Field studies of the efficacy of some commercially available essential oils against horse flies (Diptera: Tabanidae)

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© 2016 E. Schweizerbart’sche Verlagsbuchhandlung, Stuttgart, Germany www.schweizerbart.de
DOI: 10.1127/entomologia/2016/0121 0171-8177/16/0121 $ 2.25
Entomologia Generalis, Vol. 36 (2016), Issue 2, 097–105 Article
Published in print October 2016
Field studies of the efcacy of some commercially
available essential oils against horse ies (Diptera:
Tabanidae)
Stjepan Krčmar1* and Vlatka Gvozdić2
1 Odjel za biologiju, Sveučilište JJ Strossmayera, Cara Hadrijana 8/A, HR-31000
Osijek/Esseg, Hrvatska, Croatia
2 Odjel za kemiju, Sveučilište JJ Strossmayera, Cara Hadrijana 8/A, HR-31000
Osijek/Esseg: Hrvatska, Croatia
* Corresponding author: stjepan@biologija.unios.hr
With 4 tables
Abstract: The repellent activity of commercially available essential oils from the plants
Cymbopogon winterianus, Mentha piperita, Litsea citrata and Lavandula angustifolia against
female horse ies (Tabanidae) is not yet known, and it was studied in Eastern Croatia. In the
absence of standard protocols for determining repellency in eld studies, ve canopy traps
baited with 1-octen-3-ol were used, four of which were protected with essential oils. One can-
opy trap was always without any essential oil and used as negative control. The chi-square
analyses of the trapping data for the canopy traps revealed that the essential oil of Lavandula
angustifolia signicantly reduced the number of collected horse ies in comparison to those
collected in the canopy traps protected with the other essential oils. Signicantly less specimens
of Tabanus bromius were collected from the canopy traps protected with Lavandula angustifo-
lia when compared with the traps protected with the other essential oils. However, the numbers
of females of Tabanus tergestinus and Haematopota pluvialis collected from the canopy traps
protected with all four essential oils did not differ signicantly. A total of 93.6% of horse ies
collected belonged to these three species. Tabanus bromius was the most abundant species with
76.5% in the samples collected by canopy traps. Finally, the traps protected with the essential
oil of Lavandula angustifolia collected 0.50 times less horse ies than unprotected traps,
whereas traps protected with oils of Mentha piperita, Cymbopogon winterianus, and Litsea
citrata collected 0.19, 0.15 and 0.04 times less horse ies, respectively, than did unprotected
traps.
Keywords: Tabanidae; Diptera; canopy traps; repellents; Croatia
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98 S. Krčmar and V. Gvozdić
1. Introduction
Females of horse ies (Tabanidae) are intermittent feeders, their painful bites elicit a
protective response from the animal or human so they are frequently forced to move
to another host without having the chance to procure a full blood meal (Blahó et al.
2013). Therefore, they are considered to be among the major Dipteran pests of man and
animals worldwide (Foil 1989). Different insecticides are used worldwide to control
vectors that transmit parasites or pathogens, but many of them are resistant to these
chemicals (Nerio et al. 2010). The use of synthetic pyrethroids or synthetic compounds
such as DEET (N,N-diethyl-3-methilbenzamide) has elicited concerns about the dan-
gerous effects on human health and the environment (Hang Chio & Yang 2008, Cetin
et al. 2009, Soares et al. 2010). Because of that interest in plants as natural sources of
repellent compounds for personal protection against hematophagic arthropods has been
renewed (Soares et al. 2010). A large number of essential oils extracted from different
plant families has been shown to have high repellency against different arthropod spe-
cies (Nerio et al. 2010). Among essential oils producing plants, some genera, such as
Cymbopogon spp., Eucalyptus ssp. and Ocimum spp. have been widely studied (Nerio
et al. 2010). Citronella oil from Cymbopogon ssp. plants was the most widely used
repellent before the 1940s, and is still used today in many formulations (Katz et al.
