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* Tel.: #1-604-822-2329; fax: #1-604-822-8640.
E-mail address: murray.isman@ubc.ca (M.B. Isman).
Crop Protection 19 (2000) 603}608
Plant essential oils for pest and disease management
Murray B. Isman*
Faculty of Agricultural Sciences, University of British Columbia, Suite 248, 2357 Main Mall, Vancouver, BC, Canada V6T 1Z4
Abstract
Certain essential plant oils, widely used as fragrances and #avors in the perfume and food industries, have long been reputed to repel
insects. Recent investigations in several countries con"rm that some plant essential oils not only repel insects, but have contact and
fumigant insecticidal actions against speci"c pests, and fungicidal actions against some important plant pathogens. As part of an e!ort
aimed at the development of reduced-risk pesticides based on plant essential oils, toxic and sublethal e!ects of some essential oil
terpenes and phenols have been investigated using the tobacco cutworm (Spodoptera litura) and the green peach aphid (Myzus persicae)
as model pest species. In this paper I review (i) the range of biological activities of essential oils and their constituents; (ii) their toxicity
and proposed mode-of-action in insects; (iii) their potential health and environmental impacts as crop protectants; and (iv)
commercialization of pesticides based on plant essential oils. 2000 Elsevier Science Ltd. All rights reserved.
Keywords: Plant essential oils; Natural pesticides; Monoterpenoids
1. Introduction
In spite of widespread public concern for long-term
health and environmental e!ects of synthetic pesticides,
especially in Europe and North America, natural pestici-
des, both of microbial and plant origin, have yet to have
much impact in the marketplace. Bioinsecticides, domin-
ated by Bacillus thuringiensis-based products, and botan-
ical insecticides, dominated by pyrethrum-based
products, each command little more than 1% of the
global insecticide market. However, recent government
action in the United States, in the form of the Food
Quality Protection Act of 1996, will dramatically restrict
the use of many conventional insecticides upon which
growers have depended for decades (e.g. organophos-
phates and carbamates). In turn, this will create a signi"-
cant market opportunity for alternative products, in
particular `reduced-riska pesticides which are favored by
the Environmental Protection Agency in the USA.
Against this backdrop, natural pesticides based on
plant-essential oils may represent alternative crop pro-
tectants whose time has come. Essential oils, obtained by
steam distillation of plant foliage, and even the foliage
itself of certain aromatic plants (notably in the families
Myrtaceae and Lamiaceae, but in other plant families as
well) have traditionally been used to protect stored grain
and legumes, and to repel #ying insects in the home.
Though some of the claims made for these crude prepara-
tions have yet to be substantiated through controlled
experiments, scienti"c investigation into the biological
activities of these materials proliferated in the past dec-
ade. The emerging picture is that certain, speci"c oils and
their chemical constituents have demonstrable contact
and fumigant toxicity to a number of economically im-
portant insect and mite pests, as well as to plant patho-
genic fungi.
2. Biological activities of essential oils and
their constituents
Contact and fumigant insecticidal actions of plant
essential oils have been well demonstrated against
stored product pests. Among 22 essential oils tested as
fumigants against the bean weevil Acanthoscelides obtec-
tus (Bruchidae), those of Thymus serpyllum (rich in the
phenols thymol and carvacrol) and Origanum majorama
(rich in terpinen-4-ol) were the most toxic (Regnault-
Roger et al., 1993). In a more detailed study, Shaaya et al.
(1991) evaluated the fumigant toxicity of 28 essential oils
and 10 of their major constituents against four di!erent
0261-2194/00/$- see front matter 2000 Elsevier Science Ltd. All rights reserved.
PII: S 0 2 6 1 - 2 1 9 4 ( 0 0 ) 0 0 0 7 9 - X
species of stored product coleopterans. Most interesting-
ly, there was little overlap among the insect species with
respect to the most toxic oils and constituents, indicating
that while these substances are generally active against
a broad spectrum of pests, interspeci"c toxicity of indi-
vidual oils and compounds is highly idiosyncratic. Sarac
and Tunc (1995), investigating the fumigant action of four
essential oils to three species of stored product pests,
reached the same conclusion. A number of investigations
by Ho and colleagues (Ho et al., 1994, 1995, 1997; Huang
and Ho, 1998; Huang et al., 1998) have demonstrated
contact, fumigant and antifeedant e!ects of a range of
essential oil constituents (cinnamaldehyde, -pinene,
anethole, extracts of cloves, Syzygium aromaticum, and
star anise, Illicium verum) against the red #our beetle
Tribolium castaneum and the maize weevil Sitophilus
zeamais. Eugenol, the major constituent of oil of cloves
and also of the holy basil, Ocimum suave, was shown to be
e!ective against these and two additional coleopterans,
S. granarius and Prostephanus truncatus (Obeng-Ofori
and Reichmuth, 1997).
Recent studies have also indicated e$cacy against
pests on plants. Essential oils of cumin (Cuminum
cyminum), anise (Pimpinella ansium), oregano (Origanum
syriacum var. bevanii) and eucalyptus (Eucalyptus camal-
dulensis) were e!ective as fumigants against the cotton
aphid (Aphis gossypii) and the carmine spider mite (Tet-
ranychus cinnabarinus), two greenhouse pests (Tuni and
Sahinkaya, 1998). E$cacy of basil (Ocimum spp.) against
garden pests has recently been reviewed (Quarles, 1999).
