Activity of an Essential Oil Derived from Chenopodium

ambrosioides on Greenhouse Insect Pests

Author(s): Raymond A. Cloyd and Helene Chiasson
Source: Journal of Economic Entomology, 100(2):459-466. 2007.
Published By: Entomological Society of America
DOI: http://dx.doi.org/10.1603/0022-0493(2007)100[459:AOAEOD]2.0.CO;2
URL: http://www.bioone.org/doi/
full/10.1603/0022-0493%282007%29100%5B459%3AAOAEOD%5D2.0.CO
%3B2

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 HORTICULTURAL ENTOMOLOGY

Activity of an Essential Oil Derived from Chenopodium ambrosioides

on Greenhouse Insect Pests
RAYMOND A. CLOYD1 AND HELENE CHIASSON2

J. Econ. Entomol. 100(2): 459Ð466 (2007)

ABSTRACT This study involved both greenhouse and laboratory experiments evaluating the effect
of an essential oil product (QRD 400) derived from Chenopodium ambrosioides variety nr. Ambro-
sioides L. (Chenopodiaceae) on greenhouse insect pests that feed on different plant parts: citrus
mealybug, Planococcus citri (Risso); longtailed mealybug, Pseudococcus longispinus (Targioni Toz-
zetti); western ßower thrips, Frankliniella occidentalis (Pergande), and fungus gnats (Bradysia spp.).
Treatments were applied to coleus, Solenostemon scutellarioides plants; transvaal daisy, Gerbera
jamesonii ßowers; or growing medium, depending on the insect pest. The essential oil was most
effective, based on adult emergence, on both the second and third instars of the fungus gnat Bradysia
sp. nr. coprophila when applied as a drench to growing medium. In addition, there was a signiÞcant
rate response for QRD 400 on fungus gnats. The QRD 400 treatment had the highest percentage of
mortality on longtailed mealybug (55%) compared with the other treatments. However, the essential
oil was less effective against citrus mealybug (3% mortality) and western ßower thrips adults (18 Ð34%
mortality) compared with standard insecticides, such as acetamiprid (TriStar) and spinosad (Con-
serve), which are typically used by greenhouse producers. This lack of efÞcacy may be associated with
volatility and short residual properties of the essential oil or with the essential oil taking longer to kill
insect pests. Other insecticides and miticides evaluated, including sesame oil, garlic, parafÞnic oil, and
Bacillus thuringiensis subsp. israelensis, provided minimal control of the designated insect pests. In
addition, adult rove beetle Atheta coriaria Kraatz adults were not effective in controlling the larval
instars of fungus gnats when applied at a rate of Þve adults per container.

KEY WORDS essential oils, pest management, western ßower thrips, fungus gnats, mealybugs

Plants produce compounds to reduce injury from
herbivores. These compounds are secondary plant
metabolites synthesized by plants as a defense
mechanism against phytophagous insects (Hedin
and Hollingworth 1997). Mixtures of these low-mo-
lecular-weight volatiles are referred to as essential oils.
Essential oils are obtained or isolated as a result of
steam distillation from aerial plant parts (Cseke and
Kaufman 1999). Several of these compounds have
both insecticidal and miticidal properties, although
they seem to be more effective against soft-bodied
arthropods (Isman 1999). Moreover, essential oils
have a broad spectrum of insect and mite activity due
to the presence of several modes of action, including
antifeedant activity, inhibition of molting and respi-
ration, reduction in growth and fecundity, cuticle dis-
ruption, and effect on the invertebrate octopamine
pathway (Saxena 1989; Arnason et al. 1993; Isman
1999, 2000; Enan 2001; Akhtar and Isman 2004). In
addition, essential oils are used as insect repellents
(Isman 1999). The advantages of an insecticide or
1 Corresponding author: Department of Entomology, Kansas State
University, Manhattan, KS 66506-4004 (e-mail: rcloyd@ksu.edu).
2 Codena, Inc., Subsidiary of AgraQuest, Inc., Saint-Charles-sur-
Richelieu, Quebec, Canada J0H 2G0.
miticide with several modes of action may include a
delay in resistance development among arthropod pest
populations (Feng and Isman 1995). Essential oils de-
rived from plants also may have minimal direct and/or
indirect effects on natural enemies (Saxena 1989, Is-
man 2000, Bostanian et al. 2005).
The primary method of dealing with arthropod pest
outbreaks in greenhouses is the use of insecticides,
miticides, or a combination product (Parrella 1999).