2008). Many essential oils isolated from different plants have been tested against dif-
ferent kinds of mosquitoes (Barnard 1999, Gillij et al. 2008, Cilek et al. 2011, Foko
Dadji et al. 2011). Also, the essential oils and extracts from the genera Origanum,
Cymbopogon, Eucalyptus, show high repelency activity against some species of ticks,
mosquitoes and lice (Cetin et al. 2009, Nerio et al. 2010, Soares et al. 2010). Essential
oils against ticks, mosquitoes, lice and agricultural pests have been reported by a vari-
ety of authors and are considered to be an underused alternative to synthetic pesticides
(Panella et al. 2005). In this context, essential oils may represent a useful tool for the
protection from ectoparasites and can also potentially be combined with other control
strategies (Cruz et al. 2013). Furthermore, botanical extracts (essential oils) could be
contribute to high production of milk and animal meat free of unsafe chemicals that
are dangerous to humans, animals and the environment (Agnolin et al. 2010). Despite
a great number of studies on the repellent activity of some essential oils against differ-
ent groups of hematophagic arthropods such as mosquitoes and ticks, repellent activity
of essential oils against horse ies is not known. The purpose of the present study was
to investigate the repellent activity of some commercially available essential oils of
the plants Cymbopogon winterianus, Mentha piperita, Litsea citrata and Lavandula
angustifolia against female specimens of horse ies in Eastern Croatia.
2. Material and Methods
The study area: The study was carried out on a meadow in the Monjoroš Forest com-
plex (UTM CR 37), (45° 45’ N, 18° 52’ E) approximately 2 km far from the Kopački
rit Nature Park in Eastern Croatia. The length of the meadow is approximately 1000 m
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Efcacy of some commercially available essential oils against horse ies 99
and its width 300 m. This meadow is bordered on all sides by forest of common
oak Quercus robur (L.) and ash Fraxinus angustifolia (Vahl.). The largest part of the
Monjoroš Forest lies between 78 and 82.5 m above sea level.
Traps and repellents: The repellent activity of the four essential oils of the plants
Cymbopogon winterianus, Mentha piperita, Litsea citrata, and Lavandula angus-
tifolia against horse ies was studied. These essential oils were made in Pranarõm
International, Ghislenghien, Belgium. To determine the repellent activity of the essen-
tial oils against horse ies ve black and white linen modied Manitoba traps, or so
called tent-like canopy traps, were used. These traps were constructed according to the
design of Hribar et al. (1991). All traps were baited with 4 ml of 1-octen-3-ol (98%
pure; made in Sigma-Aldrich Chemie GmbH, Steinheim, Germany) and they were to
represent warm blooded animals. Attractant 1-octen-3-ol was dispensed from a plas-
tic glass. A 5 cm long cotton wick protruded from the glass to the outside. The plas-
tic glasses were placed 30 cm below the top of the modied Manitoba traps (canopy
traps). Outside of the traps four wooden sticks were placed at the distance of 1m from
all four corners of the modied Manitoba traps (canopy traps). On those wooden sticks,
plastic glasses with the essential oils were attached at the height of 80 cm. This height
corresponds to the distance of the enterance of the traps from the ground. Each time,
four traps were baited separately with 16 ml (4 × 4 ml) of the essential oils. The fresh
repellents (essential oils) and the attractant (1-octen-3-ol) were added at the beginning
of each trapping period. The repellents were rotated between traps every day. There was
always one modied Manitoba trap (canopy trap) without any repellents that served as
negative control. All traps were 100 m apart, placed in the middle of meadow, about
150 m from the forest edge. The daily trapping period was between 9 a.m. and 7 p.m.
After each daily sampling the average volumes of expended repellents and attractants
were measured. Samplings were carried out during summer months of 2012, from 7th
to 11th June, from 2nd to 6th July, and from 1st to 5th August. During 2013 samplings
were carried out from 2nd to 6th July. A total of 20 samplings were made. The experi-
ments were conducted during hot period of the year under varying weather conditions
(Table 1). The trapped horse ies were collected and stored in 70% ethanol solution.
Table 1. Weather conditions during study period.