Lee et al. (1997) reported on the toxicity of a range of
essential oil constituents to the western corn rootworm
(Diabrotica virgifera), the two-spotted spider mite (Tet-
ranychus urticae) and the house#y (Musca domestica), and
dietary e!ects of a number of monoterpenoids against the
European corn borer (Ostrinia nubilalis) have been re-
cently reported (Lee et al., 1999). There is even evidence
that certain essential oils and their constituents are e!ec-
tive against Varroa jacobsoni, an ectoparasite of the
honey bee (Calderone et al., 1997).
However, systematic investigation of the antifungal
activities of essential oils and their constituents predate
those of the insecticidal properties. Kurita et al. (1981)
screened 40 such compounds against seven species of
fungi (primarily food spoilage organisms), and Singh
et al. (1980) similarly screened "ve essential oils against
22 species of fungi, including both human and plant
pathogenic types. More recently, Muller-Riebau et al.
(1995) screened nine essential oils against four species of
plant pathogenic fungi, whereas Wilson et al. (1997)
screened 49 essential oils against the fruit pathogen
Botrytis cinerea. In the former study, antifungal activity
was strongly associated with monoterpenic phenols, es-
pecially thymol, carvacrol and eugenol, in the oils. Some
of the essential oils and constituents found to be insecti-
cidal (e.g. eugenol) were previously reported to be active
against a range of plant pathogenic nematodes
(Sangwan et al., 1990), and most recently some essential
oils were shown to e!ectively inhibit plant germination,
suggesting their potential use as bioherbicides (Dudai
et al., 1999).
3. Toxicity to insects
The aforementioned studies with insects convincingly
demonstrate the fumigant toxicity of essential oils and
their constituents. Knockdown activity and lethal toxic-
ity via contact has been demonstrated in the American
cockroach (Periplaneta americana) (Ngoh et al., 1998), the
German cockroach (Blattella germanica) and the house#y
(Musca domestica) (Rice and Coats, 1994, Coats et al.,
1991). These studies latter point to an obvious neurotoxic
site-of-action. Certain essential oil monoterpenes are
competitive inhibitors of acetylcholinesterase in vitro
(Grundy and Still, 1985; Miyazawa et al., 1997), but this
action may not be correlated with toxicity to insects
in vivo.
A recent investigation by Enan et al. (1998) using the
American cockroach points to the octopaminergic ner-
vous system as the site-of-action in insects. The binding
of H-octopamine in a cockroach nerve cord protein
preparation was signicantly a!ected in the presence of
a number of essential oil constituents. The lack of octo-
pamine receptors in vertebrates likely accounts for the
profound mammalian selectivity of essential oils as insec-
ticides (i.e. they are toxic to insects but not to mammals),
and thus the octopaminergic system of insects represents
a biorational target for insect control. Investigation of
the formamidine insecticides revealed interesting and po-
tentially important sublethal behavioral and physiolo-
gical e!ects, presumably mediated by the octopaminergic
nervous system (Matsumura and Beeman, 1982). Sub-
lethal e!ects observed with some of the essential oil
compounds (viz., feeding deterrence, repellency) may be
consistant with this mode-of-action.
To that end, the apparent correlation between the
feeding deterrent e!ect of several monoterpenoids and
their topical LD

values in the tobacco cutworm
(Spodoptera litura) (Noctuidae) is noteworthy (Fig. 1, Is-
man, unpublished data). Feeding deterrence was mea-
sured in early 5th instar larvae (avg. wt.103 mg) using
a cabbage leaf disc choice bioassay (n20) (Bomford
and Isman, 1996). Mortality was assessed following topi-
cal administration (1 l acetone carrier) to the dorsum of
3rd instar larvae (avg.wt.18 mg; n250).
Green peach aphid nymphs (2nd instar) show both
behavioral e!ects and toxicity in a laboratory bioassay
where aphids are placed on mustard cabbage (`pak
choia) leaf discs dipped in emulsions of an essential oil
based insecticide (a proprietary mixture of eugenol,
thymol and phenethylpropionate as active ingredients;
604 M.B. Isman / Crop Protection 19 (2000) 603}608
Fig. 1. Relationship between feeding deterrence and topical toxicity of
selected monoterpenes and related phenols to the tobacco cutworm
Spodoptera litura. Feeding deterrence determined for leaf discs treated
with essential oil compounds at 150 g cm.
Fig. 2. Behavioral and toxic e!ects of an essential oil-based insecticide
to the green peach aphid Myzus persicae in a laboratory leaf disc
bioassay; (a) at 24 h, (b) at 48 h. Error bars represent standard error of
the mean (n15}25 replicates with 10 insects per replicate).
Fig. 3. Chemical structures of some monoterpenes and related phenols
with insecticidal activities.
EcoSMART Technologies Inc.) at various concentra-
tions (Fig. 2). While 90% of nymphs placed on carrier-
treated control leaf discs settled and were actively feeding
after 24 h, 50% or fewer aphids fed on treated discs, and
the frequency of aphids feeding was inversely concentra-
tion-dependent. Interestingly, approximately 20% of the
aphids in all treatment groups (except controls) were
found walking in the petri dish, o! the leaf discs, after
24 h. Results were even more striking at the 48 h time of
observation: at the lowest concentration tested (0.18%),
the number of aphids feeding on discs declined from 50%
at 24 h to 25%, and the number of dead aphids at this
concentration increased from 22 to 60%.