The need for insecticides and miticides with broad-
spectrum pest activity is important for greenhouse
producers to develop successful and sustainable rota-
tion programs. Essential oils used as insecticides or
miticides typically have a low (⬍12 h) restricted entry
interval (REI), which allows greenhouse producers to
enter treated areas within a short period to conduct
necessary cultural practices such as watering and fer-
tilizing (van Lenteren and Woets 1988). In addition,
essential oils have short residual activity, which re-
duces worker exposure to residues. However, this
short residual activity may result in the need for repeat
applications, which may lead to higher probabilities of
phytotoxicity.
Many studies have demonstrated the efÞcacy of
essential oils derived from rosemary, Rosmarinus of-
ficinalis L.; peppermint, Mentha piperita L.; sweet mar-

0022-0493/07/0459Ð0466$04.00/0 䉷 2007 Entomological Society of America

460 JOURNAL OF ECONOMIC ENTOMOLOGY
joram, Majorana hortensis Moench; basil, Ocimum ba-
silicum L.; mint, Mentha virdis L.; lavender, Lavandula
officinalis Chaix and Lavandula angustifolia Mill; sage,
Salvia fruticosa Mill.; and lemongrass, Cymbopogen
citratus DC. ex Nees against different spider mite spe-
cies in the family Tetranychidae (Mansour et al. 1986;
Amer et al. 1993, 2001; Momen et al. 2001; Refaat et al.
2002; Choi et al. 2004). Tuni and Sahinkaya (1998)
reported success (100% mortality) by using essential
oils including cumin, Cuminum cyminum L.; anise,
Pimpinella anisum L.; and oregano, Origanum syri-
acum variety bevanii Holmes as fumigants for control
of carmine spider mite, Tetranychus cinnabarinus
(Boisduval) (Acari: Tetranychidae) and cotton aphid,
Aphis gossypii Glover (Homoptera: Aphididae) in
greenhouses. In laboratory bioassays, essential oils
were toxic to the green peach aphid, Myzus persicae
(Sulzer) (Homoptera: Aphididae) (Isman 1999). Es-
sential oils derived from spearmint, Mentha spicata L.;
thyme (Thymus spp.), and rosemary, Rosmarinus of-
ficinalis Giron, have been shown to inhibit settling of
the green peach aphid. It was suggested this was due
to the feeding inhibition activity of the essential oils,
although they did not all function similarly. The effect
of the essential oils on aphid mortality was attributed
primarily to starvation and to oral and fumigant tox-
icity (Hori 1999).
The essential oil used in this study was derived from
Chenopodium ambrosioides variety nr. ambrosioides L.
(Chenopodiaceae), a plant species native to Central
and South America. It is also considered an alien weed
species in eastern and mid-North America (Kliks
1985). This essential oil is a sesquiterpene consisting of
a mixture of 14 monoterpenes. It has been demon-
strated to be effective on the twospotted spider mite,
Tetanychus urticae Koch (Acari: Tetranychidae), al-
though this effect is probably due to the synergistic
effects of the constituents (Chiasson et al. 2004a).
Previous studies also have evaluated this essential
oil against the green peach aphid; western ßower
thrips, Frankliniella occidentalis Pergande (Thysan-
optera: Thripidae); and greenhouse whiteßy, Trialeu-
rodes vaporariorum (Westwood) (Homoptera: Aley-
rodidae) (Chiasson et al. 2004b). However, these
assessments were conducted with neem and insecti-
cidal soap, insecticides that may be variable in efÞcacy.
In addition, these are not the primary insecticides used
against these insect pests by greenhouse producers
(R.A.C., unpublished data). It is also important to note
that the major concern with the use of essential oils is
the likelihood of phytotoxicity (Arnason et al. 1993).
Moreover, many essential oils may be phytotoxic to
herbaceous crops grown in greenhouses (Isman
1999).
Despite the previous studies with arthropod pests,
there is relatively minimal, if any, quantitative infor-
mation on the efÞcacy of essential oils on mealybugs,
western ßower thrips, and fungus gnats, which are
major insect pests of greenhouses (Dennis 1978, Ham-
len and Mead 1979, Kole and Hennekam 1990, Lewis
1997). As such, the purpose of this study was to eval-
uate the effectiveness of the essential oil derived from
Vol. 100, no. 2
Table 1. Percentage of mortality of citrus mealybug for all
treatments (five replications per treatment) 5 d after application
Treatmenta Rate (/946 ml) % mortalityb
QRD 400 4.0 ml (AI) 3b
TriStar 0.093 g 68a
Garlic 73.9 ml 3b
Ultra-Fine Oil 9.46 ml 10b
Organocide 14.7 ml 11b
Water control 0b
Untreated check 1b
a
QRD 400 EC (emulsiÞable concentrate at 25% active ingredient
关AI兴, C. ambrosioides var. nr. ambrosioides; Codena), TriStar (AI
acetamiprid 70%; Cleary Chemical Corp., Dayton, NJ), garlic (AIs
98.2% garlic juice, 0.30% potassium sorbate, and 1.5% citric acid; Garlic
GP LTD Co., San Antonio, TX), Ultra-Fine Oil (AI 98.8% parafÞnic
oil; Whitmire Micro-Gen Inc., St. Louis, MO), Organocide (AI 5.0%
sesame oil; Organic Laboratories, Inc., Stuart, FL).
