Scientific Research on 08/31/10. For personal use only.

pyrethrum and neem are used primarily for insecticide production (R. Georgis,
personal communication).
Annu. Rev. Entomol. 2006.51:45-66. Downloaded from [Link]

Rotenone and Other Extant Botanicals

As an insecticide, rotenone has been in use for more than 150 years, but its use as a
fish poison dates back even further (82). Rotenone is one of several isoflavonoids
produced in the roots or rhizomes of the tropical legumes Derris, Lonchocarpus,
and Tephrosia. Most rotenone used at present comes from Lonchocarpus grown in
Venezuela and Peru and is often called cubé root. Extraction of the root with organic
solvents yields resins containing as much as 45% total rotenoids; studies indicate
that the major constituents are rotenone (44%) (Figure 1) and deguelin (22%) (15,
30). Rotenone is commonly sold as a dust containing 1% to 5% active ingredients
for home and garden use, but liquid formulations used in organic agriculture can
contain as much as 8% rotenone and 15% total rotenoids.
Rotenone is a mitochondrial poison, which blocks the electron transport chain
and prevents energy production (41). As an insecticide it is considered a stomach
poison because it must be ingested to be effective. Pure rotenone is comparable
to DDT and other synthetic insecticides in terms of its acute toxicity to mammals
(rat oral LD50 is 132 mg kg−1 ), although it is much less toxic at the levels seen
in formulated products. Safety of rotenone has recently been called into question
because of (a) controversial reports that acute exposure in rats produces brain
lesions consistent with those observed in humans and animals with Parkinson’s
disease (10), and (b) the persistence of rotenone on food crops after treatment. A
study of rotenone residues on olives conducted in Italy determined that the half-
life of rotenone is 4 days, and at harvest residue levels were above the tolerance
limit (17). Moreover, residues were concentrated in oil obtained from the olives.
As an agricultural insecticide, use of rotenone is limited to organic food produc-
tion. In California, about 200 kg are used annually, mostly on lettuce and tomato
crops.
Sabadilla is a botanical insecticide obtained from the seeds of the South Ameri-
can lily Schoenocaulon officinale. In purity, the active principles, cevadine-type al-
kaloids (Figure 1), are extremely toxic to mammals (rat oral LD50 is ∼13 mg kg−1 ),
but commercial preparations typically contain less than 1% active ingredient, pro-
viding a margin of safety. The mode of action of these alkaloids is remarkably
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BOTANICAL INSECTICIDES 53

similar to that of the pyrethrins, despite their lack of structural similarity. Sabadilla
is used primarily by organic growers; in California about 100 kg is used annually,
primarily on citrus crops and avocado. Another botanical in declining use is ryania,
obtained by grinding the wood of the Caribbean shrub Ryania speciosa (Flacour-
tiaceae). The powdered wood contains <1% ryanodine (Figure 1), an alkaloid that
interferes with calcium release in muscle tissue (70). It is used to a limited extent
by organic apple growers for control of the codling moth, Cydia pomonella. More
information on sabadilla and ryania can be found in a recent review (90).
Like pyrethrum and rotenone, nicotine, an alkaloid obtained from the foliage of
by Jawaharlal Nehru Centre For Advanced Scientific Research on 08/31/10. For personal use only.

tobacco plants (Nicotiana tabacum) and related species, has a long history as an
insecticide. Nicotine (Figure 1) and two closely related alkaloids, nornicotine and
Annu. Rev. Entomol. 2006.51:45-66. Downloaded from [Link]

anabasine, are synaptic poisons that mimic the neurotransmitter acetylcholine. As

such, they cause symptoms of poisoning similar to those seen with organophos-
phate and carbamate insecticides (39). Owing to the extreme toxicity of pure
nicotine to mammals (rat oral LD50 is 50 mg kg−1 ) and its rapid dermal absorption
in humans, nicotine has seen declining use, primarily as a fumigant in greenhouses
against soft-bodied pests. However, there remains some interest in preparing stable
nicotine fatty acid soaps, presumably with reduced bioavailability and toxicity to
humans (20).

