Lavender, eucalyptus, and orange essential oils as repellents against Ixodes ricinus females

Abstract

This study evaluated the repellent effect of three essential oils against females of Ixodes ricinus, which is considered to be
the main arthropod disease vector in Europe. The essential oils could be regarded as user- and environment-friendly alternatives
to synthetic repellents. As a comparison sample, the most widely used synthetic repellent DEET was used. All the tested
oils exhibited moderate to high initial repellency of 65–85% 5 min after application. The testing was terminated after 80
min, when lavender and eucalyptus repelled 45% and 15% of ticks, respectively. No effect of orange oil was observed after
a 20-min mark. The effect of DEET was found to be high and stable (95–100%) throughout the experiment. This study thus
revealed that the investigated oils are not as effective as DEET. On the other hand, especially lavender showed an interesting
potential as an alternative repellent for outdoor activities of shorter duration.

Full text

76 Scientia agriculturae bohemica, 48, 2017 (2): 76–81
animal ScienceS
doi: 10.1515/sab-2017-0014
Received for publication on October 13, 2016
Accepted for publication on December 15, 2016
INTRODUCTION
In Europe, the sheep tick (Ixodes ricinus L.) is
considered to be the main arthropod disease vector
(Jaenson et al., 2006; Hartemink, Takken,
2016). The most common of such illnesses are Lyme
disease, which infects 65 500 people annually in
Europe (R i z z o l i et al., 2011) and tick-borne en-
cephalitis, infecting 5000–12 000 people annually
in Europe (European Centre for Disease
Prevention and Control, 2014). Moreover,
rickettsial, babesia, bartonella and anaplasma syn-
dromes transmitted by ticks were newly described in
the past decade (D i e t r i c h et al., 2010; S c h o r n
et al., 2011; S o r m u n e n et al., 2016; S z e k e r e s
et al., 2016). Effective vaccinations are not available
for many of these infections, so using repellents is a
desirable option for preventing tick-borne diseases
(Del Fabbro, Nazzi, 2008).
Repellents are defined as substances that force
arthropods to move away from a repellent’s source,
which may be applied directly to skin, clothing or
shelter (D a u t e l et al., 2013). In the past five decades,
many synthetic chemical repellents were developed
to protect human health. DEET (N, N-diethyl-m-
toluamid) is one of the most widely used synthetic
repellents (G o o d y e r, B e h r e n s , 1998) provid-
ing an adequate protection for most common situa-
LAVENDER, EUCALYPTUS, AND ORANGE ESSENTIAL
OILS AS REPELLENTS AGAINST Ixodes rIcInus
FEMALES*
M. Kulma1, T. Bubová1, O. Kopecký1, F. Rettich2
1Czech University of Life Sciences Prague, Department of Zoology and Fisheries, Prague,
Czech Republic
2National Institute of Public Health, Prague, Czech Republic
This study evaluated the repellent effect of three essential oils against females of Ixodes ricinus, which is considered to be
the main arthropod disease vector in Europe. The essential oils could be regarded as user- and environment-friendly alterna-
tives to synthetic repellents. As a comparison sample, the most widely used synthetic repellent DEET was used. All the tested
oils exhibited moderate to high initial repellency of 65–85% 5 min after application. The testing was terminated after 80
min, when lavender and eucalyptus repelled 45% and 15% of ticks, respectively. No effect of orange oil was observed after
a 20-min mark. The effect of DEET was found to be high and stable (95–100%) throughout the experiment. This study thus
revealed that the investigated oils are not as effective as DEET. On the other hand, especially lavender showed an interesting
potential as an alternative repellent for outdoor activities of shorter duration.
repellency, alternative repellents, DEET, sheep tick, vector
* Supported by the Ministry of Education, Youth and Sports of the Czech Republic, (EUREKA grant,), Project No. LF14040, and by the
Internal Grant Agency of the Czech University of Life Sciences Prague (CIGA), Project No. 20152004.