Another important aspect of the toxicity of essential oil
constituents, seen previously in studies with the intact
oils themselves, are interspecic di!erences in susceptibil-
ity. Table 1 shows LD

or LC

values for two closely
related monoterpenes ( -terpineol and terpinen-4-ol) and
two monoterpenoid phenols (eugenol and carvacrol)
(Fig. 3) tested against four species of insects and against
the two-spotted spider mite. For the tobacco cutworm,
the terpenes and eugenol are comparable in toxicity,
whereas carvacrol is at least three times more active; in
the case of the house#y, -terpineol is about one-half as
active as the other three which are similar in activity. In
the fruit #y (Drosophila melanogaster), the terpenes are
themselves equipotent, as are the phenols, but the phen-
ols are about 3.5 times more active than the terpenes.
Eugenol is 7}9 times more toxic than the two terpenes in
the western corn rootworm beetle (Diabrotica virgifera
virgifera), but in the two-spotted spider mite, terpinen-4-
ol is more than twice as active as eugenol, and six times
more active than carvacrol. The salient point is that these
chemicals and other essential oil constituents can be
blended to achieve a desired spectrum of activity and
optimal e$cacy against pests. However, investigations of
M.B. Isman / Crop Protection 19 (2000) 603}608 605
Table 1
Toxicity of selected essential oil monoterpenes and phenols to four species of insect and one species of mite
Species (units) LD

or LC

Eugenol Carvacrol -terpineol Terpinen!4-ol
Spodoptera litura ( g larva) 157.6 42.7 141.3 130.4
Drosophila melanogaster ( g cm) 4.6 4.8 17.4 17.7
Musca domestica ( g #y) 77 92 173 79
Diabrotica virgifera ( g beetle) 12 NT 112 90
Tetranychus urticae (ppm) 219 629 NT 96
Application methods: S. litura (3rd instar), D. virgifera (3rd instar), M. domestica (adult) * topical administration to the dorsum using 1 l acetone;
D. melanogaster (adult) * residue on inner walls of glass vials; T. urticae (adult) * bean leaves dipped in 5% aqueous acetone solutions.
Data for Spodoptera and Drosophila unpublished; for Musca, Diabrotica and Tetranychus from, Lee et al. (1997).
Not tested.
Table 2
Toxicity of some pesticide active ingredients to juvenile rainbow trout
in static water tests (modied from Stroh et al., 1998)
Compound or product (% as active ingredient) 96 h LC

(ppm)
Eugenol (90%) 60.8
Thyme oil (90%) 16.1
-terpineol (90%) 6.6
Emulsier 18.2
Neem (3% azadirachtin) 4.0
Pyrethrum (20% pyrethrins) 0.04
Rotenone (44%) 0.03
Azinphosmethyl (94%) 0.004
Endosulfan (96%) 0.001
Proprietary blend of anionic and nonionic emulsiers.
structure-activity relations among these compounds with
respect to their toxicity to insects (e.g. Rice and Coats
1994) have not proven especially fruitful as far as predic-
ting which compounds will be most e$cacious to any
particular type of pest.
4. Health and environmental impacts
Perhaps the most attractive aspect of using essential
oils and/or their constituents as crop protectants (and in
other contexts for pest management) is their favorable
mammalian toxicity. Some of the pure essential oil com-
pounds are slightly toxic, with rat acute oral LD

values
of 2}3 g kg (viz. carvacrol, pulegone), but an essential
oil insecticide consisting of a proprietary mixture of es-
sential oil constituents (EcoSMART Technologies Inc.),
resulted in no mortality when fed to rats at 2 g kg
(Enan, unpublished data), the upper limit required for
acute toxicity tests by most pesticide regulatory agencies
including the EPA. in the United States. In that many of
the essential oils and their constituents are commonly
used as culinary herbs and spices, pesticide products
containing certain of these are actually exempt from
toxicity data requirements by the EPA.
Static water toxicity tests using juvenile rainbow trout
(Oncorhynchus mykiss) indicated that based on 96 h-LC

values, eugenol is approximately 1500 times less toxic
than the botanical insecticide pyrethrum, and 15,000
times less toxic than the organophosphate insecticide
azinphosmethyl (Stroh et al., 1998; Table 2). In addition,
eugenol and other essential oil constituents are non-
persistent in fresh water, based on laboratory tests. These
compounds are also non-persistent in soils: under aero-
bic conditions at 233C, the half-life for -terpineol ranges
from 30}40 h, with complete degradation by 50 h
(Misra and Pavlostathis, 1997). Eugenol is completely
broken down to common organic acids by soil-borne
Pseudomonas bacteria (Rabenhorst, 1996). Concerns for
residues of essential oil pesticides on food crops should
be mitigated by the growing body of evidence that some
essential oil constituents acquired through the diet are
actually benexcial to human health (Huang et al., 1994).
5. Commercialization of essential oil-based pesticides
In a recent review paper on neem and other botanical
insecticides, three barriers to the commercialization of
new products of this type were identied: (i) the scarcity
of the natural resource; (ii) the need for chemical stan-
dardization and quality control; and (iii) di$culties in
registration. As the essential oils and their puried con-
stituents have a long history of global use by the food and
fragrance industries, and most recently in the eld of
aromatherapy, many of the oils and/or constituents that
are pesticidal are readily available at low to moderate
cost in quantity (USD 7}30 kg). A number of constitu-
ents are available commercially in reasonable purity
(95%), and essential oil producers and suppliers can often
provide chemical specications for even the most com-
plex oils.
