Exp Appl Acarol (2016) 68:241–249

DOI 10.1007/s10493-015-9994-0

Evaluation of DEET and eight essential oils

for repellency against nymphs of the lone star tick,
Amblyomma americanum (Acari: Ixodidae)

Hao Meng1,2 • Andrew Y. Li1 • Livio M. Costa Junior3 •

Ivan Castro-Arellano4 • Jingze Liu2

Received: 30 September 2015 / Accepted: 5 November 2015 / Published online: 21 November 2015
Ó Springer International Publishing Switzerland (outside the USA) 2015

Abstract DEET and Eight commercially available essential oils (oregano, clove, thyme,
vetiver, sandalwood, cinnamon, cedarwood, and peppermint) were evaluated for repellency
against host-seeking nymphs of the lone star tick, Amblyomma americanum. Concentra-
tion-repellency response was established using the vertical paper bioassay technique for
each essential oil and compared with that of N,N-diethyl-3-methyl benzamide (DEET), a
standard repellent compound present in many commercial repellent formulations. The
effective concentration of DEET that repels 50 % of ticks (EC50) was estimated at
0.02 mg/cm2, while EC50s of the essential oils fall between 0.113 and 0.297 mg/cm2.
Based on EC50 estimates, oregano essential oil was the most effective among all essential
oils tested, followed by clove, thyme, vetiver, sandalwood, cinnamon, cedarwood, and
peppermint oils. None of the tested essential oils demonstrated a level of tick repellency
found with DEET. Results from this study illustrated the challenge in search for more
effective natural tick repellents.

Keywords Repellent
Essential oil
Lone star tick
Amblyomma americanum

This article reports the results of research only. Mention of a proprietary product does not constitute an
endorsement or a recommendation by the USDA for its use. The USDA is an equal opportunity provider and
employer.

& Andrew Y. Li
Andrew.Li@ars.usda.gov
1
USDA, ARS, Invasive Insect Biocontrol and Behavior Laboratory, 10300 Baltimore Avenue,
Beltsville, MD 20705, USA
2
College of Life Sciences, Hebei Normal University, No 20, Road E. 2nd Ring South,
Shijiazhuang 050024, Hebei, China
3
Biological and Health Science Center, Federal University of Maranhão, Av. dos portugueses, 1966,
Cidade Universitária do Bacanga, São Luı́s, MA CEP 65080-805, Brazil
4
Department of Biology, Texas State University, 601 University Drive, San Marcos, TX 78666,
USA

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Introduction

Ticks are vectors of viruses, bacteria, and protozoa that cause serious diseases affecting human
and animal health (Parola and Raoult 2001; Jongejan and Uilenberg 2004; Perez de León et al.
2014; Sonenshine and Roe 2014). The most commonly reported vector-borne diseases in the
USA are transmitted by ticks. Lyme disease and other tick-borne diseases can be attributed
largely to three species of ticks, the blacklegged tick Ixodes scapularis Say, the lone star tick
Amblyomma americanum (L.), and the American dog tick Dermacentor variabilis (Say) (Acari:
Ixodidae). In the past decade there has been a substantial increase of Lyme disease cases, which
is caused by the spirochete Borrelia burgdorferi and transmitted by the blacklegged tick (Gratz
1999; CDC 2004, 2013). Over 30,000 cases of Lyme disease have been reported annually to the
Centers for Disease Control and Prevention, although a more recent study put the number of
annual cases at 300,000, 10 times higher than previous estimates (Mead et al. 2013).
The lone star tick, A. americanum, is an aggressive tick that uses humans, domestic
animals, and wildlife as hosts during all postembryonic stages (Merten and Durden 2000;
Childs and Paddock 2003; Schulze et al. 2005; Springer et al. 2014). This tick is widely
distributed in the USA, and increases in distribution range and population density have
been observed in the Northeastern and Midwestern regions (Ginsberg et al. 1991; Means
and White 1997; Springer et al. 2014; Barrett et al. 2015). A. americanum is one of most
common tick species found in the Southern and Eastern USA and transmits pathogens that
cause a number of human and animal diseases (Childs and Paddock 2003; Schulze et al.
2005; Goddard and Varela-Stokes 2009).
Use of chemical acaricides, such as area- and host-targeted applications and baits, is
important in control of ticks, including the blacklegged tick and the lone star tick (Piesman
and Eisen 2008). Host-targeted acaricides intended for rodents (Dolan et al. 2004; Mather
et al. 1987) and deer (Carroll et al. 2003, 2009; Pound et al. 2009) have achieved varying
degrees of control. N,N-diethyl-meta-toluamide (DEET) and permethrin (a synthetic
pyrethroid insecticide) currently serve as the primary chemical protective measures against
ticks affecting humans (Bissinger and Roe 2010; Vaughn and Meshnick 2011; Cisak et al.
2012). A number of plant-derived natural products also have been reported to kill or repel
ticks, including the lone star tick (Jaenson et al. 2005; Carroll et al. 2007, 2010; Garboui
et al. 2007; Bissinger et al. 2009; Jordan et al. 2012; Bissinger et al. 2014).
Due to problems associated with use of DEET, and its potential risk to human health,
safer and more effective alternatives are being investigated by the scientific community.
Essential oils and other natural products are considered as potential repellents that are safer
to use as they may have fewer side effects from regular use (Bissinger and Roe 2010).
There have been ongoing efforts to search for safe plant-based natural tick/insect repellents
that are as effective as, or better than, DEET. The objective of current study was to
determine repellency of several essential oils that have demonstrated toxicity or repellency
against other insect pests, but have not been evaluated against lone star ticks.