Scientia agriculturae bohemica, 48, 2017 (2): 76–81 77
tions in concentrations 10–35% (K a t z et al., 2008).
The long duration of protection DEET provides is an
unquestionable advantage, but there are still doubts
regarding safety for human health (A q u i n o et al.,
2004). These uncertainties are based on documented
medical complications occurring after its application,
poisonings after inhalation or eye contact (G o o d y e r,
B e h r e n s , 1998). Additionally, damage to the central
nervous system has also been reported, particularly in
children (F r a n c e s , 2007;O s i m i t z et al., 2010).
Other known complications associated with DEET
exposure include cardiovascular and dermatological
reactions (Stajković, Milutinović, 2013).
Additionally, S e m m l e r et al. (2011) also point out
that DEET is sticky, has an unpleasant odour, and
dissolves plastic. Due to its long half-life, DEET has
also been identified as a contaminant of aquatic water
systems all over the world (A q u i n o et al., 2004;
C o s t a n z o et al., 2007). For these reasons, the de-
velopment of alternative repellents without adverse
effects is very important.
Essential oils can be considered as an alternative
repellent (M e n g et al., 2016). These substances
are complex mixtures of volatile organic compounds
produced by metabolism of a plant as secondary me-
tabolites (N e r i o et al., 2010; Y o o n et al., 2011).
Some have been reported as quite effective natural
repellents against arthropod pests (e.g. C a r r o l l et
al., 2007; Z e r i n g ó t a et al., 2013; M e n g et al.,
2016), including I. ricinus (e.g. J a e n s o n et al.,
2006; T h o r s e l l et al., 2006; E l - S e e d i et al.,
2012). However, due to their high volatility, repel-
lency of essential oils is generally regarded as short
term in nature (Z h u et al., 2001) and thus they offer
protection for shorter periods of time (J a e n s o n et
al., 2006; N e r i o et al., 2010).
Our study is focused on comparison of repellency
effect and duration between three essential oils and
synthetic repellent 10% DEET, when used as a time-
stable control, against host-seeking I. ricinus females.
It should be noted that not all essential oils are safe
for human use, and several types have even been de-
scribed as allergens or mutagens (T h o r s e l l et al.,
2006). Our primary intention was to test essential oils
that have some repellency effect and which are also
‘user-friendly’ and do not endanger human health. We
therefore selected eucalyptus oil, lavender oil, and
orange oil and statistically compared the efficiency
of these oils with the effectiveness of DEET.
MATERIAL AND METHODS
Adult females of I. ricinus were obtained from a
commercial source (Insect Services, Berlin, Germany).
Prior to analysis, all ticks were kept unfed for one
week to acclimate in polypropylene tubes (with strips
of filter paper inside) stored in a desiccator outfitted
with a plastic cup with soaked cotton wool (to maintain
high humidity) at room temperature. Essential oils were
obtained from Hofigal (Bucharest, Romania), which
also provided chromatographic profiles – see Table
1. The synthetic DEET was obtained from Vertellus
(Herriard, UK). Prior to conducting the bioassays, all
repellent samples were diluted in diethyl ether (Penta,
Chrudim, Czech Republic) to a 10% test concentration.
To evaluate repellency, we used a novel bioassay
based on methods previously described by C a r r o l l
et al. (2011), K r ö b e r et al. (2013), and da C a m a r a
et al. (2015). The experimental and control bioas-
says consisted of two concentric circles (Ø19 cm and
Ø15 cm) drawn on an A4-size sheet of cardboard. In
the experimental arena, the 4 cm wide zone between
these circles was treated evenly with 1 ml of the in-
vestigated repellent solution and the same area in the
control arena was treated with diethyl ether only. The
cardboard sheets were treated separately with each of
the three essential oils (orange, eucalyptus, lavender)
and DEET. Five ticks were first placed in the control
arena (without repellent) to exclude inactive ticks.
If they crossed the outer border of the circle in the
control arena within 60 s, they were then released to
the central untreated zone in the experimental area.
Each repellent was tested in this manner using a total
of 120 individual ticks.
To investigate the effect of time on repellency,
bioassays were performed in six 15 min intervals
from 5 min to 80 min after application. Each tick
was used only once. Ticks are known to be attracted
by many compounds, usually found on a host’s skin
or breath (D a u t e l et al., 2013) so, all tested ticks
were activated to host-seeking mode by the observer’s
Component Percentage
Orange essential oil limonene 18.5–24.0
cineol 5.0–8.0
Eucalyptus essential oil
α-pinene 0.05–10
β-pinene 0.05–1.5
limonene 0.05–15.0
1,8-cineol > 60.0
Lavender essential oil
limonene > 1.0
cineol > 2.5
3-octanone > 2.5
camphor > 1.2
linalool 20.0–45.0
linalyn acetate 25.0–46.0
terpinen-4-ol 0.1–6.0
lavandulyl acetate > 0.2
lavandulol > 0.1
α-terpineol < 2.0
Table 1. Chromatographic profiles of tested essential oils