Of most importance, some of these materials are
exempt from the usual data requirements for registration,
606 M.B. Isman / Crop Protection 19 (2000) 603}608
if not exempt from registration altogether (at least in the
USA.). Some American companies have recently taken
advantage of this situation and have been able to bring
essential-oil-based pesticides to market in a far shorter
time period than would normally be required for a con-
ventional pesticide. Mycotech Corporation produces
Cinnamite2+, an aphidicide/miticide/fungicide for glass-
house and horticultural crops, and Valero2+, a mitic-
ide/fungicide for use in grapes, berry crops, citrus and
nuts. Both products are based on cinnamon oil, with
cinnamaldehyde (30% in EC formulations) as the active
ingredient.
With over a dozen registered products by the end of
1999, EcoSMART Technologies is aiming to become
a world leader in essential oil-based pesticides. They
currently produce aerosol and dust formulations con-
taining proprietary mixtures of essential oil compounds,
including eugenol and 2-phenethyl propionate aimed at
controlling domestic pests (cockroaches, ants, #eas, #ies,
wasps, etc.). These are marketed to pest control profes-
sionals under the brand name EcoPCO0, with less
concentrated formulations for sale to the consumer
under the name Bioganic2+. Insecticides and miticides
for horticultural crops and for glasshouse and nursery
crops will be released shortly. Additional products
(e.g. EcoVET2+ for veterinary applications) are under
development.
Commercial success with these products based on
well-known chemistry will likely provide an impetus for
the development and commercialization of future pestici-
des based on more exotic essential oils with even greater
potency (e.g. Shaaya and Kostjukovsky, 1998).
6. Conclusions
Certain plant essential oils and/or their constituents
have a broad spectrum of activity against insect and mite
pests, plant pathogenic and other fungi, and nematodes.
As such, they have considerable potential as crop pro-
tectants and for pest management in other situations (e.g.
urban pest control). Current information indicates that
they are safe to the user and the environment, with few
qualications. As a cautionary note, the essential oils that
are most e$cacious against pests are often the most
phytotoxic; this latter property requires serious attention
when formulating products for agricultural and land-
scape use. Also, selectivity among invertebrates is not
well documented. Honeybees appear somewhat suscep-
tible (Lindberg et al., 2000), and the susceptibility of
various natural enemies has yet to be reported, although
the lack of persistence of essential oils under eld condi-
tions could provide some measure of temporal selectivity
favoring these non-target species.
Like other alternative pest management products,
essential oil-based pesticides will not be a panacea for
crop protection, but there should be substantial
market niches, particularly where there is a premium on
worker safety and environmental protection, in which
these types of products will nd wide acceptance among
growers.
Acknowledgements
I thank Drs. David Lindsay and Essam Enan for
reviewing the manuscript. Laurin Hummelbrunner, An-
drew Wan and Emma Gelok provided excellent technical
assistance. Plant essential oil research in my laboratory
has been funded by EcoSMART Technologies Inc.
(Franklin, TN, USA).
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Plant Essential Oils for Pest & Disease Management; Gardening Guidebook for British Columbia

  • 1. * Tel.: #1-604-822-2329; fax: #1-604-822-8640. E-mail address: murray.isman@ubc.ca (M.B. Isman). Crop Protection 19 (2000) 603}608 Plant essential oils for pest and disease management Murray B. Isman* Faculty of Agricultural Sciences, University of British Columbia, Suite 248, 2357 Main Mall, Vancouver, BC, Canada V6T 1Z4 Abstract Certain essential plant oils, widely used as fragrances and #avors in the perfume and food industries, have long been reputed to repel insects. Recent investigations in several countries con"rm that some plant essential oils not only repel insects, but have contact and fumigant insecticidal actions against speci"c pests, and fungicidal actions against some important plant pathogens. As part of an e!ort aimed at the development of reduced-risk pesticides based on plant essential oils, toxic and sublethal e!ects of some essential oil terpenes and phenols have been investigated using the tobacco cutworm (Spodoptera litura) and the green peach aphid (Myzus persicae) as model pest species. In this paper I review (i) the range of biological activities of essential oils and their constituents; (ii) their toxicity and proposed mode-of-action in insects; (iii) their potential health and environmental impacts as crop protectants; and (iv) commercialization of pesticides based on plant essential oils. 2000 Elsevier Science Ltd. All rights reserved. Keywords: Plant essential oils; Natural pesticides; Monoterpenoids 1. Introduction In spite of widespread public concern for long-term health and environmental e!ects of synthetic pesticides, especially in Europe and North America, natural pestici- des, both of microbial and plant origin, have yet to have much impact in the marketplace. Bioinsecticides, domin- ated by Bacillus thuringiensis-based products, and botan- ical insecticides, dominated by pyrethrum-based products, each command little more than 1% of the global insecticide market. However, recent government action in the United States, in the form of the Food Quality Protection Act of 1996, will dramatically restrict the use of many conventional insecticides upon which growers have depended for decades (e.g. organophos- phates and carbamates). In turn, this will create a signi"- cant market