POTENTIAL NEW BOTANICALS

Annonaceous Acetogenins
Botanical insecticides have been traditionally prepared from the seeds of tropical
Annona species, members of the custard apple family (Annonaceae). These include
the sweetsop (A. squamosa) and soursop (A. muricata), important sources of fruit
juices in Southeast Asia. Detailed investigations in the 1980s led to the isolation
of a number of long-chain fatty acid derivatives, termed acetogenins, responsi-
ble for the insecticidal bioactivity. The major acetogenin obtained from seeds of
A. squamosa is annonin I, or squamocin, and a similar compound, asimicin
(Figure 1), was isolated from the bark of the American pawpaw tree, Asimina
triloba (53, 65). McLaughlin and colleagues (66) hold a U.S. patent on insecti-
cides based on acetogenins from A. triloba; Bayer AG (Germany) holds a similar
patent based on Annona acetogenins (67). These compounds are slow acting stom-
ach poisons, particularly effective against chewing insects such as lepidopterans
and the Colorado potato beetle (Leptinotarsa decemlineata).
Further investigations revealed that the acetogenins have a mode of action iden-
tical to that of rotenone, i.e., they block energy production in mitochondria in
both insects and mammals (61). In purity certain acetogenins are toxic to mam-
mals (LD50 is <20 mg kg−1 ), an impediment to regulatory approval, even though
standardized extracts from Annona seeds and Asimina bark are much less toxic.
McLaughlin and associates (53) have isolated hundreds of acetogenins from the
Annonaceae, and for many their potential as anticancer agents exceeds their value
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54 ISMAN

as insecticides. In spite of the patents based on the insecticidal activities of these

materials, no commercial development has proceeded with the exception of a head
lice shampoo that contains a standardized pawpaw extract among its active ingre-
dients (Nature’s Sunshine Products, Inc., United States). Annona seed extracts may
prove more useful in tropical countries where the fruits are commonly consumed
or used to produce fruit juice, in which case the seeds are a waste product. For
example, Leatemia & Isman (59, 60) recently demonstrated that crude ethanolic
extracts or even aqueous extracts of seeds from A. squamosa collected at several
sites in eastern Indonesia are effective against the diamondback moth (Plutella
by Jawaharlal Nehru Centre For Advanced Scientific Research on 08/31/10. For personal use only.

xylostella).
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Sucrose Esters
In the early 1990s scientists at the U.S. Department of Agriculture discovered that
sugar esters naturally occurring in the foliage of wild tobacco (Nicotiana gossei)
were insecticidal to certain soft-bodied insects and mites. Although patented (75),
extraction of these substances on a commercial scale from plant biomass proved
impractical, leading to the development of sucrose esters manufactured from sugar
and fatty acids obtained from vegetable oils. AVA Chemical Ventures (United
States) has patented and registered an insecticide/miticide based on C8 and C10 fatty
acid mono-, di-, and triesters of sucrose octanoate and sucrose dioctanoate (31).
The product, first registered in 2002, contains 40% active ingredient. Functionally,
this product appears to differ little from the insecticidal soaps based on fatty
acid salts developed in the 1980s, particularly potassium oleate. Both products
are contact insecticides that kill small insects and mites through suffocation (by
blocking the spiracles) or disruption of cuticular waxes and membranes in the
integument, leading to desiccation. Although useful in home and garden products
and in greenhouse production, the utility of these materials for agriculture remains
to be seen.

Melia Extracts
The remarkable bioactivity of azadirachtin from the Indian neem tree (Azadirachta
indica) led to the search for natural insecticides in the most closely related genus,
Melia. Seeds from the chinaberry tree, M. azedarach, contain a number of triter-
penoids, the meliacarpins (Figure 2), that are similar but not identical to the
azadirachtins, and these too have insect growth regulating bioactivities (58). But in
spite of the abundance of chinaberry trees in Asia and other tropical and subtropi-
cal areas to which they were introduced, development of commercial insecticides
has not paralleled that of the neem insecticides. The main reason is the pres-
ence, in chinaberry seeds, of additional triterpenoids, the meliatoxins, that have
demonstrated toxicity to mammals (4). However the chemistry of chinaberry varies
considerably across its natural and introduced range, and seeds of M. azedarach
growing in Argentina lack meliatoxins but produce triterpenoids (most notably
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BOTANICAL INSECTICIDES 55