78 Scientia agriculturae bohemica, 48, 2017 (2): 76–81
breath (to simulate host stimuli) immediately after
their entrance to both experimental and control arenas.
The ticks were considered to be repelled only if they
did not cross the repellent barrier. Based on the test
results, the ticks were then divided into two respective
groups: repelled/unrepelled (1/0).
Repellent effectiveness data were processed using
a generalized linear model (GLM) with quasibinomial
distribution. Time and type of repellent were desig-
nated as fixed factors. Quasibinomial distribution
was used because of expected overdispersion in our
dataset. GLM was followed by a post-hoc Tukey’s
test, which was performed in the multcomp package
using the glht function. All statistical tests were run
using R software (Version 3.1.2, 2014).
RESULTS
We detected a great variability in repellent ef-
fectiveness (Table 2). The Tukey’s post-hoc test re-
vealed differences in effectiveness between each of the
tested repellents (P < 0.001 for all tests). The orange
oil stopped only 10.8% of ticks, while eucalyptus
stopped 39.2%, lavender 73.3%, and DEET 98.3%.
Effectiveness generally decreased over time (Fig. 1),
but this was true mainly for the natural repellents
(orange, eucalyptus, lavender). Efficiency of DEET
was not influenced by time (Table 2, Fig. 1).
DISCUSSION
The results obtained showed significant differences
between the tested repellents as well as in the effect
of time on repellency, particularly for the essential
oils. All investigated samples showed high initial
repellency. Five minutes after application, repellency
ranged from 65 to 85%; however, the effectiveness of
the investigated essential oils decreased after 80 min
to a range of 0–45%.
The bioassay performed in this study also dem-
onstrated that all the essential oils may be regarded
as ‘true repellents’ and do not merely cover the host
odour, as do some other oils according to a report by
J a e n s o n et al. (2006). Sampled ticks apparently
changed the direction of their movement immediately
after first contact with treated areas.
A high initial repellency of essential oils against
I. ricinus has been reported in previous studies by
J a e n s o n et al. (2006) or G a r b o u i et al.(2007).
Additionally, the long-term effectiveness of oils against
these ticks was demonstrated in a study by E l - S e e d i
et al. (2012), who found no significant changes in
repellency even after 24 h. That field test was per-
formed, however, using treated flannel cloth, which
has different evaporation characteristics as compared
to cardboard, filter paper or human skin.
Some people (especially parents with children) do
not spend long time in parks or other areas with natural
tick incidence or maybe do not want to use synthetic
repellents due to allergy or sensitivity. Therefore, we
believe it is essential to understand fully the interaction
between repellency and time. Lavender and eucalyptus
oils were included into this study despite the results
presented by T h o r s e l l et al. (2006), who found no
repellency from these two oils against ticks 4 h after
application.
The strongest and most stable repellency effect
was found for lavender oil. A rather high protective
effect of this plant has previously been described
against the cigarette beetle (Lasioderma serricorne
Fabricius) (H o r i , 2003) and spot clothing wax cicada
(Lycorma delicatula) (Yo o n et al., 2011). It also has
been found to be quite effective against I. ricinus in
high concentrations and shortly (15 min) after ap-
plication (K r ö b e r et al., 2013). On the other hand,
it is apparent both from other previously published
results (T h o r s e l l et al., 2006; S e m m l e r et al.,
2011) and also from our data that lavender essential
oil exhibits a significant protection period against I.
ricinus. The aforementioned authors tested laven-
der oils on such surfaces as cardboard (this study),
petri dishes (T h o r s e l l et al., 2006), and bare skin
(S e m m l e r et al., 2011). We may expect a longer
period of protection if lavender oil would be tested
on textile materials.
M a g a n o et al. (2011) tested the effectiveness of
eucalyptus essential oil as a repellent against another
Table 2. Repellency of essential oils (GLM model)
χ² test P
Repellent 257.252 < 0.001
Time 61.112 < 0.001
Repellent*time 30.185 < 0.001
Fig. 1. Repellent effectiveness of three essential oils and DEET over time
1


