Bioactivity of Cedarwood Oil and Cedrol Against Arthropod Pests

Abstract

Heartwood samples from Juniperus virginiana L. were extracted with liquid carbon dioxide, and the bioactivity of carbon dioxide-derived cedarwood oil (CWO) toward several species of ants and cedrol toward ticks was determined. Repellency was tested for ants, and toxicity was tested for ticks. Ants in an outdoor bioassay were significantly repelled by the presence of CWO on a pole leading to a sugar-water solution. Similarly, CWO was a significant repellent barrier to red imported fire ants and prevented them from finding a typical food source. Black-legged tick nymphs exhibited dosage-dependent mortality when exposed to cedrol and at the highest dosage (i.e., 6.3 mg/ml) tested, the cedrol killed 100% of the ticks. These repellency and toxicity results together demonstrate a clear potential for the use of CWO as a pest control agent.

Full text

CHEMICAL ECOLOGY
Bioactivity of Cedarwood Oil and Cedrol Against Arthropod Pests
F. J. ELLER,
1,2
R. K. VANDER MEER,
3
R. W. BEHLE,
4
L. B. FLOR-WEILER,
4
AND DEBRA E. PALMQUIST
5
Environ. Entomol. 43(3): 762Ð766 (2014); DOI: http://dx.doi.org/10.1603/EN13270
ABSTRACT Heartwood samples from Juniperus virginiana L. were extracted with liquid carbon
dioxide, and the bioactivity of carbon dioxide-derived cedarwood oil (CWO) toward several species
of ants and cedrol toward ticks was determined. Repellency was tested for ants, and toxicity was tested
for ticks. Ants in an outdoor bioassay were signiÞcantly repelled by the presence of CWO on a pole
leading to a sugarÐwater solution. Similarly, CWO was a signiÞcant repellent barrier to red imported
Þre ants and prevented them from Þnding a typical food source. Black-legged tick nymphs exhibited
dosage-dependent mortality when exposed to cedrol and at the highest dosage (i.e., 6.3 mg/ml) tested,
the cedrol killed 100% of the ticks. These repellency and toxicity results together demonstrate a clear
potential for the use of CWO as a pest control agent.
KEY WORDS cedarwood oil, repellency, toxicity, red imported Þre ant, black-legged tick
Eastern red cedar (Juniperus virginiana L.), western
juniper (Juniperus occidentalis Hook.), and ashe ju-
niper (Juniperus ashei J. Buchholz) (Cupressaceae)
are very abundant conifers in the United States. The
area covered by junipers has been expanding
(Schmidt and Leatherberry 1995, Ganguli et al. 2008),
and all three are often considered pest species because
of their encroachment onto rangeland and pastures
(Adams et al. 1988).
In addition to its aromatic smell, junipers are known
for their resistance to both microbial decay and ter-
mite attack. Because of this resistance, juniper has long
been used for fence posts (Hemmerly 1970, Adams
2004). The antifungal (i.e., wood-rot fungi) activities
of juniper heartwood extracts have recently been re-
ported (Eller et al. 2010, Mun and Prewitt 2011).
Juniper wood has been shown to be resistant to both
Formosan (Morales-Ramos and Rojas 2001) and east-
ern subterranean (Carter and Smythe 1974, Arango et
al. 2006) termites. Particleboard-chip panels made
from eastern red cedar are moderately resistant to
termite damage (Kard et al. 2007), and Ko¨se and Tay-
lor (2012) recently reported heartwood and included
sapwood of eastern red cedar were resistant to ter-
mites.
The wood of eastern red cedar is also known for its
toxicity and repellency to several species of insects
including clothes moths (Huddle and Mills 1952),
ßour beetles (Sighamony et al. 1984), and cockroaches
(Appel and Mack 1989). Eastern red cedar mulch was
also reported to be repellent to ants (Meissner and
Silverman 2001, Thorvilson and Rudd 2001).
However, the bioactivity of eastern red cedar ex-
tracts toward arthropods has not been extensively
studied. Antitermite compounds have been extracted
from eastern red cedar heartwood by organic solvent
(i.e., acetone, pentane, hexane, or methanol) extrac-
tion (Carter and Smythe 1974, Carter 1976, Adams et
al. 1988, McDaniel et al. 1989). An acetoneÐhexaneÐ
water extract of eastern red cedar signiÞcantly re-
duced termite attack when applied to southern pine
by vacuum impregnation (McDaniel and Dunn 1994).