b
Means followed by a common letter are not signiÞcantly different
(P ⫽ 0.05) as determined by Fisher protected LSD test.
C. ambrosioides variety nr. ambrosioides compared
with other insecticides used against these insect pests.
Materials and Methods
A series of experiments were conducted to de-
termine the efÞcacy of the C. ambrosioides variety
nr. ambrosioides-based product QRD 400 (Codena,
Saint-Charles-sur-Richelieu, Quebec, Canada) on
insect pests that feed on different plant parts. The
Þrst two experiments included two mealybug spe-
cies that feed on the aerial portions of plants, citrus
mealybug, Planococcus citri (Risso) (Hemiptera:
Pseudococcidae), and longtailed mealybug, Pseudo-
coccus longispinus (Targioni Tozzetti) (Hemiptera:
Pseudococcidae). The third experiment involved west-
ern ßower thrips adults, which primarily feed in ßower
buds or open ßowers; and the fourth experiment was
with fungus gnat Bradysia sp. nr. coprophila Lintner
(Diptera: Sciaridae) larvae, which inhabit the growing
medium feeding on plant roots.
Experiment 1: Citrus Mealybug. Thirty-Þve green
coleus, Solenostemon scutellarioides (L.) Codd, plants
were started from cuttings taken from stock plants and
transplanted into 15.2-cm-diameter containers (Kord
Products; Toronto, Ontario, Canada) in a growing
medium consisting of 50% composted pine bark, 20%
Canadian sphagnum peat moss, 20% medium coarse
vermiculite, 10% perlite, a starter nutrient charge, and
wetting agent (SunGro Sunshine Universal SB300 Mix;
Strong-Lite Horticultural Products, Pine Bluff, AR).
Plants were fertilized with 20.0 Ð 8.3Ð 8.8 (NÐPÐK) at
250 ppm nitrogen in a constant liquid feed program.
Plants were grown in a glass greenhouse on wire-mesh
raised benches and arranged in a completely random-
ized design. There were seven treatments with Þve
replications per treatment. The treatments and rates
are presented in Table 1.
Plants were ⬇15.0 cm in height when they were
artiÞcially infested with 20 s and late third instars of
citrus mealybug. After 24 h, all plants were sprayed
with the appropriate treatments by using a 946-ml
plastic spray bottle. Individual plants were sprayed to
April 2007 CLOYD AND CHIASSON: EFFECT OF ESSENTIAL OIL ON INSECT PESTS
Table 2. Percentage of mortality of longtailed mealybug for all
treatments (five replications per treatment) 4 d after application
Treatmenta Rate (/946 ml) % mortalityb
QRD 400 RTU 55a
Garlic 73.9 ml 18cd
Ultra-Fine Oil 9.46 ml 23c
Celero 0.21 g 38b
Water control 7de
Untreated check 0e
a
QRD 400 RTU (Ready-To-Use at 0.5% AI) (AI C. ambrosioides var.
nr. ambrosioides; Codena), Celero (AI 16.0% clothianidin; Arysta
LifeScience Corp., San Francisco, CA). Refer to Table 1 for infor-
mation on Garlic and Ultra-Fine Oil.
b b
Means followed by a common letter are not signiÞcantly different
(P ⫽ 0.05) as determined by Fisher protected LSD test.
runoff with 35 ml of spray solution. Deionized water
was used for all treatment applications. Greenhouse
temperatures during the experiment ranged from 21 to
24⬚C with a relative humidity between 60 and 70%.
The test plants received natural lighting for the du-
ration of the experiment. Plants were watered using a
hand-held water breaker. No overhead irrigation was
performed. Coleus plants were harvested and the
number of live, dead, and total number of citrus mea-
lybugs were counted for each plant (⫽replicate) 5 d
after application.
Experiment 2: Longtailed Mealybug. The initial
procedures implemented in this experiment were sim-
ilar to the previous experiment, except that 30 red
coleus, Solenostemon scutellarioides (L.) Codd, plants
were used. There were a total of six treatments with
Þve replications per treatment. The treatments and
rates are presented in Table 2.