meliartenin) that are strong feeding deterrents to pest insects and could prove
useful for pest management (19). Similar results have been obtained from South
Africa using aqueous extracts of chinaberry leaves, presumably lacking meliatox-
ins but efficacious against the diamondback moth (22).
In the early 1990s a botanical insecticide produced in China was based on an
extract of bark of Melia toosendan, a tree considered by most taxonomists to be
synonymous with M. azedarach. The extract contains a number of triterpenoids
based on toosendanin (Figure 2), a substance reported to be a stomach poison for
chewing insects (24). Later studies suggest that this substance acts primarily as a
by Jawaharlal Nehru Centre For Advanced Scientific Research on 08/31/10. For personal use only.

feeding deterrent but can also serve as a synergist for conventional insecticides (23,
32). Although relatively nontoxic to mammals, it is unclear whether this material
Annu. Rev. Entomol. 2006.51:45-66. Downloaded from [Link]

remains in production or whether it is sufficiently efficacious as a stand-alone crop

protectant.
When M. toosendan came under scientific scrutiny, investigation of the east
African M. volkensii demonstrated bioactivity in insects from seed extracts of this
species. The active principles in M. volkensii include the triterpenoid salannin, also
a major constituent of neem seed extracts, and some novel triterpenoids such as
volkensin (Figure 2). Collectively these function as feeding deterrents and stom-
ach poisons with moderate efficacy against chewing insects and as a mosquito
larvicide. Although a standardized seed extract has been made in quantities suf-
ficient for research (80), commercial production appears unlikely owing to a lack
of infrastructure for harvesting seeds in addition to regulatory impediments.

INSECT ANTIFEEDANTS AND REPELLENTS

Antifeedants
The possibility of using nontoxic deterrents and repellents as crop protectants is
intuitively attractive. The concept of using insect antifeedants (=feeding deter-
rents) gained strength in the 1970s and 1980s with the demonstration of the potent
feeding deterrent effect of azadirachtin and neem seed extracts to a large number of
pest species. Indeed, considerable literature, scientific and otherwise, touts neem
as a successful demonstration of the antifeedant concept. In reality, it is the phys-
iological actions of azadirachtin that appear most reliably linked to field efficacy
of neem insecticides (42); although purely behavioral effects cannot be ruled out,
there is hardly any irrefutable evidence or documentation of field efficacy based
on the antifeedant effects of neem alone.
As an academic exercise, the discovery and demonstration of plant natural prod-
ucts as insect antifeedants has been unquestionably successful. In addition to the
neem triterpenoids, extensive work has been performed on clerodane diterpenes
from the Lamiaceae (55) and sesquiterpene lactones from the Asteraceae (38).
On the other hand, not a single crop protection product based unequivocally on
feeding or oviposition deterrence has been commercialized. Two main problems
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56 ISMAN

face the use of antifeedants in agriculture (47). The first is interspecific variation
in response—even closely related species can differ dramatically in behavioral
responses to a substance—limiting the range of pests affected by a particular an-
tifeedant (43). Some substances that deter feeding by one pest can even serve as
attractants or stimulants for other pests. The second is the behavioral plasticity in
insects—pests can rapidly habituate to feeding deterrents, rendering them ineffec-
tive in a matter of hours. This has been recently demonstrated not only for pure
substances like azadirachtin (13), but also for complex mixtures (plant extracts)
(1). Whereas a highly mobile (flying) insect may leave a plant upon first encounter-
by Jawaharlal Nehru Centre For Advanced Scientific Research on 08/31/10. For personal use only.

ing an antifeedant, a less mobile one (larva) may remain on the plant long enough
for the deterrent response to wane. Such behavioral changes are important in light
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of the observation that some plant substances are initially feeding deterrents but
lack toxicity if ingested. Azadirachtin is clearly an exception to this rule, as inges-
tion leads to deleterious physiological consequences, but many other compounds
or extracts with demonstrated antifeedant effects lack toxicity when administered
topically or via injection (8, 9).