Zhu et al. (2001) found that cedarwood oil (CWO)
repelled termites. Interestingly, cedarwood and its
extracts have also been demonstrated to induce ovi-
position by ladybird beetles (Boldyrev et al. 1969,
Smith et al. 1973).
Our laboratory has been investigating the extraction
and composition of CWO, using supercritical and liq-
uid carbon dioxide as well as pressurized solvents such
as ethanol and hot water (Eller and King 2000, Eller
and Taylor 2004). Carbon dioxide-derived CWO con-
tains higher levels of cedrol and has an odor that more
closely resembles that of eastern red cedar wood than
does CWO obtained by steam distillation (Eller and
King 2000). Carbon dioxide-derived CWO has been
Mention of trade names or commercial products in this article is
solely for the purpose of providing scientiÞc information and does not
imply recommendation or endorsement by the U.S. Department of
Agriculture.
1
Functional Foods Research Unit, National Center for Agricultural
Utilization Research, Agricultural Research Service, United States
Department of Agriculture, 1815 North University St., Peoria, IL
61604.
2
Corresponding author, e-mail: Fred.Eller@ARS.USDA.gov.
3
Imported Fire Ant and Household Insects Research Unit, Center
for Medical, Agricultural, and Veterinary Entomology, Agricultural
Research Service, United States Department of Agriculture, 1600 S.W.
23rd Dr., Gainesville, FL 32608.
4
Crop Bioprotection Research Unit, National Center for Agricul-
tural, Agricultural Research Service, United States Department of
Agriculture, 1815 North University St., Peoria, IL 61604.
5
Agricultural Research Service, United States Department of Ag-
riculture, Midwest Area, 1815 North University St., Peoria, IL 61604.

demonstrated to have antifungal, antitermite and anti-
inßammatory effects (Eller et al. 2010; Tumen et al.
2013a,b). CWO is considered safe and is approved as
a food additive by the U.S. Food and Drug Adminis-
tration (2013).
The purpose of this research was to investigate
potential uses of CWO against several economically
important arthropods as a safe natural pest control
agent. Evaluations included its use as a general ant
repellent on hummingbird feeders, a repellent against
red imported Þre ant, Solenopsis invicta Buren, and
toxicity against black-legged ticks, Ixodes scapularis
Say.
Materials and Methods
CWO Samples. Heartwood samples from eastern
red cedar (Woodford Co., IL) were prepared from
freshly cut trees. Sapwood was removed from the
samples using a band saw, and heartwood sawdust was
prepared using a compound miter saw. Sawdust sam-
ples were held in glass containers at room temperature
before extraction. Extractions were made using liquid
carbon dioxide (25⬚C and 10.3 Mpa), and the CO
2
was
depressurized into glass vials to collect the CWO as
described previously (Eller et al. 2010). (⫹)-Cedrol
was purchased from Aldrich (Milwaukee, WI).
Ant Repellent–Hummingbird Feeder Bioassay.
The experiment was set up as a paired test of untreated
control versus a CWO barrier treatment. The hum-
mingbird feeders (First Nature, Rogers, AR) used in
this study consisted of a large inverted reservoir to
provide a constant level of the sugarÐwater solution
(1:4 by volume). The sugar solution was accessible
through 10 holes in the cover. A plastic hook on the top
of the feeder is used to suspend the feeder. The hum-
mingbird feeders were hung on a 1.63-m-tall black
shepherdÕs hook (Enchanted Garden, Menards, Eau
Claire, WI), and the traps were ⬇1.2 m from the
ground. Twine (⬇1.5 mm in diameter and 30 cm in
length) was wrapped Þve times around the base of the
shepherdÕs hook ⬇15 cm from the ground and tied in
a knot with the excess trimmed off. The concentration
of the CWO in the string was ⬇500 mg/cm
3
. The
control was left untreated while the treated twine had
250
␮
l(⬇200 mg) of neat CWO extract applied to the
twine. The two shepherdÕs hooks were placed 1 m
apart at eight separate locations in Peoria and Wood-
ford counties, IL. The feeders were checked daily for
the presence of ants. When ants were Þrst detected,
that replication was ended and each feeder was placed
in a separate plastic bag and placed in a freezer
(⫺10⬚C) to kill the ants present. The ants were then
removed, counted, and preserved in 70% ethanol. The
ants were identiÞed to genus.