Study period Average daily
temperature
°C
Relative
humidity
%
Cloudiness Wind
velocity
m/s
Rainfall
mm/m2
from 7th to 11th June 2012 18,3 – 25,5 40 – 95 2/8 – 7/8 1,9 – 2,5 –
from 2nd to 6th July 2012 25,3 – 27,8 35 – 80 0/8 – 5/8 1,9 – 2,5 –
from 1st to 5th August 2012 22,6 – 29 37 – 83 1/8 – 3/8 0,8 – 1,3 –
from 2nd to 6th July 2013 22,1 – 26,4 41 – 97 1/8 – 8/8 1,2 – 3,8 20
Identication and analysis: Identication and nomenclature followed that of Chvála
et al. (1972), Chvála (1988) and Krčmar et al. (2011). The differences observed
between the numbers of horse ies collected in modied Manitoba traps (canopy
traps) protected with the four essential oils and the behavior of the most abundant
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100 S. Krčmar and V. Gvozdić
horse ies towards the traps with the different essential oils were tested by a Chi-
square analysis at P < 0.05. The Kruskal-Wallis test, was used to detect differences
between the numbers of horse ies repelled/attracted to each repellent/attractant and
between trap sites. Pearson’s correlation coefcient (at p < 0.05) was used for relation-
ship analysis between evaporated amount of essential oils and the number of collected
horse ies. All statistical analyses were performed by using Statistica 12 software.
3. Results
A total of 2565 specimens were collected, belonging to 18 species of horse ies grouped
into the genera: Chrysops, Atylotus, Hybomitra, Tabanus and Haematopota (Table 2).
Tabanus bromius comprised 76.5% of the horse ies collected. It was followed by
Tabanus tergestinus with 11.6% and Haematopota pluvialis with 5.3%. These three
species represented 93.5% of the horse ies collected, while the remaining 15 species
made up the remainder (Table 2). The majority of horse ies 24.3% were collected
from the control traps without any essential oils, whereas 23.3% were obtained from
traps protected with the Litsea citrata essential oils, 20.7% were obtained from traps
protected with oils from Cymbopogon winterianus, while 19.6% were obtained from
traps protected with oils of Mentha piperita. The least number of horse ies 12.1%
of the total collected was obtained from the modied Manitoba traps (canopy traps)
protected with essential oils of Lavandula angustifolia. The χ2 test of the trapping data
revealed that the essential oil of Lavandula angustifolia signicantly reduced the num-
ber of horse ies collected in the modied Manitoba traps (canopy traps) in compari-
son to the other essential oils used in this experiment (Table 3). Also, χ2 test revealed
that there was signicant difference between the numbers of horse is collected in
traps with essential oils of Cymbopogon winterianus, Mentha piperita and Litsea cit-
rata (Table 3). However, there was no signicant difference between the numbers of
horse ies collected in the traps with Litsea citrata and numbers of horse ies attracted
to the control traps (χ2 = 0.598, P > 0.05). The Kruskall-Wallis test revealed that there
was no signicant site effect on the number of collected horse ies in the control traps
and in the traps with repellents (H = 1.8670, df = 4, p = 0.7602; H = 4.6748, df = 4,
p = 0.3223; H = 3.6081, df = 4, p = 0.4616, H = 2.2726, df = 4, p = 0.6857; H = 3.3157,
df = 4, p = 0.5064). The canopy traps protected with Lavandula angustifolia collected
signicantly less Tabanus bromius then traps protected with the other essential oils
as potential repellents (Table 4). However, there was no signicant difference in the
numbers of collected specimens of Tabanus tergestinus and Haematopota pluvialis in
traps protected with all four essential oils (Table 4). The response of the other species
to the repellents was not analyzed because of small sample sizes. The largest number
of horse ies, 53.2% was collected during July 2012. All of the collected specimens
were females. A negative relationship was between evaporated rate of essential oils
and the number of collected specimens of Tabanus bromius (r = – 0.94, p = 0.058) and
Tabanus tergestinus (r = – 0.87, p = 0.130). Increase of evaporated rate of essential
oil reduces the number of sampled speciemens of these species in traps. Unlike from
Haematopota pluvialis (r = 0.91, p = 0.083) for whom positive relationship between
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Efcacy of some commercially available essential oils against horse ies 101
Table 2. List of total number of horse ies sampled by modied Manitoba traps (canopy traps) protected with different essential oils and control
traps baited with 1-octen-3-ol (Diptera: Tabanidae).