opportunity for alternative products, in particular `reduced-riska pesticides which are favored by the Environmental Protection Agency in the USA. Against this backdrop, natural pesticides based on plant-essential oils may represent alternative crop pro- tectants whose time has come. Essential oils, obtained by steam distillation of plant foliage, and even the foliage itself of certain aromatic plants (notably in the families Myrtaceae and Lamiaceae, but in other plant families as well) have traditionally been used to protect stored grain and legumes, and to repel #ying insects in the home. Though some of the claims made for these crude prepara- tions have yet to be substantiated through controlled experiments, scienti"c investigation into the biological activities of these materials proliferated in the past dec- ade. The emerging picture is that certain, speci"c oils and their chemical constituents have demonstrable contact and fumigant toxicity to a number of economically im- portant insect and mite pests, as well as to plant patho- genic fungi. 2. Biological activities of essential oils and their constituents Contact and fumigant insecticidal actions of plant essential oils have been well demonstrated against stored product pests. Among 22 essential oils tested as fumigants against the bean weevil Acanthoscelides obtec- tus (Bruchidae), those of Thymus serpyllum (rich in the phenols thymol and carvacrol) and Origanum majorama (rich in terpinen-4-ol) were the most toxic (Regnault- Roger et al., 1993). In a more detailed study, Shaaya et al. (1991) evaluated the fumigant toxicity of 28 essential oils and 10 of their major constituents against four di!erent 0261-2194/00/$- see front matter 2000 Elsevier Science Ltd. All rights reserved. PII: S 0 2 6 1 - 2 1 9 4 ( 0 0 ) 0 0 0 7 9 - X
  • 2. species of stored product coleopterans. Most interesting- ly, there was little overlap among the insect species with respect to the most toxic oils and constituents, indicating that while these substances are generally active against a broad spectrum of pests, interspeci"c toxicity of indi- vidual oils and compounds is highly idiosyncratic. Sarac and Tunc (1995), investigating the fumigant action of four essential oils to three species of stored product pests, reached the same conclusion. A number of investigations by Ho and colleagues (Ho et al., 1994, 1995, 1997; Huang and Ho, 1998; Huang et al., 1998) have demonstrated contact, fumigant and antifeedant e!ects of a range of essential oil constituents (cinnamaldehyde, -pinene, anethole, extracts of cloves, Syzygium aromaticum, and star anise, Illicium verum) against the red #our beetle Tribolium castaneum and the maize weevil Sitophilus zeamais. Eugenol, the major constituent of oil of cloves and also of the holy basil, Ocimum suave, was shown to be e!ective against these and two additional coleopterans, S. granarius and Prostephanus truncatus (Obeng-Ofori and Reichmuth, 1997). Recent studies have also indicated e$cacy against pests on plants. Essential oils of cumin (Cuminum cyminum), anise (Pimpinella ansium), oregano (Origanum syriacum var. bevanii) and eucalyptus (Eucalyptus camal- dulensis) were e!ective as fumigants against the cotton aphid (Aphis gossypii) and the carmine spider mite (Tet- ranychus cinnabarinus), two greenhouse pests (Tuni and Sahinkaya, 1998). E$cacy of basil (Ocimum spp.) against garden pests has recently been reviewed (Quarles, 1999). Lee et al. (1997) reported on the toxicity of a range of essential oil constituents to the western corn rootworm (Diabrotica virgifera), the two-spotted spider mite (Tet- ranychus urticae) and the house#y (Musca domestica), and dietary e!ects of a number of monoterpenoids against the European corn borer (Ostrinia nubilalis) have been re- cently reported (Lee et al., 1999). There is even evidence that certain essential oils and their constituents are e!ec- tive against Varroa jacobsoni, an ectoparasite of the honey bee (Calderone et al., 1997). However, systematic investigation of the antifungal activities of essential oils and their constituents predate those of the insecticidal properties. Kurita et al. (1981) screened 40 such compounds against seven species of fungi (primarily food spoilage organisms), and Singh et al. (1980) similarly screened "ve essential oils against 22 species of fungi, including both human and plant pathogenic types. More recently, Muller-Riebau et al. (1995) screened nine essential oils against four species of plant pathogenic fungi, whereas Wilson et al. (1997) screened 49 essential oils against the fruit pathogen Botrytis cinerea. In the former study, antifungal activity was strongly associated with monoterpenic phenols, es- pecially thymol, carvacrol and eugenol, in the oils. Some of the essential oils and constituents found to be insecti- cidal (e.g. eugenol) were previously reported to be active against a range of plant pathogenic nematodes (Sangwan et al., 1990), and most recently some essential oils were shown to e!ectively inhibit plant germination, suggesting their potential use as bioherbicides (Dudai et al., 1999). 