Imported Red Fire Ant Contact Repellency. The
bioassay for contact repellency was similar to that
described by Vander Meer et al. (1996). It was hy-
pothesized that the CWO would act as a close-range
repellent not as a volatile long-range repellent. The
test tray was composed of a porcelain pan measuring
180 by 290 by 50 mm. The upper 3 mm of the pan was
coated with Fluon (BioQuip Products, Rancho
Dominguez, CA) to preclude ants from escaping. A
petri dish nest cell (55 mm in diameter) was placed at
one end of the pan. The petri dish had a 5-mm layer
of Castone dental cement on the bottom that acted as
a moisture reservoir. The lid of the petri dish had a
hole placed in the center to allow ant access. To
protect the bottom of the pan from contamination by
the test materials, 2.5-cm
2
pieces of aluminum foil
were placed in the opposite end of the pan from the
nest cell at each corner ⬇3.0 cm from the sides of the
pan. No food or water was available to the ants during
the bioassay. Fifty microliters of test material was
introduced to the test chamber on a 2.0-cm
2
piece of
Whatman silicone-treated Þlter paper (cat. # 2200
125; Sigma-Aldrich, St. Louis, MO) and was randomly
assigned and placed on one of the aluminum foil
squares. The other aluminum square received a Þlter
paper square with 50
␮
l of pentane as a control. The
solvent was allowed to evaporate to apparent dryness.
Placed on top of each Þlter paper square was a small
wad of cotton soaked in 10% sucrose to serve as a
phagostimulant. Once test materials were in place, ⬇1
g of ants, Solenopsis invicta Buren (Hymenoptera: For-
micidae) (starved for a minimum of 24 h) was placed
in the nest cell and a stopwatch was started. The
number of ants actively feeding on the treatment and
control cotton balls was observed and recorded after
a total of 5 min. The score for each bioassay replicate
was the number of the 5-min values for control and
treatment. Each experiment was replicated three
times, each with a unique monogyne colony and in a
different test tray. CWO at three concentrations (1
and 10% in pentane: wt:vol, and neat) was tested
against pentane controls. Cedrol at 50% (wt:vol in
pentane) was tested against a pentane control.
Black-Legged Tick Contact Toxicity.
Tick Colony. Unfed nymphs (⬇2Ð3 wk since molt-
ing) of the black-legged tick, I. scapularis (Acari: Ix-
odidae), were procured from the Tick Rearing Facil-
ity, National Tick Research and Education Resource,
Department of Entomology and Plant Pathology,
Oklahoma State University, Stillwater, OK. Before tox-
icological bioassays, nymphs were held in four-dram
vials contained in a desiccator with potassium sulfate
solution to maintain high relative humidity (RH;
⬎90%), at room temperature (22Ð24⬚C), with a pho-
toperiod of 16:8 (L:D) h. Nymphs were allowed to
acclimate to our laboratory conditions at least 24 h
before starting the toxicological assay.
Coating of Vials and Bioassays. Different concen-
trations of cedrol were tested on unfed nymphs of I.
scapularis, in laboratory bioassays. Three serial dilu-
tions (10⫻) of cedrol were made with hexane ranging
from 6.3 to 0.063 mg/ml. Coating of vials with cedrol
concentrations in hexane was done following the
method of Panella et al. (2005) with modiÞcations.
Each four-dram size vial (27.25 by 67 mm, Fisher-
brand, Fisher ScientiÞc, Pittsburgh, PA) was coated
evenly on the inside by adding 1 ml of the appropriate
solution of cedrol in hexane. Vials were placed on their
side on a roller (Bellco Biotechnology, Bellco Glass,
June 2014 ELLER ET AL.: BIOACTIVITY OF CEDARWOOD OIL AND CEDROL 763

Inc., Vineland, NJ) and allowed to dry in a fume hood
for 15Ð20 min or until hexane had completely evapo-
rated. There were three replications (i.e., vials) of
each treatment concentration, and three additional
vials were treated with hexane only as a control treat-
ment. The coated vials had only a very thin coating of
oil, which did not appear to impair the movement of
the tick nymphs.