Plants were ⬇25.0 cm in height when they were
artiÞcially infested with 15Ð20 early to late second
instars of longtailed mealybug. Treatment application
procedures and greenhouse environmental conditions
were the same as in the citrus mealybug experiment
(described above). Plants were harvested, and the
number of live, dead, and total number of longtailed
mealybugs were counted for each plant (⫽replicate)
4 d after application.
Experiment 3: Western Flower Thrips. Thirty-Þve
cut transvaal daisy, Gerbera jamesonii (H. Bolus ex.
Hook f), ßowers of various colors were obtained from
a wholesale broker (Bill Doran Wholesale Florists,
Bloomington, IL). No pesticides had been applied to
the cut ßowers 2 wk before harvest from the broker,
so the possibility of any pesticide residues negatively
affecting western ßower thrips survival in this exper-
iment was minimal. Flower stems were excised 7.6 Ð
10.1 cm below the base of the ßowers or sepals and
placed into 22.0-mm borosilicate glass vials (Research
Products International Corp., Mt. Prospect, IL) con-
taining ßoral preservative (1.32 g per 0.946 liters [1 tsp
per quart]; Floralife, Walterboro, SC), which were
inserted into 10.1-cm-diameter standard plastic con-
tainers Þlled with SunGro Sunshine Universal SB300
Mix growing medium. The growing medium held the
glass vial containing ßoral preservative and the cut
ßower upright during the experiment. Each ßower
461
Table 3. Percentage of mortality of western flower thrips for
all treatments (five replications per treatment) 3 d after application
Treatmenta Rate (/946 ml) % mortalityb
QRD 400 EC 11.3 ml 18cd
QRD 400 EC 18.9 ml 34bc
Overture 0.56 g 49b
Overture 1.13 g 37bc
Conserve 0.81 ml 97a
Water control 0d
Untreated check 6d
a
QRD 400 EC (emulsiÞable concentrate at 25% AI; C. ambrosioides
var. nr. ambrosioides; Codena), Overture (AI 35% pyridalyl; Valent
USA Corp.), Conserve (AI 11.6% spinosad; Dow AgroSciences).
Means followed by a common letter are not signiÞcantly different
(P ⫽ 0.05) as determined by Fisher LSD test.
was artiÞcially infested with ⬇15 adult western ßower
thrips, obtained from a greenhouse colony, by using a
soft-bristled camelÕs-hair brush. All plastic containers
with the cut ßowers were placed on two wire-meshed
raised benches in a glass greenhouse and arranged in
a completely randomized design. There were seven
treatments with Þve replications per treatment. The
treatments and rates are presented in Table 3.
All ßowers were sprayed, after 24 h, with the ap-
propriate treatments by using a 946-ml plastic spray
bottle. Individual ßowers were sprayed to runoff with
⬇25 ml of spray solution. This spray volume thor-
oughly saturated the ßower surface and allowed the
spray solution to penetrate into the disk portion of
the ßowers. The glass vials were reÞlled regularly with
ßoral preservative to ensure lasting quality of the cut
ßowers. The temperature inside the greenhouse dur-
ing the experiment was 21Ð26⬚C with a relative hu-
midity between 60 and 70%. Flowers were harvested
three d after application, placed into petri dishes with
lids, and then emasculated under laboratory condi-
tions. The numbers of live, dead, and total number of
western ßower thrips adults were counted.
Experiment 4: Fungus Gnat. This experiment con-
sisted of nine treatments (Table 4) with Þve replica-
tions per treatment per fungus gnat instar (second and
third) for a total of 90 samples. Forty-Þve samples of
growing medium (Universal SB300 Mix; SunGro Hor-
ticulture, Pine Bluff, AZ) were inoculated with second
instars of Bradysia sp. nr. coprophila, and 45 samples
were inoculated with third instars. Adult emergence
was assessed using a 2.5- by 2.5-cm yellow sticky card
(Whitmire Micro-Gen; St. Louis, MO). The experi-
ment was set up as a completely randomized design.