3. Toxicity to insects The aforementioned studies with insects convincingly demonstrate the fumigant toxicity of essential oils and their constituents. Knockdown activity and lethal toxic- ity via contact has been demonstrated in the American cockroach (Periplaneta americana) (Ngoh et al., 1998), the German cockroach (Blattella germanica) and the house#y (Musca domestica) (Rice and Coats, 1994, Coats et al., 1991). These studies latter point to an obvious neurotoxic site-of-action. Certain essential oil monoterpenes are competitive inhibitors of acetylcholinesterase in vitro (Grundy and Still, 1985; Miyazawa et al., 1997), but this action may not be correlated with toxicity to insects in vivo. A recent investigation by Enan et al. (1998) using the American cockroach points to the octopaminergic ner- vous system as the site-of-action in insects. The binding of H-octopamine in a cockroach nerve cord protein preparation was signicantly a!ected in the presence of a number of essential oil constituents. The lack of octo- pamine receptors in vertebrates likely accounts for the profound mammalian selectivity of essential oils as insec- ticides (i.e. they are toxic to insects but not to mammals), and thus the octopaminergic system of insects represents a biorational target for insect control. Investigation of the formamidine insecticides revealed interesting and po- tentially important sublethal behavioral and physiolo- gical e!ects, presumably mediated by the octopaminergic nervous system (Matsumura and Beeman, 1982). Sub- lethal e!ects observed with some of the essential oil compounds (viz., feeding deterrence, repellency) may be consistant with this mode-of-action. To that end, the apparent correlation between the feeding deterrent e!ect of several monoterpenoids and their topical LD values in the tobacco cutworm (Spodoptera litura) (Noctuidae) is noteworthy (Fig. 1, Is- man, unpublished data). Feeding deterrence was mea- sured in early 5th instar larvae (avg. wt.103 mg) using a cabbage leaf disc choice bioassay (n20) (Bomford and Isman, 1996). Mortality was assessed following topi- cal administration (1 l acetone carrier) to the dorsum of 3rd instar larvae (avg.wt.18 mg; n250). Green peach aphid nymphs (2nd instar) show both behavioral e!ects and toxicity in a laboratory bioassay where aphids are placed on mustard cabbage (`pak choia) leaf discs dipped in emulsions of an essential oil based insecticide (a proprietary mixture of eugenol, thymol and phenethylpropionate as active ingredients; 604 M.B. Isman / Crop Protection 19 (2000) 603}608
  • 3. Fig. 1. Relationship between feeding deterrence and topical toxicity of selected monoterpenes and related phenols to the tobacco cutworm Spodoptera litura. Feeding deterrence determined for leaf discs treated with essential oil compounds at 150 g cm. Fig. 2. Behavioral and toxic e!ects of an essential oil-based insecticide to the green peach aphid Myzus persicae in a laboratory leaf disc bioassay; (a) at 24 h, (b) at 48 h. Error bars represent standard error of the mean (n15}25 replicates with 10 insects per replicate). Fig. 3. Chemical structures of some monoterpenes and related phenols with insecticidal activities. EcoSMART Technologies Inc.) at various concentra- tions (Fig. 2). While 90% of nymphs placed on carrier- treated control leaf discs settled and were actively feeding after 24 h, 50% or fewer aphids fed on treated discs, and the frequency of aphids feeding was inversely concentra- tion-dependent. Interestingly, approximately 20% of the aphids in all treatment groups (except controls) were found walking in the petri dish, o! the leaf discs, after 24 h. Results were even more striking at the 48 h time of observation: at the lowest concentration tested (0.18%), the number of aphids feeding on discs declined from 50% at 24 h to 25%, and the number of dead aphids at this concentration increased from 22 to 60%. Another important aspect of the toxicity of essential oil constituents, seen previously in studies with the intact oils themselves, are interspecic di!erences in susceptibil- ity. Table 1 shows LD or LC values for two closely related monoterpenes ( -terpineol and terpinen-4-ol) and two monoterpenoid phenols (eugenol and carvacrol) (Fig. 3) tested against four species of insects and against the two-spotted spider mite. For the tobacco cutworm, the terpenes and eugenol are comparable in toxicity, whereas carvacrol is at least three times more active; in the case of the house#y, -terpineol is about one-half as active as the other three which are similar in activity. In the fruit #y (Drosophila melanogaster), the terpenes are themselves equipotent, as are the phenols, but the phen- ols are about 3.5 times more active than the terpenes. Eugenol is 7}9 times more toxic than the two terpenes in the western corn rootworm beetle (Diabrotica virgifera virgifera), but in the two-spotted spider mite, terpinen-4- ol is more than twice as active as eugenol, and six times more active than carvacrol. The salient point is that these chemicals and other essential oil constituents can be blended to achieve a desired spectrum of activity and optimal e$cacy against pests. However, investigations of M.B. Isman / Crop Protection 19 (2000) 603}608 605
  • 4. Table 1 Toxicity of selected essential oil monoterpenes and phenols to four species of insect and one species of mite Species (units) LD or LC Eugenol Carvacrol -terpineol Terpinen!4-ol Spodoptera litura ( g larva) 157.6 42.7 141.3 130.4 Drosophila melanogaster ( g cm) 4.6 4.8 17.4 17.7 Musca domestica ( g #y) 77 92 173 79 Diabrotica virgifera ( g beetle) 12 NT 112 90 Tetranychus urticae (ppm) 219 629 NT 96 Application methods: S. litura (3rd instar), D. virgifera (3rd instar), M. domestica (adult) * topical administration to the dorsum using 1 l acetone; D. melanogaster (adult) * residue on inner walls of glass vials; T. urticae (adult) * bean leaves dipped in 5% aqueous acetone solutions. Data for Spodoptera and Drosophila unpublished; for Musca, Diabrotica and Tetranychus from, Lee et al. (1997). Not tested. Table 2 Toxicity of some pesticide active ingredients to juvenile rainbow trout in static water tests (modied from Stroh et al., 1998) Compound or product (% as active ingredient) 96 h LC (ppm) Eugenol (90%) 60.8 Thyme oil (90%) 16.1 -terpineol (90%) 6.6 Emulsier 18.2 Neem (3% azadirachtin) 4.0 Pyrethrum (20% pyrethrins) 0.04 Rotenone (44%) 0.03 Azinphosmethyl (94%) 0.004 Endosulfan (96%) 0.001 Proprietary blend