Materials and methods

Ticks

Nymphs of the lone star tick, A. americanum, were obtained from a colony maintained in a
tick rearing facility at Oklahoma State University, Stillwater, OK, USA. Prior to use in

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bioassays, unfed nymphs were maintained at 22–23 °C with a relative humidity (R.H.) of
95 ± 2 % on a photoperiod of 16:8 h (L:D) at USDA, ARS, Invasive Insect Biocontrol
and Behavior Laboratory, Beltsville, MD, USA. Two- to three-month-old nymphs were
used in repellency bioassays.

DEET and essential Oils

Eight essential oils included in this study were obtained from commercial sources. Thyme
essential oil was obtained from Envisage Essentials (Canton, GA, USA). Oregano, clove,
vetiver, sandalwood, cinnamon, cedarwood, and peppermint essential oils were purchased
from Puritan’s Pride (Oakdale, NY, USA). The sources, scientific names of plants, and
origin of the essential oils are listed in Table 1. Technical DEET (97 % active ingredient)
was purchased from Aldrich (Sigma-Aldrich, St. Louis, MO, USA). DEET was tested as
the positive control for comparison with essential oils in repellency against the A. amer-
icanum nymphs.
All essential oils and Technical DEET were serial diluted in ethanol to generate fol-
lowing test concentrations (10.0, 5.0, 2.5, 1.25, 0.625, 0.313, 0.156, 0.078, and 0.039 %).
A volume of 165 ll of each test solution was applied to the filter paper (see below),
resulting in corresponding surface concentration of 0.826, 0.413, 0.206, 0.103, 0.052,
0.026, 0.013 and 0.008 mg/cm2, respectively. Filter paper treated with ethanol alone was
tested as the negative control.

Repellency bioassay

The vertical filter paper bioassay takes advantage of the tendency of host-seeking ticks to
climb slender vertical surfaces, and the bioassay technique has been described in detail
previously by Carroll et al. (2009, 2011). Briefly, a 4 9 7 cm rectangle of Whatman No. 4
filter paper was marked with a pencil into two 1 9 4 cm zones at the far ends of the paper
and a central 4 9 5 cm zone. A volume of 165 ll of test solution was applied to the central
zone of the filter paper with even and complete coverage by pipettor and given 10–15 min
to dry. The paper strip was suspended from a bulldog clip hung from a slender dowel held
by an Aptex No. 10 double clip work holder (Aptex, Bethel, CT, USA). A Petri dish (9 cm

Table 1 The names, sources, plant species, and countries of origin of the essential oils tested for repellency
against Amblyomma americanum nymphs
Essen. oil Source Plant species—parts extracted Country of origin