Species / essential oils and attractant Lavandula
angustifolia
Mentha
piperita
Cymbopogon
winterianus
Litsea
citrata
1-octen-3-ol ∑
Tabanus bromius L. 216 381 422 485 459 1963
Tabanus tergestinus Egger 45 56 55 63 80 299
Haematopota pluvialis L. 29 29 22 15 43 138
Tabanus sudeticus Zeller 4 13 6 12 14 49
Atylotus loewianus (Villeneuve) 5 14 10 9 10 48
Tabanus autumnalis L. 25 4 3 5 19
Hybomitra ciureai (Séguy) 3 1 1 2 2 9
Tabanus maculicornis Zetterstedt 2-212 7
Tabanus bovinus L. - - 1 4 1 6
Haematopota ocelligera (Kröber) -21 1 26
Haematopota subcylindrica Pandellé 1 - 2-25
Hybomitra acuminata (Loew) -21 - 25
Atylotus avoguttatus (Szilády) 2- 1 - 1 4
Chrysops relictus Meigen 1 - 1 1 - 3
Atylotus rusticus (L.) - - 1 - - 1
Hybomitra ukrainica (Olsufjev) - - - - 1 1
Haematopota crassicornis Wahlberg - - 1 - - 1
Haematopota italica Meigen - - - 1 - 1
∑ 18 310 503 531 597 624 2565
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102 S. Krčmar and V. Gvozdić
both variables was observed (at p < 0.05). During the study period the average evapo-
rate rate for the essential oils of Lavandula angustifolia was 1.0 ml per hour, followed
by Mentha piperita with 0.8 ml, Cymbopogon winterianus with 0.5 ml and Litsea
citrata with 0.4 ml.
Table 3. The χ2-test values for horse ies sampled by modied Manitoba traps (canopy traps)
protected with four essential oils (Diptera: Tabanidae).
Essential oils Lavandula
angustifolia
Mentha
piperita
Cymbopogon
winterianus
Litsea
citrata
χ2
Number of sampled horse ies 310 503 531 597 93.97*
503 531 597 8.56*
*Signicant differences (P < 0.05).
Table 4. The χ2-test values for some of the most abundant horse ies sampled by modied
Manitoba traps (canopy traps) protected with different essential oils (Diptera: Tabanidae).
Species / essential oils Lavandula
angustifolia
Mentha
piperita
Cymbopogon
winterianus
Litsea
citrata
χ2
Tabanus bromius L. 216 381 422 485 105.87*
Tabanus tergestinus Egger 45 56 55 63 2.77
Haematopota pluvialis L. 29 29 22 15 5.66
*Signicant differences (P < 0.05)
4. Discussion
Vector-borne disease transmission among human population and farmed animals
mainly involves members of the arthropod class Insecta (Logan & Birkett 2007).
These insects predominantly comprise dipterous ies, including the families Culicidae,
Muscidae, Ceratopogonidae, Glossinidae and Psychodidae (Logan & Birkett 2007).