of anionic and nonionic emulsiers. structure-activity relations among these compounds with respect to their toxicity to insects (e.g. Rice and Coats 1994) have not proven especially fruitful as far as predic- ting which compounds will be most e$cacious to any particular type of pest. 4. Health and environmental impacts Perhaps the most attractive aspect of using essential oils and/or their constituents as crop protectants (and in other contexts for pest management) is their favorable mammalian toxicity. Some of the pure essential oil com- pounds are slightly toxic, with rat acute oral LD values of 2}3 g kg (viz. carvacrol, pulegone), but an essential oil insecticide consisting of a proprietary mixture of es- sential oil constituents (EcoSMART Technologies Inc.), resulted in no mortality when fed to rats at 2 g kg (Enan, unpublished data), the upper limit required for acute toxicity tests by most pesticide regulatory agencies including the EPA. in the United States. In that many of the essential oils and their constituents are commonly used as culinary herbs and spices, pesticide products containing certain of these are actually exempt from toxicity data requirements by the EPA. Static water toxicity tests using juvenile rainbow trout (Oncorhynchus mykiss) indicated that based on 96 h-LC values, eugenol is approximately 1500 times less toxic than the botanical insecticide pyrethrum, and 15,000 times less toxic than the organophosphate insecticide azinphosmethyl (Stroh et al., 1998; Table 2). In addition, eugenol and other essential oil constituents are non- persistent in fresh water, based on laboratory tests. These compounds are also non-persistent in soils: under aero- bic conditions at 233C, the half-life for -terpineol ranges from 30}40 h, with complete degradation by 50 h (Misra and Pavlostathis, 1997). Eugenol is completely broken down to common organic acids by soil-borne Pseudomonas bacteria (Rabenhorst, 1996). Concerns for residues of essential oil pesticides on food crops should be mitigated by the growing body of evidence that some essential oil constituents acquired through the diet are actually benexcial to human health (Huang et al., 1994). 5. Commercialization of essential oil-based pesticides In a recent review paper on neem and other botanical insecticides, three barriers to the commercialization of new products of this type were identied: (i) the scarcity of the natural resource; (ii) the need for chemical stan- dardization and quality control; and (iii) di$culties in registration. As the essential oils and their puried con- stituents have a long history of global use by the food and fragrance industries, and most recently in the eld of aromatherapy, many of the oils and/or constituents that are pesticidal are readily available at low to moderate cost in quantity (USD 7}30 kg). A number of constitu- ents are available commercially in reasonable purity (95%), and essential oil producers and suppliers can often provide chemical specications for even the most com- plex oils. Of most importance, some of these materials are exempt from the usual data requirements for registration, 606 M.B. Isman / Crop Protection 19 (2000) 603}608
  • 5. if not exempt from registration altogether (at least in the USA.). Some American companies have recently taken advantage of this situation and have been able to bring essential-oil-based pesticides to market in a far shorter time period than would normally be required for a con- ventional pesticide. Mycotech Corporation produces Cinnamite2+, an aphidicide/miticide/fungicide for glass- house and horticultural crops, and Valero2+, a mitic- ide/fungicide for use in grapes, berry crops, citrus and nuts. Both products are based on cinnamon oil, with cinnamaldehyde (30% in EC formulations) as the active ingredient. With over a dozen registered products by the end of 1999, EcoSMART Technologies is aiming to become a world leader in essential oil-based pesticides. They currently produce aerosol and dust formulations con- taining proprietary mixtures of essential oil compounds, including eugenol and 2-phenethyl propionate aimed at controlling domestic pests (cockroaches, ants, #eas, #ies, wasps, etc.). These are marketed to pest control profes- sionals under the brand name EcoPCO0, with less concentrated formulations for sale to the consumer under the name Bioganic2+. Insecticides and miticides for horticultural crops and for glasshouse and nursery crops will be released shortly. Additional products (e.g. EcoVET2+ for veterinary applications) are under development. Commercial success with these products based on well-known chemistry will likely provide an impetus for the development and commercialization of future pestici- des based on more exotic essential oils with even greater potency (e.g. Shaaya and Kostjukovsky, 1998). 6. Conclusions Certain plant essential oils and/or their constituents have a broad spectrum of activity against insect and mite pests, plant pathogenic and other fungi, and nematodes. As such, they have considerable potential as crop pro- tectants and for pest management in other situations (e.g. urban pest control). Current information indicates that they are safe to the user and the environment, with few qualications. As a cautionary note, the essential oils that are most e$cacious against pests are often the most phytotoxic; this latter property requires serious attention when formulating products for agricultural and land- scape use. Also, selectivity among invertebrates is not well documented. Honeybees appear somewhat suscep- tible (Lindberg et al., 2000), and the susceptibility of various natural enemies has yet to be reported, although the lack of persistence of essential oils under eld condi- tions could provide some measure of temporal selectivity favoring these non-target species. Like other alternative pest management products, essential oil-based pesticides will not be a panacea for crop protection, but there should be substantial market niches, particularly where there is a premium on worker safety and environmental protection, in which these types of products will nd wide acceptance among growers. Acknowledgements I thank Drs. David Lindsay and Essam Enan for reviewing the manuscript. Laurin Hummelbrunner, An- drew Wan and Emma Gelok provided excellent technical assistance. Plant essential oil research in my laboratory has been funded by EcoSMART Technologies Inc. (Franklin, TN, USA). References Bomford, M.K., Isman, M.B., 1996. 