0
25
50
75
100
5 20 35 50 65 80
repellent effectiveness (%)
time (min)
ORANGE EUCALYPTUS LAVENDER DEET

Scientia agriculturae bohemica, 48, 2017 (2): 76–81 79
tick species, Hyalomma marginatum rufipes, and dem-
onstrated that the repellency of Eucalyptus globoidea
(Blakely) extract compared favourably with that of
the commercial arthropod repellent DEET. Moreover,
P i r a l i - K h e i r a b a d i et al. (2009) reported acari-
cidal effects of eucalyptus. Nevertheless, the repellency
after 80 min determined in this study was only 15%.
To the best of our knowledge, this was the first
evaluation of orange essential oil as a repellent against
ticks. In comparison with established types of es-
sential oils, it exhibited the fastest evaporation and
its efficiency was the weakest from the onset of the
experiment. We can conclude, therefore, that this type
of oil shows no potential for future studies.
The protection periods offered by such essential oils
as those from lemongrass (Cymbopogon Spreng), cloves
(Syzygium aromaticum Merrill & Perry) (T h o r s e l l
et al., 2006), carnation flowers (Dianthus caryophyllus
L.) (T u n ó n et al., 2006), and wormwood (Artemisia
absinthium L.) (J a e n s o n et al., 2006) are compa-
rable to that of 15% DEET (T h o r s e l l et al., 2006;
T u n ó n et al., 2006; B i s s i n g e r et al., 2016).
On the other hand, it must be said that the duration
of tick repellency among essential oils is connected
with toxicity and various side effects (T h o r s e l l et
al., 2006). Thus, the potential user of essential oils
as repellents faces a trade-off between longer dura-
tion of protection with greater health risks or safer
but shorter protection. This trade-off suggests there
to be two possible areas for future research on es-
sential oil repellency: (i) eliminating health risks of
essential oils providing strong and long protection,
or (ii) enhancing the repelling efficacy of harmless
oils. Such research should therefore focus mainly
on the dosage or concentration of oils (M a g a n o
et al., 2011; M e n g et al., 2016), synergistic effects
(Hummelbrunner, Isman, 2001; Reegan et
al., 2014), or a microencapsulation process (B o h ,
K n e z , 2006; F a u l d e et al., 2012).
CONCLUSION
There are currently many essential oils with un-
known repellency effects, and it is possible that a
natural repellent based on essential oils both effective
and harmless to the user may be discovered. At this
time, lavender oil appears to satisfy the requirement
for compromise between efficiency and health risk.
ACKNOWLEDGEMENT
We are grateful to Kateřina Imrichová for technical
assistance in the laboratory and the company Hofigal
for providing samples. We thank English Editorial
Services, s.r.o., for assistance with the text.
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Corresponding Author:
Ing. Martin K u l m a , Czech University of Life Sciences Prague, Department of Zoology and Fisheries, Kamýcká 129,
165 21 Prague 6-Suchdol, Czech Republic, phone: +420 603 859 559, e-mail: kulma@af.czu.cz