Oregano Puritan’s Pride Origanum vulgare—whole plant Hungary

Clove Puritan’s Pride Eugenia caryophyllta—flowers Indonesia
Thyme Envisage solutions Thymus satureloldes—leaves and flowers Morocco
Vetiver Puritan’s Pride Vetiveria zizanioides—root Haiti/India/Indonesia
Sandalwood Puritan’s Pride Sanalum album—trunk, stem, and roots Indonesia
Cinnamon Puritan’s Pride Cinnamomum zelanicum—stem and leaves Sri Lanka
Cedarwood Puritan’s Pride Cedrus atlantica—root Morocco
Peppermint Puritan’s Pride Mentha piperita—flowers and leaves India

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diameter) was glued in the center of a 15 cm diameter larger Petri dish to create a moat
between their walls. Water was added in the moat to prevent tick escape. The moated Petri
dishes were placed beneath the suspended filter paper. Ten A. americanum nymphs were
released from rim of a storage vial on the lower untreated zone of the paper strip. Locations
of the nymphs were recorded at 1, 3, 5, 10 and 15 min. Ticks were considered repelled if
they stayed on the lower untreated zone or fell off the filter paper without having crossed
into the upper untreated zone. If they climbed to the upper untreated zone, they were
removed to prevent return to the lower zones. Each treatment had three replicates, and full
concentration response was established for DEET and each essential oil.

Data analysis

The concentration repellency response data from the vertical filter paper bioassays were
analyzed using the PoloPlus 2.0 software (Leora Software, Petaluma, CA, USA) to obtain
the effective concentrations that repel 50 % and 95 % of the ticks (EC50 and EC95). The
difference between an essential oil and DEET in repellency was designated as significant
(a = 0.05) if the 95 % confidence interval (CI) of their respective EC50 did not overlap.
Graphs were generated using SigmaPlot (Systat Software, San Jose, CA, USA).

Results

The concentration repellency response curves of DEET and eight essential oils against
unfed A. americanum nymphs are shown in Fig. 1. DEET was tested at five different
concentrations, ranging from 0.000 (ethanol only control) to 0.052 mg/cm2. The minimum
DEET concentration that elicited repellency against A. americanum nymphs was
0.008 mg/cm2. Since the mean repellency at the highest concentration tested for DEET,
0.052 mg/cm2, was 90.0 (±5.8) %, no further tests were done at higher concentrations. In
contrast, none of the essential oils elicited higher than 20 % repellency at the same con-
centration (0.052 mg/cm2). All essential oils were tested at higher concentrations, ranging
from 0.052 to 0.836 mg/cm2, and all demonstrated clear concentration-repellency
responses within the concentration range tested (Fig. 1). Results of data analysis using
PoloPlus software are summarized in Table 2. The EC50 and EC95 for DEET was 0.020
and 0.057 mg/cm2, respectively. The LC50s of all essential oils, ranging from 0.113 to
0.297 mg/cm2, were significantly higher than that of DEET (P \ 0.05). Among the eight
essential oils, oregano oil was the most effective (EC50 = 0.113 mg/cm2) and peppermint
oil the least effective (0.297 mg/cm2). The EC50 of peppermint essential oil was similar to
those of cinnamon and cedarwood oils, but was significantly higher than other essential oils
(P \ 0.05). With a few exceptions, the order of EC95s was in general agreement with that
of EC50s.

Discussion

In this study, a vertical filter paper bioassay was used to test the repellency of eight
essential oil samples against unfed A. americanum nymphs, and to compare their effec-
tiveness with DEET which is a standard repellent and the most commonly used repellent
compound in the past decades (Bissinger and Roe 2010). To our knowledge the essential

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Fig. 1 Concentration-repellency
responses of DEET and eight
essential oils against nymphs of
Amblyomma americanum

oils reported in the current study have not been extensively tested to evaluate their
repellency against common tick species in the USA. As ethanol is included as a component
(solvent) of many commercial DEET formulations, it was used as untreated control in
repellency bioassays for the current and previous published studies (Mehlhorn et al. 2005;
Schwantes et al. 2008; Bissinger et al. 2009). None of the eight essential oils performed as
well as DEET in repelling A. americanum nymphs in the current study. DEET was 6–15
times more effective than essential oil. It is not uncommon to see relatively lower repel-
lency of essential oils against vector species in comparison to synthetic repellent com-
pounds like DEET. Based on the EC50 estimates, the order of the eight essential oils in
repellency against A. americanum nymphs is: oregano [ clove [ thyme [ vetiver [
sandalwood [ cinnamon [ cedarwood [ peppermint.