Fungus gnat larvae to be used in this experiment
were reared to a known age by using the following
procedure. A standard glass petri dish (100 by 20-mm)
was lined with Whatman no. 1 Þlter paper (90 mm)
and moistened with deionized water. The petri dish
was Þlled with a mixture of sterilized Universal SB300
Mix consisting of pine bark compost, Canadian sphag-
num peat, horticultural vermiculite, perlite, and a wet-
ting agent, and pureed potatoes at a ratio of 1:1/8
(0.125). Approximately 1.06 g (0.5 tsp) of fresh oat-
meal was distributed onto the surface, and then the
growing medium was moistened with 75 ml of deion-
462 JOURNAL OF ECONOMIC ENTOMOLOGY
Table 4. Mean ⴞ SE adult Bradysia sp. nr. coprophila emer-
gence based on yellow sticky card (2.5 by 2.5 cm) countsa from
growing medium samples initially inoculated with either 20 second
or third instars per replicate for all treatments
Second Third
Treatmentb Rate (/60 ml)
instar instar
QRD 400 0.3 ml 9.0 ⫾ 0.9bcc 10.2 ⫾ 1.6b
QRD 400 0.6 ml 5.0 ⫾ 1.1d 4.6 ⫾ 1.8c
QRD 400 1.0 ml 1.2 ⫾ 0.7e 1.0 ⫾ 0.5d
Garlic 9.3 ml 11.6 ⫾ 0.7b 14.8 ⫾ 1.1a
Gnatrol 0.6 ml 14.6 ⫾ 1.0a 15.6 ⫾ 1.4a
Ornazin 0.037 ml 8.6 ⫾ 1.4c 9.6 ⫾ 0.7b
Pylon 0.032 ml 0.0 ⫾ 0.0e 0.2 ⫾ 0.2d
A. coriaria 5 adults/container 15.0 ⫾ 1.0a 15.6 ⫾ 1.0a
Water control 14.8 ⫾ 0.8a 14.4 ⫾ 1.2a
a
Sticky cards were counted after 20 d for both second and third
instars after application of all treatments. There were Þve replications
per treatment.
b
QRD 400 (microemulsion at 50% AI used for soil application; C.
ambrosioides var. nr. ambrosioides; Codena), Garlic (AI 98.2% garlic
juice, 0.30% potassium sorbate, and 1.5% citric acid; Garlic GP LTD
Co.), Gnatrol (AI Bti 6.38%; Valent USA Corp.), Ornazin (AI 3.0%
azadirachtin; SePro Corp., Carmel, IN), Pylon (AI 21.4% chlorfena-
pyr; OHP, Inc., Mainland, PA), A. coriaria (University of Illinois,
Urbana, IL).
c
Means followed by a common letter are not signiÞcantly different
(P ⫽ 0.05) as determined by Fisher protected LSD test.
ized water by using a 946-ml spray bottle. The petri
dish was enclosed in a 739-ml container retroÞtted
with ventilation holes. Approximately 30 Ð 40 fungus
gnat adults (mixture of female and male) were col-
lected from a laboratory colony (Cabrera et al. 2005)
into a 9-dram plastic vial, secured with a lid, and then
the vial (with the lid removed) was enclosed inside a
container, which was then placed into an environmen-
tal growth chamber (Sherer Environmental Chamber
model CEL-36-10, Warren/Sherer Division of Kysor
Industrial Corp., Marshall, MI) set at 24 ⫾ 2⬚C. The
petri dish (with the lid removed) remained in the
chamber for 48 h to allow the females to mate, and
then lay eggs. After 48 h, the petri dish was removed
from the container, and 4.0 ml of deionized water was
applied to the growing medium surface. A glass lid was
placed on the petri dish, which was then returned to
the growth chamber. The petri dish was checked daily,
and 2.0 ml of deionized water was applied to the
surface to prevent the growing medium from drying
out. Under the environmental conditions of the
growth chamber, fungus gnat larvae were second in-
stars after 6 d and third instars after 10 d.
The petri dish surface was carefully evaluated under
a dissecting microscope to assess the fungus gnat larval
population. Using a laboratory spoon, we removed a
small sample of growing medium (1.32Ð3.33 g or 0.25Ð
0.5 tsp) containing larvae from the original petri dish
and placed the sample into another glass petri dish
(100 by 20 mm). The sample was carefully rinsed with
deionized water, and then the petri dish was Þlled
with water. The petri dish was examined under a
dissecting microscope, and any ßoating larvae were
collected using a micropipette. The larvae were placed
into a small glass petri dish (60 by 15 mm) and covered
with deionized water. The larvae remained in the
Vol. 100, no. 2
water for up to 30 min or until they were applied to the
growing medium samples. Before inoculating the
growing medium samples, the second and third instars
were counted again by using a dissecting microscope
with a grid placed underneath the petri dish.
Growing medium used for the samples was steril-
ized for 10 min in a microwave oven (1,200-W output).
The percentage of moisture content of the sterilized
growing medium, which was determined gravimetri-
cally before conducting the experiment, was 48%.