Repellents
For many chemists, an effective alternative to DEET (N,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 provides the
degree of protection against biting mosquitoes or persistence on human skin af-
forded by DEET (74). Concerns with the safety of DEET, especially to children,
have resulted in the introduction of several plant oils as natural alternatives. Some
personal repellents in the U.S. marketplace contain oils of citronella, eucalyp-
tus, or cedarwood as active ingredients; 2-phenethylpropionate, a constituent of
peanut oil, and p-menthane-3,8-diol (obtained from a particular species of mint)
(Figure 2) are also used in consumer products. All of these materials can pro-
vide some protection, but the duration of their effect can be limited (often <1 h)
(36). In tropical areas where mosquito-borne disease is a threat (e.g., yellow fever,
dengue, malaria), DEET probably remains the only reliable repellent. Oil of cit-
ronella or the constituent citronellal (Figure 2) is also used in mosquito coils to
repel mosquitoes from outdoor areas. Several veterinary products for flea and tick
control on domestic pets contain d-limonene (from citrus peels; Figure 2) as the
active ingredient. Other uses for repellents under investigation include perimeter
treatments of buildings to exclude termites and the use of essential oils to repel
cockroaches from kitchens and flies from dairy barns (64). Another important use
of plant essential oil constituents is in fumigation of beehives to manage econom-
ically important honey bee parasites, the Varroa mite (Varroa jacobsoni) and the
tracheal mite (Acarapis woodi). In North America, menthol (from peppermint;
Figure 2) is widely used for this purpose (27), and in Europe thymol (from garden
thyme; Figure 2) is most often used (34).
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BOTANICAL INSECTICIDES 57

CURRENT TRENDS IN THE USE OF BOTANICALS

North America
At present, the United States allows the broadest range of botanical insecticides
among industrialized countries, with registrations for pyrethrum, neem, rotenone,
several essential oils, sabadilla, ryania, and nicotine (Table 1). Several azadirachtin-
based (neem) insecticides are sold in the United States, and a number of plant
essential oils are exempt from registration altogether. Canada has been more con-
by Jawaharlal Nehru Centre For Advanced Scientific Research on 08/31/10. For personal use only.

servative with respect to pesticide registrations, allowing pyrethrum, rotenone, and

nicotine, but only a handful of essential oils (73). Neem has yet to achieve full
registration in Canada, to the disappointment of many organic growers. Mexico
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allows the use of most products sold in the United States, although there is no
specific exemption for plant oils.

Europe
Although considered by many in the agrochemical industry to be especially restric-
tive with respect to pesticide registrations, the European Union permits the use of
pyrethrum, neem, rotenone, and nicotine, along with “components of etheric oils

TABLE 1 Botanical insecticides approved for use in specific countries

Country Pyrethrum Rotenone Nicotine Neema Others

Australia X X — — Citrus oils

New Zealand X X — X
India X X X X Ryania
Philippines X — — —
Hungary X — — — Quassia
Denmark X X — — Lemongrass, clove,
eucalyptus oils
Germany X — — X
Netherlands X — — —
United Kingdom X X X —
South Africa X — — —
Brazil X X — X Garlic
United States X X X X Specified essential oils,
ryania, sabadilla
Canada X X X — Specified essential oils
Mexico X X — X Garlic, capsicum
a
Includes insecticides listing azadirachtin as the active ingredient.
Source: Reference 73 and personal communications (D. Badulescu, B. Chung, J. Immaraju & J. Vendramin).
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58 ISMAN

of plant origin” (73). Individual countries in western Europe show considerable

variation in the botanicals they permit. For example, Hungary permits pyrethrum
and nicotine, although the latter is severely restricted. Denmark permits only
pyrethrum and rotenone, Germany pyrethrum and neem. The Netherlands per-
mits pyrethrum alone. In spite of years of research on azadirachtin and neem in
the United Kingdom, this botanical has never achieved registration there, leaving
pyrethrum, rotenone, and nicotine as the only approved botanicals.

Pacific/Asia
by Jawaharlal Nehru Centre For Advanced Scientific Research on 08/31/10. For personal use only.