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Table 2 Estimated effective concentrations of DEET and eight essential oils that repel 50 % (EC50) and
95 % (EC95) of Amblyomma americanum nymphs from vertical filter paper bioassays
Repellent EC50 (mg/cm2) 95 % CI EC95 (mg/cm2) 95 % CI v2 (df)

DEET 0.020 0.016–0.026 0.057 0.041–0.115 12.3 (10)

Oregano 0.113 0.092–0.140 0.261 0.196–0.450 16.2 (13)
Clove 0.122 0.099–0.148 0.396 0.295–0.642 11.4 (13)
Thyme 0.132 0.112–0.156 0.315 0.249–0.462 11.3 (13)
Vetiver 0.133 0.099–0.173 0.655 0.438–1.320 13.0 (13)
Sandalwood 0.147 0.103–0.202 0.568 0.367–1.370 23.4 (13)
Cinnamon 0.205 0.159–0.269 0.497 0.355–0.988 23.1 (13)
Cedarwood 0.224 0.166–0.307 1.936 1.065–5.899 10.0 (13)
Peppermint 0.297 0.227–0.394 0.806 0.561–1.643 22.5 (13)

Three groups of ten nymphs each were tested at each of five concentrations, including the control (ethanol
only)

Essential oil of oregano (Origanum vulgare) as a repellent was also evaluated against
the midge Cuicoide imicola, but similar to the current study it was less effective than
DEET (Braverman and Chizov-Ginzburg 1997). Both thyme and oregano essential oils
demonstrated moderate repellency against female stable flies, Stomoxys calcitrans (L.),
from biting humans (Hieu et al. 2010). Essential oil extracted from Mexican oregano
leaves (Lippia graveolens) demonstrated toxicity against larvae of the cattle tick, Rhipi-
cephalus microplus (Canestrini), and was regarded to have the potential to be used as a
biopesticide for management of cattle ticks (Martinez-Velazquez et al. 2011). Carvacrol,
an active ingredient of essential oils from oregano and thyme species has been investigated
for its potential use as insecticide/acaricide to control arthropod pests of veterinary and
medical importance (Vucinic et al. 2011). Clove oil, which contains eugenol, has been
shown to repel mosquitoes and the sheep tick Ixodes ricinus (L.) (Thorsell et al. 2006), and
was recommended as an insect repellent to prevent vector transmitted diseases (Shapiro
2012).
Vetiver essential oil was as effective as oregano, clove and thyme oils in the present
study. Vertiver oil has been reported to act as both repellent and toxicant against ants,
cockroaches, mosquitoes, and ticks (Maistrello et al. 2001; Henderson et al. 2005;
Sathantriphop et al. 2014). Sandalwood, cinnamon, cedarwood and peppermint essential
oils have been shown to be repellent to ants, mosquitoes and ticks (Ritchie et al. 2006;
Eller et al. 2014). Santanol, a mixture of the two major components of the sandalwood
essential oil, was shown to be repellent to the mite Tetranychus urticae Koch (Roh et al.
2012), but were the least effective against A. americanum.
The relatively low repellency of essential oils found from this study and other studies
illustrated the challenge in search for more effective natural tick repellents. Repellent
formulations that contain multiple essential oils demonstrated synergist effects against
mosquitoes (Reegan et al. 2014). Synergistic effects of essential oil mixtures to increase
repellency have not been investigated for tick species. The mixture repellent approach may
lead to enhanced tick repellency of natural product ingredients to a level that use of the
synergized formulations would provide sufficient protection to humans, domestic animals,
and wildlife from bites by the lone star tick and the blacklegged tick, the most abundant
tick and Lyme disease vector, respectively, in the Unites States.

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Acknowledgments The authors wish to thank James McCrary of USDA, ARS, Invasive Insect Biocontrol
and Behavior Laboratory (IIBBL) for technical support, and Dr. Erika Machtinger (USDA, ARS, IIBBL) for
critical review of the manuscript. H. Meng was supported by a scholarship from China Scholarship Council;
LM Costa Junior was supported by a Grant from the Science Without Borders Program of CAPES, a
Foundation affiliated with the Ministry of Education of Brazil; and AY Li was supported by funds from an
ARS in-house Project (#8042-32000-008-00)—Prevention of Arthropod Bites.

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