Each sample consisted of 300 ml of sterilized growing
medium moistened with 75 ml of deionized water, and
amended with 1.06 g (0.5 tsp) of oatmeal. The growing
medium was measured into 250- and 50-ml glass bea-
kers and leveled off. The sample was placed into a
473-ml polypropylene deli container (Fabri-Kal Corp.,
Kalamazoo, MI) and lightly compressed. A lid, retro-
Þtted with thrips screening (0.02 by 0.08 cm) for
ventilation, was placed on the container. The samples
were placed inside the growth chamber for 48 h to
allow for natural fungal growth before inoculation
with larvae. Six-day-old second and 10-d-old third
instars were applied to the samples of growing me-
dium. Twenty larvae (second or third instars, depend-
ing on the sample) from the petri dish (described
above) were poured onto each sample, and then the
petri dish was rinsed with deionized water to ensure
that all larvae had been placed into the sample. The
inoculated samples were then returned to the growth
chamber for 24 h to allow the larvae to migrate
throughout the growing medium proÞle. After 24 h,
the treatments were applied to the samples with Þve
replications per treatment, and then the samples were
returned to the growth chamber. The treatments and
rates are presented in Table 4.
A yellow sticky card (2.5 by 2.5 cm) was attached to
the underside of the lid of each deli squat container
to assess adult fungus gnat emergence. Seventy-two
hours after applying the treatments, 4.0 ml of deion-
ized water was added through the lid of each deli squat
container. The samples were moistened with 60 ml of
deionized water 1 wk after the treatments had been
applied. The watering regime for the deli squat con-
tainers in the growth chamber for the remainder of the
experiment consisted of adding 4.0 ml of deionized
water to the surface of the growing medium through
the lid of each deli squat container once per week and
60 ml of deionized water applied once per week into
tubs located underneath the base of the deli squat
containers.
Rove beetle Atheta coriaria Kraatz (Coleoptera:
Staphylinidae) adults were obtained from a laborato-
ry-reared colony by placing a sample of growing me-
dium (1,034 g) from the colony into a glass petri dish
(100 by 20 mm). The contents were then positioned
into a 180-␮m sieve. Adults were aspirated into a
9-dram vial, which was covered with a lid. Rove beetle
adults were placed on the surface of the growing
medium in the deli squat containers. The deli squat
containers with rove beetle adults were all located in
plastic tubs (7.8 liter). To prevent the adults from
being captured initially on the yellow sticky cards, the
April 2007 CLOYD AND CHIASSON: EFFECT OF ESSENTIAL OIL ON INSECT PESTS
sticky card cover was not removed until 5 d after
applying the fungus gnat larvae. Fungus gnat adult
counts on the yellow sticky cards as well as the number
of adults that were ßying within the sample container
were recorded after 20 d.
Statistical Analysis. Percentage of mortality for each
treatment was calculated by dividing the number of
dead citrus mealybugs, longtailed mealybugs, or west-
ern ßower thrips by the total number of each pest
recovered per plant or ßower (⫽replicate). Percent-
age of mortality values were then normalized by arc-
sine square-root transformation and subject to a one-
way analysis of variance (ANOVA) with treatment as
the main effect (SAS Institute 2002). SigniÞcant treat-
ment means were separated using a Fisher protected
least signiÞcant difference (LSD) test at P ⱕ 0.05
(SAS Institute 2002). All data presented are non-
transformed.
All data for the fungus gnat experiment was ana-
lyzed using a one-way ANOVA with treatment as the
main effect (SAS Institute 2002). Treatment means for
the number of fungus gnat adults recovered from both
second and third instar samples were separated using
a Fisher protected LSD test at P ⱕ 0.05 (SAS Institute
2002).
Results
Experiment 1: Citrus Mealybug. Percentage of mor-
tality was signiÞcant (F ⫽ 29.79; df ⫽ 6, 34; P ⬍ 0.0001).
The acetamprid (TriStar; Cleary Chemical Corp.,
Dayton, NJ) treatment was the only treatment that
resulted in ⬎50% mortality of citrus mealybug 5 d after
application (Table 1). However, it should be noted
that we inadvertently used 0.25 the recommended
application rate of QRD 400.
Experiment 2: Longtailed Mealybug. Percentage of
mortality was signiÞcant (F ⫽ 32.07; df ⫽ 5, 29; P ⬍
0.0001). QRD 400 RTU (Ready-To-Use) was the only
treatment that resulted in ⬎50% mortality of long-
tailed mealybug 4 d after application (Table 2).
Experiment 3: Western Flower Thrips. Among the
treatments, percentage of mortality was signiÞcant
(F ⫽ 34.62; df ⫽ 6, 34; P ⬍ 0.0001). However, none of
the treatments were effective, based on adult western
ßower thrips mortality, with the exception of spinosad
(Conserve; Dow AgroSciences, Indianapolis, IN),
which had the highest mortality rate (97%) and was
signiÞcantly different from the other treatments (Ta-
ble 3).