India appears to embrace botanicals more than many other countries in the region,
permitting all of the materials (save sabadilla) mentioned herein and allowing
Annu. Rev. Entomol. 2006.51:45-66. Downloaded from [Link]

new products provisional registration while toxicological and environmental data

in support of full registration are acquired. New Zealand has registrations for
pyrethrum, rotenone, and neem, whereas Australia has yet to approve neem in
spite of almost two decades of research and development in that country. Likewise,
neem has yet to be approved for use in the Philippines, where pyrethrum is the
only approved botanical insecticide.

Latin America
In Brazil, each state has autonomous regulatory authority. Botanicals registered
in most states include pyrethrum, rotenone, neem, and garlic, although nicotine
and extracts of native plants are used to a small extent (J. Vendramin, personal
communication). Throughout Latin America plant oils and extracts are produced
by cottage industries on a small scale and used outside of any regulatory system
on a regional basis (D. Badulescu, personal communication).

Africa
Data on regulated insecticides are not readily available for most African countries.
Among botanicals, only pyrethrum is approved for use in South Africa. As in
Latin America, numerous crude plant extracts and oils are likely in local use in the
poorer countries.

Trends and Changes in Registration

Given the ongoing negative perception of pesticides by the general public, govern-
ment response to that perception, and increasing documentation of environmental
contamination, it is hard to imagine pesticide regulators easing toxicological re-
quirements for new pesticides, with the possible exception of certain plant oils
and extracts widely used in human foods. Globalization of agricultural commodi-
ties will serve only to tighten restrictions on pesticide use in developing countries
where fresh produce for export to wealthier countries is an important source of
revenue. All produce imported into the European Union, United States, and Japan
(for example) must comply with pesticide regulations in the respective importing
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BOTANICAL INSECTICIDES 59

country, meeting the same standards as their own domestic produce. As a result,
pesticide regulations set in the wealthiest countries have global reach—they affect
growers directly in developing countries who are forced to comply. In short, a
lack of confidence in the safety of a specific botanical insecticide by the European
Union could make that product unfavorable in a tropical country, even where it
makes sense for poorer growers providing agricultural produce for their domestic
markets, and perhaps where the botanical source material grows and could be inex-
pensively prepared for crop protection. If nothing else, this review should highlight
the fact that few new botanical insecticides are likely to see commercialization on
by Jawaharlal Nehru Centre For Advanced Scientific Research on 08/31/10. For personal use only.

a meaningful scale in the near future, in spite of the continual discovery of plant
natural products with bioactivity against insect pests.
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DRAWBACKS AND BARRIERS TO COMMERCIALIZATION

In reviewing this subject previously (44), I identified three main barriers to com-
mercialization for botanical insecticides: sustainability of the botanical resource,
standardization of chemically complex extracts, and regulatory approval. For each
of these there are also important cost considerations. Other drawbacks or limita-
tions are the slow action of many botanicals—growers must gain confidence in
insecticides that do not produce an immediate “knockdown” effect—and the lack
of residual action for most botanicals.

Sustainability
To produce a botanical insecticide on a commercial scale, the source plant biomass
must be obtainable on an agricultural scale and preferably not on a seasonal
basis. Unless the plant in question is extremely abundant in nature, or already
grown for another purpose (e.g., sweetsop, Annona squamosa, grown for its
edible fruit; rosemary, Rosmarinus officinale, as a flavoring), it must be amenable
to cultivation. Pyrethrum and neem meet this criterion; the latter has been exten-
sively introduced into Africa, Australia, and Latin America, more so as a shade
tree, windbreak, or source of firewood than for its yield of natural medicines
or insecticides. Research aimed at producing azadirachtin from neem tissue cul-
ture provided proof of concept, but economic feasibility has yet to be attained
(2).
In the not-too-distant future it may be possible to produce botanical insecticides
by “phytopharming,” i.e., through genetic engineering of an existing field crop to
produce high-value natural products originally isolated from a different botanical
source. But as progress in plant biotechnology continues at a rapid pace, it may
prove just as easy to modify the plants we wish to protect from pests directly, such
that they produce the natural product protectant constitutively, alleviating the need
to obtain the desired botanical product through extraction, formulate it, and then
apply it to the crop we wish to protect. These sorts of technological advancements
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60 ISMAN