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Inhibition of acetylcholinesterases by pulegone-1,2-epoxide. Pestic. Biochem. Physiol. 23, 383}388. Ho, S.H., Cheng, L.P.L., Sim, K.Y., Tan, H.T.W., 1994. Potential of cloves (Syzygium aromaticum [L.] Merr. and Perry) as a grain protectant against Tribolium castaneum (Herbst) and Sitophilus zeamais Motsch. Postharvest Biol. Technol. 4, 179}183. Ho, S.H., Ma, Y., Goh, P.M., Sim, K.Y., 1995. Star anise, Illicium verum Hook F. as a potential grain protectant against Tribolium castaneum (Herbst) and Sitophilus zeamais Motsch. Postharvest Biol. Technol. 6, 341}347. Ho, S.H., Ma, Y., Huang, Y., 1997. Anethole, a potential insecticide from Illicium verum Hook F., against two stored product insects. Int. Pest Control 39 (2), 50}51. Huang, M.-T., Ferraro, T., Ho, C.-T., 1994. Cancer chemoprevention by phytochemicals in fruits and vegetables. Am. Chem. Soc. Symp. Ser. 546, 2}15. Huang, Y., Ho, S.H., 1998. 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  • 6. Lee, S., Tsao, R., Peterson, C.J., Coats, J.R., 1997. Insecticidal activity of monoterpenoids to western corn rootworm (Coleoptera: Chrysomelidae), twospotted spider mite (Acari: Tetranychidae), and house #y (Diptera: Muscidae). J. Econ. Entomol. 90, 883}892. Lee, S., Tsao, R., Coats, J.R., 1999. In#uence of dietary applied mono- terpenes and derivatives on survival and growth of the European corn borer (Lepidoptera: Pyralidae). J. Econ. Entomol. 92, 56}67. Lindberg, C.M., Melathopoulos, A.P., Winston, M.L., 2000. Laborat- ory evaluation of miticides to control Varroa jacobsoni (Acari: Varroidae), a honey bee (Hymentoptera: Apidae) parasite. J. Econ. Entomol. 93, 189}198. Matsumura, F., Beeman, R.W., 1982. Toxic and behavioral e!ects of chlordimeform on the American cockroach Periplaneta americana. In: Coats, J.R. (Ed.), Insecticide Mode of Action. Academic Press, New York, pp. 229}242. Misra, G., Pavlostathis, S.G., 1997. Biodegradation kinetics of monoterpenes in liquid and soil- slurry systems. Appl. Microbiol. Biotechnol. 47, 572}577. Miyazawa, M., Watanabe, H., Kameoka, H., 1997. Inhibition of acetylcholinesterase activity by monoterpenods with a p-menthane skeleton. J. Agric. Food Chem. 45, 677}679. Muller-Riebau, F., Berger, B., Yegen, O., 1995. Chemical composition and fungitoxic properties to phytopathogenic fungi of essential oils of selected aromatic plants growing wild in Turkey. J. Agric. Food Chem. 43, 2262}2266. Ngoh, S.P., Hoo, L., Pang, F.Y., Huang, Y., Kini, M.R., Ho, S.H., 1998. Insecticidal and repellent properties of nine volatile constituents of essential oils against the American cockroach. Periplaneta ameri- cana (L.). Pestic. Sci. 54, 261}268. Obeng-Ofori, D., Reichmuth, Ch., 1997. Bioactivity of eugenol, a major component of essential oil of Ocimum suave (Wild.) against four species of stored-product Coleoptera. Int. J. Pest Manage. 43, 89}94. Quarles, W., 1999. Grow pesto for your pests! Common Sense Pest Control 15(4), 13}19 Rabenhorst, J., 1996. Production of methoxyphenol-type natural aroma chemicals by biotransformation of eugenol with a new Pseudomonas sp. Appl. Microbiol. Biotechnol. 46, 470}474. Regnault-Roger, C., Hamraoui, A., Holeman, M., Theron, E., Pinel, R., 1993. Insecticidal e!ect of essential oils from mediterranean plants upon Acanthoscelides obtecus Say (Coleoptera: Bruchidae), a pest of kidney bean (Phaseolus vulgaris L.). J. Chem. Ecol. 19, 1233}1244. Rice, P.J., Coats, J.R., 1994. Insecticidal properties of monoterpenoid derivatives to the house #y (Diptera: Muscidae) and red #our beetle (Coleoptera: Tenebrionidae). Pestic. Sci. 41, 195}202. Sangwan, N.K., Verma, B.S., Verma, K.K., Dhindsa, K.S., 1990. Nematicidal activity of some essential plant oils. Pestic. Sci. 28, 331}335. Sarac, A., Tunc, I., 1995. Toxicity of essential oil vapours to stored- product insects. Z. P#anzenkr. P#anzenschutz. 102, 69}74. Shaaya, E., Kostjukovsky, M., 1998. E$cacy of phyto-oils as contact insecticides and fumigants for the control of stored-product insects. In: Ishaaya, I., Degheele, D. (Eds.), Insecticides With Novel Modes of Action. Mechanisms and Application. Springer, Berlin, pp. 171}187. Shaaya, E., Ravid, U., Paster, N., Juven, B., Zisman, U., Pissarev, V., 1991. Fumigant toxicity of essential oils against four major stored- product insects. J. Chem. Ecol. 17, 499}504. Singh, A.K., Dikshit, A., Sharma, M.L., Dixit, S.N. 1980. Fungitoxic activity of some essential oils. Econ. Bot. 34, 186}190. Stroh, J., Wan, M.T., Isman, M.B., Moul, D.J., 1998. Evaluation of the acute toxicity to juvenile pacic coho salmon and rainbow trout of some plant essential oils, a formulated product, and the carrier. Bull. Environ. Contam. Toxicol. 60, 923}930. Tuni, I., Sahinkaya, S., 1998. Sensitivity of two greenhouse pests to vapours of essential oils. Entomol. Exp. Appl. 86, 183}187. Wilson, C.L., Solar, J.M., El Ghaouth, A., Wisniewski, M.E., 1997. Rapid evaluation of plant extracts and essential oils for antifungal activity against Botrytis cinerea. Plant Dis. 81, 204}210. 608 M.B. Isman / Crop Protection 19 (2000) 603}608