For the bioassay, 10 unfed nymphs were introduced
into each vial and the vials were then capped with a
piece of cotton fabric secured with a rubber band and
Þnally covered with aluminum foil. Vials were placed
in the desiccator with potassium sulfate solution to
maintain high RH (⬎90%), at room temperature (22Ð
24⬚C), with a photoperiod of 16:8 (L:D)h. Thus, 30 tick
nymphs were exposed to each cedrol concentration.
Tick mortality was recorded 24 and 48 h after exposure
to the cedrol-coated vials. Ticks were considered alive
when they exhibited normal behavior, and considered
moribund or dead when they were incapable of move-
ment, failed to maintain normal posture, exhibited
uncoordinated movement, were unable to right them-
selves, or showed no sign of life (motionless).
Statistical Analyses. A sign test was used to test the
probability of obtaining the observed results in the ant
repellentÐhummingbird feeder bioassay, and a one-
way analysis of variance (ANOVA) was used to com-
pare the number of ants at the CWO treatment with
the number of ants at the control after square-root
transformation of the count data plus 1 (Statistix 7.0,
Analytical Software, Tallahassee, FL). A
␹
2
analysis
was used to compare number of red imported Þre ants
at the CWO treatments with the number of red im-
ported Þre ants at the controls. Probit analysis with
logistic distribution was used to analyze probability of
tick mortality based on cedrol concentration (SAS
version 9.3 @ 2002Ð2110 [SAS Institute Inc., Cary,
NC]).
Results and Discussion
Ant Repellent–Hummingbird Feeder Bioassay.
Ants were Þrst detected at the feeders at 2Ð10 d after
placement in the Þeld. Ants were found at the hum-
mingbird feeders at seven of the eight control repli-
cates, whereas no ants were found at the hummingbird
feeders treated with CWO (n⫽8). The Pvalue for this
result was P⫽0.0078 (Sign test; n⫽7). The total
number of ants captured at the controls ranged from
8 to 112, and the mean number of ants found on the
feeders was 30.7 (n⫽8). The ANOVA indicated that
signiÞcantly more ants were captured at the control
feeders than the feeders with the CWO (F
1,14
⫽14.1;
P⫽0.0021). Five genera of ants were identiÞed from
the seven sites and included Camponotus (at two
sites), Formica (at two sites), and Crematogaster (one
site), Lasius (one site), and Tapinoma sessile Say (at
one site). These results indicate that the ants were
much more likely to be found on the untreated sugar
source than the sugar source with the CWO barrier
and this experiment demonstrated 100% exclusion of
ants with CWO without the use of synthetic pesti-
cides.
A CWO-impregnated barrier could be an alterna-
tive to ant deterrent products for hummingbird feed-
ers currently in the market. Commercial products in-
clude “barrier”type products such as AntGuard,
which contains the synthetic insecticide permethrin.
Other types of products are water-Þlled moats (e.g.,
Trap-It), which rely on water, which is subject to
evaporation, to prevent contact with the attractive
source. Because the most abundant component of
CO
2
-derived CWO is cedrol (Eller and King 2000) and
cedrol has a relatively high melting point (i.e., 86Ð
87⬚C; Merck Index, 1989), CWO might be expected to
last over the course of a season outdoors. A CWO-
based ant deterrent could be a natural long-lasting,
inexpensive, safe, and effective means to exclude ants
from otherwise attractive sources, such as humming-
bird feeders as well as other uses in structural pest
control.
Red Imported Fire Ant Contact Repellency. The
results of the red imported Þre ant contact CWO
repellency tests are shown in Fig. 1. At every dosage,
the CWO treatment had signiÞcantly fewer ants on
the food source than did the control. Although there
was not a clear dosageÐresponse of CWO concentra-
tion and repellency, during the 5-min test period, the
100% CWO had a mean (SE) of only 1.3 (0.9) ants on
the food source compared with ⬇40 (6.0) for the
corresponding control (Fig. 1). The major component
of CWO is cedrol (⬇50% of total). When cedrol alone
was tested against a control, a mean (SE) of only 31.2
(2.7) red imported Þre ants were at the cedrol treat-
ment compared with a mean (SE) of 68.8 (2.7) red
imported Þre ants at the control. The cedrol treatment
had signiÞcantly fewer red imported Þre ants than did
the control (P⬍0.0001 using
␹
2
). The 50% cedrol
treatment matches the amount of cedrol in the CWO.