seem far more likely now than they did even a decade ago; however, the cost
of these technologies will dictate that the traditional means of obtaining botanical
insecticides, and indeed their minor uses (on small acreage specialty crops) or uses
in developing countries on lesser value crops will continue for many years to come.
For example, neem seed oil had a long history of use in India for the production of
soaps and low grade industrial oil. When extraction companies began purchasing
neem seeds in bulk to produce insecticides, the price of seeds increased 10-fold.
In contrast, certain plant essential oils have numerous uses as fragrances and
flavorings, and the massive volumes required to satisfy these industries maintain
by Jawaharlal Nehru Centre For Advanced Scientific Research on 08/31/10. For personal use only.

low prices that make their use as insecticides attractive.

Annu. Rev. Entomol. 2006.51:45-66. Downloaded from [Link]

Standardization of Botanical Extracts

An often cited drawback to the adoption of botanical insecticides by growers is the
variation in performance of a particular product, even when prepared by the same
process. Natural variation in the chemistry of a plant-based commodity should
come as no surprise to anyone who enjoys coffee, tea, wine, or chocolate. Recent
investigation of seed extracts from sweetsop (A. squamosa) collected in Indonesia
demonstrated both geographical and annual variation in their insecticidal potency
(60). For a botanical insecticide to provide a reliable level of efficacy to the user,
there must be some degree of chemical standardization, presumably based on the
putative active ingredient(s). This has certainly been achieved with more refined
products based on pyrethrum, neem, and rotenone, but crude preparations often
contain low concentrations of active ingredients without adequate quantitation.
To achieve standardization, the producer must have an analytical method and the
equipment necessary for analysis and may need to mix or blend extracts from
different sources, which requires storage facilities and is partially dependent on
the inherent stability of the active principles in the source plant material or extracts
thereof held in storage (5).

Regulatory Approval
Regulatory approval remains the most formidable barrier to the commercializa-
tion of new botanical insecticides. In many jurisdictions, no distinction is made
between synthetic pesticides and biopesticides, including botanicals. Simply put,
the market for botanicals in industrialized countries—based mostly on uses in
greenhouse production and organic agriculture—is too small to generate suffi-
cient profits to offset multimillion dollar regulatory costs. Unfortunately, this sit-
uation may prevent many “green” pesticides from reaching the marketplace in
countries where the demand is greatest. I am not making the case that botanicals
should be exempt from all regulatory scrutiny; as discussed above, nicotine is
as toxic and hazardous as many synthetic insecticides, and strychnine, still used
for rodent and insect control in some regions, is responsible for some human
poisonings (54). Natural products can pose risks, and safety cannot be assumed
(25, 87). But most of the botanicals discussed in this review are characterized by
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BOTANICAL INSECTICIDES 61

low mammalian toxicity, reduced effects on nontarget organisms, and minimal

environmental persistence.
As noted, several plant essential oils and their constituents are exempt from
registration in the United States, attributed to their long use history as food and
beverage flavorings or as culinary spices. This exemption has facilitated the rapid
development and commercialization of insecticides based on these materials as
active ingredients (46). Although other jurisdictions have yet to follow the lead
of the United States in this regard, there are proposals in some Asian countries
to exempt some types of pesticides from registration for specific uses in public
by Jawaharlal Nehru Centre For Advanced Scientific Research on 08/31/10. For personal use only.

health, for example, in head lice preparations or for cockroach and fly suppression.
It seems that regulatory agencies continue to focus their efforts on protecting the
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general public from miniscule traces of pesticides in the food supply rather than
focusing on the safety of applicators and farmworkers, for whom, arguably, the
more demonstrable hazards occur.