Experiment 4: Fungus Gnat. Treatment was signif-
icant for the number of fungus gnat adults recovered
(based on yellow sticky card counts) from samples
inoculated with second instars (F ⫽ 36.17; df ⫽ 8, 44;
P ⬍ 0.0001) and third instars (F ⫽ 26.36; df ⫽ 8, 44; P ⬍
0.0001). The chlorfenapyr (Pylon; OHP, Inc., Main-
land, PA), high rate (1.0 ml/60 ml) of QRD 400, and
medium rate (0.6 ml/60 ml) of QRD 400 treatments
resulted in signiÞcantly fewer fungus gnat adults re-
covered on sticky cards than the other treatments for
the samples inoculated with second instars (Table 4).
Similarly, the chlorfenapyr (Pylon), high rate (1.0
463
ml/60 ml) of QRD 400, and medium rate (0.6 ml/60
ml) of QRD 400 treatments resulted in signiÞcantly
fewer fungus gnat adults recovered on sticky cards
than the other treatments for the samples inoculated
with third instars (Table 4).
Discussion
In this study, the essential oil product QRD 400
derived from C. ambrosioides variety nr. ambrosioides
was active on both the second and third instars of the
fungus gnat Bradysia sp. nr. coprophila. In addition,
there was a signiÞcant rate response (Table 4). Es-
sential oils have been shown to have nematicidal prop-
erties (Sangwan et al. 1990), indicating that they pos-
sess residual activity in growing medium. Additionally,
incorporation into growing medium may protect the
essential oil from photodegradation and decrease vol-
atility. Rice and Coats (1994) tested seven monoter-
penoids to determine their efÞcacy against the third
stage instar of the southern corn rootworm, Diabrotica
undecimpunctata howardii Barber (Coleoptera: Chry-
somelidae) and found that although the monoterpe-
noids were toxic to the larvae, the standard, chlorpyr-
ifos was 10 times more lethal than verbenone, the most
active monoterpenoid. Similarly, Lee et al. (1997)
reported that several monoterpenoids exhibited some
level of activity against the western corn rootworm,
Diabrotica virgifera virgifera LeConte larvae in both
laboratory and greenhouse tests with perillaldehyde
and ␣-terpineol the most toxic. However, the stan-
dards, carbofuran and chlorpyrifos were 3 times more
active than the most effective monoterpenoids. In our
study, the high rate (1.0 ml/60 ml) of QRD 400 was not
signiÞcantly different from chlorfenapyr (Pylon),
which was the most efÞcacious insecticide overall
against both fungus gnat instars (Table 4). In addition,
the high rate of QRD 400 was comparable, in terms of
efÞcacy, with the insect growth regulators typically
used by greenhouse producers for control of fungus
gnats (R.A.C., unpublished data). All three rates of
QRD 400 also were more toxic to the second and third
instars than Gnatrol (Valent USA Corp., Walnut
Creek, CA) (Table 4), which contains the active in-
gredient Bacillus thuringiensis subsp. israelensis (Bti).
This microbial insecticide is derived from a soilborne
bacterium and is used in commercial greenhouse pro-
duction systems strictly for the control of fungus gnat
larvae in vegetables, herbs, and bedding plants (Wein-
zierl and Cloyd 2004). However, Bti seems to be less
effective on the second and third instars of fungus
gnats (Cloyd and Dickinson 2006).
Although QRD 400 provided better control of long-
tailed mealybug, based on percentage of mortality,
than the other treatments; mortality was only 55%
(Table 2). QRD 400 was no better than the check and
water control in controlling citrus mealybug and west-
ern ßower thrips, with the exception of the high rate
(18.9 ml/946 ml) of QRD 400 in the western ßower
thrips experiment, which was signiÞcantly different
from the check and water control (Table 3). The
reason why QRD 400 was less active on both mealybug
464 JOURNAL OF ECONOMIC ENTOMOLOGY
species is likely due to the waxy-coating present on the
body, which tends to protect mealybugs from insec-
ticide applications (Copland et al. 1985). Holling-
sworth (2005) reported that the citrus extract, li-
monene, at a rate of 1%, failed to control the third and
fourth instars of P. citri (⬍45% mortality). Similar to
our study, this was likely due to the protective waxy
coating of the mealybug, particularly in later instars.