Although 50% cedrol is a signiÞcant red imported Þre
ant repellent, it does not account for all the activity
from the CWO. Other compounds in the CWO that
contribute to CWO repellency against red imported
Þre ants will be the subjects of future investigations.
Essential oils have previously been demonstrated
to be repellent to red imported Þre ants. Mint oil
0
5
10
15
20
25
30
35
40
45
50
1% 10% Neat
Cedarwood Oil
Control
Trea tme nt
Mean Number of Fire Ants
a
a
a
b
b
b
Fig. 1. Effect of CWO on number of Þre ants on food
source. SigniÞcantly more Þre ants were on control than
CWO at all three levels (P⬍0.0001, P⬍0.0007, and P⬍
0.0001, respectively for 1%, 10% and Neat using
␹
2
).
764 ENVIRONMENTAL ENTOMOLOGY Vol. 43, no. 3

(Appel et al. 2004), an essential oil product from
China (Chen 2009), the sesquiterpenes callicarpe-
nal and intermedeol (Chen et al. 2008), and com-
pounds from cloves (Kaße and Shih 2013), have all
been shown to be repellent to red imported Þre ants.
In addition, Anderson et al. (2002) reported a water
suspension from Juniperus wood was repellent to
red imported Þre ants. In this study, the CO
2
-de-
rived CWO from J. virginiana was also repellent to
red imported Þre ants. The potential uses for repel-
ling red imported Þre ants could include exclusion
from homes as well as structures such as electrical
systems.
Black-Legged Tick Mortality. The results of the tick
mortality tests are shown in Table 1. Only 3.3% of the
tick nymphs in the control treatment were dead after
either 24 or 48 h. However, for those exposed to the
cedrol, a high percentage was dead after as little as
24 h. Nymphs exhibited very high mortality (i.e.,
⬎60%) when exposed to cedrol in glass vials after both
24 and 48 h compared with only 3% mortality for those
exposed to controls. Mortality increased with dosage,
and toxic effects were observed sooner in ticks ex-
posed to higher concentrations based on Probit anal-
ysis of the data.
Previously, essential oils have been shown to be
effective against I. scapularis. Flor-Weiler et al. (2011)
reported nootkatone was toxic to I. scapularis, and
Elias et al. (2013) reported a rosemary-based acaricide
was effective against I. scapularis. Chen et al. (2005)
reported that vetiver oil and nootkatone were repel-
lent to both ants and ticks, and Dolan et al. (2009)
suggested the natural products, nootkatone and car-
vacrol, could be alternative control products to con-
ventional synthetic acaricides. Carroll et al. (2011)
reported that the essential oil from Juniperus chinensis
L. was repellent to I. scapularis. Our results demon-
strate that CWO or cedrol from J. virginiana could also
be used as an alternative to conventional synthetic
acaricides for I. scapularis.
The possible uses for CWO in insect management
beyond the species investigated here could be much
broader. In addition to its potential beneÞts in insect
control, the use of CWO would also use an under-
utilized abundant domestic natural resource.
Acknowledgments
The authors thank Allard Cosse, Steven Vaughn, Ray Hol-
loway, Amber Durham, and Karen Ray for their assistance
with conducting Þeld tests; and Michele Hosack and David
Milne for red imported Þre ant technical assistance. The
Þeld-collected ants were identiÞed by Michael W. Gates
(Systematic Entomology Laboratory, Agriculture Research
Service, USDA, Beltsville, MD). Gregory Akerman provided
the eastern red cedar samples.
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0 (control) 3.3c 3.3b
0.063 mg/ml 63.3b 76.7a
0.63 mg/ml 83.3ab 93.3a
6.3 mg/ml 100a 100a
n⫽3 reps of 10 ticks (I. scapularis nymphs) each. Means in a
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Received 23 September 2013; accepted 21 February 2014.
766 ENVIRONMENTAL ENTOMOLOGY Vol. 43, no. 3