ROLE OF BOTANICALS IN THE FUTURE

What role can botanical insecticides play in crop protection and for other uses in
the near future? In industrialized countries it is hard to imagine botanicals playing
a greater role than at present, except in organic food production. Organic produc-
tion is estimated to be growing by 8% to 15% per annum in Europe and in North
America (70), and it is in those marketplaces that botanicals face the fewest com-
petitors. Even there, however, microbial insecticides and spinosad have proven
efficacious and cost-effective. Rather than considered as stand-alone products,
botanicals might be better placed as products in crop protectant rotations, espe-
cially in light of the documented resistance of the diamondback moth to Bacillus
thuringiensis and spinosad due to overuse (85, 91). In conventional agriculture,
botanicals face tremendous competition from the newest generation of “reduced
risk” synthetic insecticides such as the neonicotinoids. Between 1998 and 2003,
use of reduced risk pesticides in California increased more than threefold (from
138 to 483 tons), whereas biopesticide use declined (from 652 to 472 tons) (18).
Botanicals, constituting less than 1% of biopesticide use in California (18), are
also in decline. Overall, it is hard not to conclude that the best role for botanicals
in the wealthier countries is in public health (mosquito, cockroach abatement) and
for consumer (home and garden) use.
The real benefits of botanical insecticides can be best realized in developing
countries, where farmers may not be able to afford synthetic insecticides and the
traditional use of plants and plant derivatives for protection of stored products is
long established. Even where synthetic insecticides are affordable to growers (e.g.,
through government subsidies), limited literacy and a lack of protective equipment
result in thousands of accidental poisonings annually (35).
Recent attention has been paid to traditional plants used in West Africa for
postharvest protection against insects (6, 11, 12). Some of the more efficacious
plants used have well-known active principles (e.g., rotenoids from Tephrosia,
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62 ISMAN

nicotine from Nicotiana, methyl salicylate from Securidaca, and eugenol from
Ocimum); some of these are volatile and act as natural fumigants that kill adult
pests and their progeny (52). At least one study indicates that these materials are
relatively safe in the forms in which they are used (7). Some plant products could
even be useful in industrialized countries for the protection of grain from storage
pests (33).
Many of the plants discussed in this review are tropical in distribution and the-
oretically available to growers in developing countries. However, efficacy against
pests is only one factor in the adoption of botanicals—logistics of production,
by Jawaharlal Nehru Centre For Advanced Scientific Research on 08/31/10. For personal use only.

preparation, or use of botanicals can mitigate against their use (68). Perhaps it is
time to refocus the attention of the research community toward the development
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and application of known botanicals rather than screen more plants and isolate
further novel bioactive substances that satisfy our curiosity but are unlikely to be
of much utility.

ACKNOWLEDGMENTS
I thank NSERC (Canada) and EcoSMART Technologies, Inc., for supporting orig-
inal research on botanical insecticides and antifeedants in my laboratory. Industrial
colleagues in western Europe, Latin America, and Australia provided information
on registered botanical insecticides in their regions.

The Annual Review of Entomology is online at [Link]

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Annual Review of Entomology

Volume 51, 2006

CONTENTS
SIGNALING AND FUNCTION OF INSULIN-LIKE PEPTIDES IN INSECTS,
by Jawaharlal Nehru Centre For Advanced Scientific Research on 08/31/10. For personal use only.

Qi Wu and Mark R. Brown 1

PROSTAGLANDINS AND OTHER EICOSANOIDS IN INSECTS: BIOLOGICAL
Annu. Rev. Entomol. 2006.51:45-66. Downloaded from [Link]