However, using 0.25 the recommended label rate also
may have inßuenced efÞcacy of the essential oil. Es-
sential oils, in general, tend to be volatile and are
subject to photodegradation in addition to being less
persistent than synthetically derived insecticides
(Misra et al. 1996). This may reduce the efÞcacy of
essential oils when used to control insect pests feeding
on aboveground plant parts, which may explain why
QRD 400 was less effective against western ßower
thrips compared with the standard, spinosad (Con-
serve), which tends to kill insects rapidly. However, it
is possible that the 3- to 5-d assessment periods were
too early to evaluate efÞcacy as preliminary data seem
to suggest that evaluations 7Ð10 d after treatment are
more indicative of the products performance (H.C.,
unpublished data). Additionally, the formulation of
the product also may determine effectiveness for in-
sect control. In general, essential oils exhibit variabil-
ity in providing control of western ßower thrips. For
example, extracts from R. officinalis and other essential
oils tested had no signiÞcant effect on the response of
western ßower thrips (Katerinopoulos et al. 2005),
whereas the commercial essential oil, neroly speca,
seems to be active on western ßower thrips when
feeding on greenhouse cucumbers, Cucumis sativus L.
(Roditakis et al. 2002). Because western ßower thrips
adults tend to reside in ßowers, when plants are in
bloom (Yudin et al. 1987, Terry 1997), essential oils
must not only demonstrate efÞcacy against western
ßower thrips but also they cannot harm open ßowers.
The primary concern with using essential oils in
greenhouses is the risk of phytotoxicity. Essential oils
have been shown to be harmful to vegetables and
herbaceous plant material grown in greenhouses (Is-
man 1999, Ibrahim et al. 2001). Hollingsworth (2005)
indicated that a 1% rate of limonene was phytotoxic to
LauaÕe fern, Phymatosorus scolopendria (Burm. f.) Pic.
Serm; red ginger, Alpina purpurate (Vieill.) K. Schum;
and green dracaena, Dracaena deremensis Engl. ÔWar-
neckiiÕ, whereas the essential oil was less harmful to
plants with thick, waxy leaves such as sago palm, Cycas
revoluta Thunb.; areca palm, Chrysalidocarpus lute-
scens (Bory) H. Wendl.; and ßamingo lily, Anthurium
andraeanum Linden. That essential oils are phytotoxic
limits their use in greenhouses; however, if they could
be formulated in a manner that lowers the risk of
phytotoxicity, then greenhouse producers would
likely use them. One option is microencapsulation,
which involves incorporating the insecticide particles
into minute polymeric spheres (15Ð50 ␮m in diame-
ter) or surrounding the particles with a plastic coating.
After an application, the active ingredient is slowly
released as the plastic coating dissolves or breaks
down. Formulating essential oils, as microencapsules,
Vol. 100, no. 2
may reduce phytotoxicity to sensitive plants (Marer
1988, Ware and Whitacre 2004).
We tested a number of short- and long-term residual
insecticides, and it was apparent that the short-term
insecticides including sesame oil, garlic, parafÞnic oil,
and Bacilllus thuringiensis subsp. israelensis were
minimally effective on the designated insect pests,
whereas the long-term residual insecticides such as
acetamiprid (TriStar), chlorfenapyr (Pylon), and spi-
nosad (Conserve) were more effective on the target
insect pests (Tables 1, 2, and 4). It should be noted that
both sesame oil and garlic are considered essential oils
(Boyd and Alverson 2000, Rahman and Talukder
2006), but similar to QRD 400, failed to provide control
of mealybugs and fungus gnats (Tables 1, 2, and 4).
The rove beetle, A. coriaria adult did not seem to
control fungus gnat larvae (Table 4), although the rate
used (Þve rove beetle adults per container) may have
been to low; however, the release rate recommended
by Biobest Biological Systems (Ilse Velden 18, B-2260
Westerlo, Belgium) is two rove beetle adults per
square meter. Nonetheless, there is no quantitative
data to assess the rate of rove beetles that will effec-
tively control fungus gnat larvae.
In this study, we have demonstrated that the essen-
tial oil product QRD 400, which is derived from C.
ambrosioides variety nr. ambrosioides, is more efÞca-
cious on insects that inhabit the growing medium, e.g.,
fungus gnat larvae, than insects such as citrus and
longtailed mealybug and western ßower thrips, which
feed on either the vegetative or ßoral parts of plants.
However, the essential oil may take longer to kill
mealybugs and western ßower thrips than standard
products, which means that evaluations for efÞcacy
need to be conducted 7Ð10 d after application.
Acknowledgments
We thank Amy Dickinson for providing technical, support
particularly for the fungus gnat experiment. We also want to
thank Eli Levine (Center for Ecological Entomology, Cham-
paign, IL) for valuable contribution in critically reviewing
the manuscript.
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