Although insect-borne diseases currently represent a greater health problem in tropi-
cal and subtropical climates, no part of the world is immune to their risks (Fradin
& Day 2002). Because of this protection from insect bites is best achived using an
insect repellent (Fradin & Day 2002). Repellents reduce the number of arthropod
bites because arthropod bites are a necessary step in the transmission of vector-
borne pathogens, therefore repellents reduce the occurrence of infection and disease
(Debboun & Strickman 2013). The best known synthetic (chemical) insect repellent
is N,N-Diethyl-3-methyl-benzamidae (DEET), (Fradin & Day 2002). Though a lot
of plants have been tested as potential sources of insect repellents, only a few plant
derived chemicals tested to date demonstrate the broad effectiveness and duration as
good as N,N-Diethyl-3-methyl-benzamidae (Cockcroft et al. 1998 according to Koul
et al. 2008). However, recent studies have conrmed the repellency effectiveness of
plant essential oils against Dipteran blood-sucking insects, particularly in mosquitoes
(Zhu et al. 2006). Some essential oils are known as effective repellents against the
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Efcacy of some commercially available essential oils against horse ies 103
Culex speceis and against some species from the family Ixodidae in the laboratory
and eld studies (Jaenson et al. 2006, Choi et al. 2002, Soares et al. 2010). The data
obtained from this study provide insight into the repellent activity of the essential oils
of the plants Cymbopogon winterianus, Mentha piperita, Litsea citrata and Lavandula
angustifolia against horse ies. There were no earlier studies for the evaluation of the
efcacy of the above mentioned essential oils as potential repellents against horse
ies in eld studies. Similar eld studies were carried out in Puerto Rico, where the
citronella essential oil from plants (Cymbopogon winterianus) was an effective repel-
lent against female mosquitoes, because it repelled 22% of mosquitoes from traps
(Müller et al. 2009). Also, the Cymbopogon winterianus oil showed the repellent
effect against the stable y Stomoxys calcitrans (Baldacchino et al. 2013), whereas
mixture of Cymbopogon winterianus oil with 5% vanilin gave 100% protection for 6h
against Aedes aegypti, Culex quinquefasciatus and Anopheles dirus (Tawatsin et al.
2001). Citronella oil alone, without any other chemicals mostly showed inferior ef-
cacy in comparison with newer products (Katz et al. 2008). However, in this study in
eastern Croatia its repellence was low against horse ies, indicating that the repellent
activity of this essential oil varies for the different haematophagous families of the
Diptera order. Moreover, major differences in the efcacy of some natural repellents
were caused by the differences in concentration, application and test methods (i.e.
hand in box vs. eld trials, human landing catch vs. eld trials), (Müller et al. 2009).
The present results showed that the essential oil of Lavandula angustifolia had best
effect against horse ies compared to the oils of Cymbopogon winterianus, Mentha
piperita and Litsea citrata. Similar observation was made in Turkey for L. angustifo-
lia which is also effective against various groups of insects (Koul et al. 2008). Also,
the essential oil of Lavandula angustifolia was highly effective against stored product
beetles Sitophilus oryzae (L.) and Rhyzopertha dominica (F.) (Rozman et al. 2007).
In the comparison of the repellent activity between the essential oils of Mentha piper-
ita, Cymbopogon winterianus and Litsea citrata, the essential oil of Mentha piperita
showed the best effect against horse ies. Also, the essential oil of Mentha piperita
repels ies, ants, lice and moths (Koul et al. 2008). In many cases the efciency of
a repellent depends on various factors such as vector species, age, sex, temperature,
rainfall and wind velocity (Hazarika et al. 2012). Essential oils are liquid at room tem-
perature and get easily transformed from a liquid to a vapor phase (Koul et al. 2008).
In general, monitoring of volatile plant extracts and essential oil composition demon-
strated that stability forfeits with temperature rise from 23 to 38 °C (Turek & Stintzing
2012). Moreover, augmentation in degrees Celsius increases the amount of unidenti-
ed polymerization products (Turek & Stintzing 2013). In our study the repellents did
not evaporate by the end, as always one small part separated through sedimentation at
the bottom of the plastic glasses in solid state. Terpenoids in essential oils, especially
mere terpens and aldehydes are thermolabile and susceptible to rearrangement pro-
cesses at elevated temperatures (Turek & Stintzing 2013). The application of essential
oils on linen canopy traps might be more effective than application in plastic glasses
far away from the traps. Some studies showed that a synthetic repellent absorbed onto
the linen of traps results in long-term repellency (N’ Guessan et al. 2006). Without a
standardized protocol, it is very hard to comapre the repellency of the same essential
oils between diferrent athropod groups.
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104 S. Krčmar and V. Gvozdić
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Manuscript received: 9 April 2014
Accepted: 11 April 2016
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