SIGNIFICANCE, David Stanley 25

BOTANICAL INSECTICIDES, DETERRENTS, AND REPELLENTS IN
MODERN AGRICULTURE AND AN INCREASINGLY REGULATED
WORLD, Murray B. Isman 45
INVASION BIOLOGY OF THRIPS, Joseph G. Morse and Mark S. Hoddle 67
INSECT VECTORS OF PHYTOPLASMAS, Phyllis G. Weintraub
and LeAnn Beanland 91
INSECT ODOR AND TASTE RECEPTORS, Elissa A. Hallem, Anupama
Dahanukar, and John R. Carlson 113
INSECT BIODIVERSITY OF BOREAL PEAT BOGS, Karel Spitzer
and Hugh V. Danks 137
PLANT CHEMISTRY AND NATURAL ENEMY FITNESS: EFFECTS ON
HERBIVORE AND NATURAL ENEMY INTERACTIONS, Paul J. Ode 163
APPARENT COMPETITION, QUANTITATIVE FOOD WEBS, AND THE
STRUCTURE OF PHYTOPHAGOUS INSECT COMMUNITIES,
F.J. Frank van Veen, Rebecca J. Morris, and H. Charles J. Godfray 187
STRUCTURE OF THE MUSHROOM BODIES OF THE INSECT BRAIN,
Susan E. Fahrbach 209
EVOLUTION OF DEVELOPMENTAL STRATEGIES IN PARASITIC
HYMENOPTERA, Francesco Pennacchio and Michael R. Strand 233
DOPA DECARBOXYLASE: A MODEL GENE-ENZYME SYSTEM FOR
STUDYING DEVELOPMENT, BEHAVIOR, AND SYSTEMATICS,
Ross B. Hodgetts and Sandra L. O’Keefe 259
CONCEPTS AND APPLICATIONS OF TRAP CROPPING IN PEST
MANAGEMENT, A.M. Shelton and F.R. Badenes-Perez 285
HOST PLANT SELECTION BY APHIDS: BEHAVIORAL, EVOLUTIONARY,
AND APPLIED PERSPECTIVES, Glen Powell, Colin R. Tosh,
and Jim Hardie 309

vii
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November 2, 2005 13:47 Annual Reviews AR263-FM

viii CONTENTS

BIZARRE INTERACTIONS AND ENDGAMES: ENTOMOPATHOGENIC

FUNGI AND THEIR ARTHROPOD HOSTS, H.E. Roy,
D.C. Steinkraus, J. Eilenberg, A.E. Hajek, and J.K. Pell 331
CURRENT TRENDS IN QUARANTINE ENTOMOLOGY, Peter A. Follett
and Lisa G. Neven 359
THE ECOLOGICAL SIGNIFICANCE OF TALLGRASS PRAIRIE
ARTHROPODS, Matt R. Whiles and Ralph E. Charlton 387
MATING SYSTEMS OF BLOOD-FEEDING FLIES, Boaz Yuval 413
by Jawaharlal Nehru Centre For Advanced Scientific Research on 08/31/10. For personal use only.

CANNIBALISM, FOOD LIMITATION, INTRASPECIFIC COMPETITION, AND

THE REGULATION OF SPIDER POPULATIONS, David H. Wise 441
Annu. Rev. Entomol. 2006.51:45-66. Downloaded from [Link]

BIOGEOGRAPHIC AREAS AND TRANSITION ZONES OF LATIN AMERICA

AND THE CARIBBEAN ISLANDS BASED ON PANBIOGEOGRAPHIC AND
CLADISTIC ANALYSES OF THE ENTOMOFAUNA, Juan J. Morrone 467
DEVELOPMENTS IN AQUATIC INSECT BIOMONITORING: A
COMPARATIVE ANALYSIS OF RECENT APPROACHES, Núria Bonada,
Narcı́s Prat, Vincent H. Resh, and Bernhard Statzner 495
TACHINIDAE: EVOLUTION, BEHAVIOR, AND ECOLOGY,
John O. Stireman, III, James E. O’Hara, and D. Monty Wood 525
TICK PHEROMONES AND THEIR USE IN TICK CONTROL,
Daniel E. Sonenshine 557
CONFLICT RESOLUTION IN INSECT SOCIETIES, Francis L.W. Ratnieks,
Kevin R. Foster, and Tom Wenseleers 581
ASSESSING RISKS OF RELEASING EXOTIC BIOLOGICAL CONTROL
AGENTS OF ARTHROPOD PESTS, J.C. van Lenteren, J. Bale, F. Bigler,
H.M.T. Hokkanen, and A.J.M. Loomans 609
DEFECATION BEHAVIOR AND ECOLOGY OF INSECTS, Martha R. Weiss 635
PLANT-MEDIATED INTERACTIONS BETWEEN PATHOGENIC
MICROORGANISMS AND HERBIVOROUS ARTHROPODS,
Michael J. Stout, Jennifer S. Thaler, and Bart P.H.J. Thomma 663

INDEXES
Subject Index 691
Cumulative Index of Contributing Authors, Volumes 42–51 717
Cumulative Index of Chapter Titles, Volumes 42–51 722

ERRATA
An online log of corrections to Annual Review of Entomology
chapters may be found at [Link]

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