Table Of ContentISSN 0373-5680 (impresa), ISSN 1851-7471 (en línea) Rev. Soc. Entomol. Argent. 68 (3-4): 329-338, 2009 329
Chemical composition of four essential oils from
Eupatorium spp. Biological activities toward Tribolium
castaneum (Coleoptera: Tenebrionidae)
LANCELLE, Hugo G.**, Oscar S. GIORDANO**, Marta E. SOSA*
and Carlos E. TONN **
Facultad de Química, Bioquímica y Farmacia. Universidad Nacional de San Luis. Chacabuco
y Pedernera, 5700, San Luis, Argentina.
*Área de Zoología; e-mail: [email protected]
**INTEQUI-CONICET
Composición química de cuatro aceites esenciales provenientes
de Eupatorium spp. y su toxicidad para Tribolium castaneum
(Coleoptera: Tenebrionidae)
RESUMEN. Se evaluaron las propiedades tóxicas y repelentes de
los aceites esenciales de cuatro especies del género Eupatorium (Asteraceae):
E. buniifolium Hook. et Arn, E. inulaefolium Kunth, E. arnottii Baker y E.
viscidum Hook. & Arn, en diferentes concentraciones frente a adultos de
Tribolium castaneum Herbst. Los aceites esenciales se aislaron de las partes
aéreas de las plantas, mediante técnicas de hidrodestilación y se analizaron
por los métodos GC-FID y GC-MS. Los ensayos de toxicidad por contacto
demostraron que todos los aceites fueron tóxicos y la mortalidad fue, en
todos los casos, dependiente de la dosis. El aceite esencial de E. buniifolium
presentó la mayor actividad repelente.
PALABRAS CLAVE. Tribolium castaneum. Eupatorium. Monoterpenos.
Sequiterpenos. Aceites esenciales. Repelencia. Toxicidad.
ABSTRACT. Toxic and repellent properties of whole essential oils
from four Eupatorium (Asteraceae) species (E. buniifolium Hook. et Arn, E.
inulaefolium Kunth, E. arnottii Baker, and E. viscidum Hook. & Arn) were
investigated in different concentrations toward Tribolium castaneum Herbst
adults. The essential oils were isolated by hydrodistillation techniques from
the aerial parts. The analysis was performed by GC-FID and GC-MS methods.
Contact toxicity assays showed that all the evaluated essential oils were
toxic. Furthermore, in all the cases mortality was dose dependent. The main
repellency was observed for the essential oil recovered from E. buniifolium.
KEY WORDS. Tribolium castaneum. Eupatorium. Monoterpenes.
Sesquiterpenes. Essential oils. Repellency. Toxicity.
INTRODUCTION of Tribolium castaneum Herbst have been
reported. The malathion-specific resistance
Insect pests are one of the main causes of has been intensively studied (Assié et al.,
extensive damage in stored grains and their 2007). Therefore, the use of several kinds
products. Since 1961 (Parkin et al., 1962), of safe insecticides or repellents in food
the resistance to insecticide in many strains grains storage is necessary, and the interest
Recibido: 14-V-2009; aceptado: 19-X-2009
330 Rev. Soc. Entomol. Argent. 68 (3-4): 329-338, 2009
for the development of the pesticides with and cytotoxic (Mongelli et al., 2000). The
natural products extracted from plants has essential oil of Eupatorium betonicaeforme
recently been growing. The interference (D.C.) Baker has been reported due to its
of plant natural products with the feeding, larvicidal properties toward Aedes aegypti
development and survival of insects has been (L.) larvae (Albuquerque et al., 2004).
extensively studied (Sosa & Tonn, 2008). Eupatorium buniifolium Hook. et Arn.
It is well known that the presence of some (known as “romerillo”, “romerillo colorado”
monoterpenes and sesquiterpenes in plants or “chilca”) spreads from northern to central
could help them against predators through Argentina, and decoctions of the aerial
some protection mechanism. Thus, volatile parts are used for antirheumatic, antiseptic
terpenes with low molecular-weight have or digestive treatments. In addition, free-
been reported as insect behavior modifiers as radical inhibition and cytotoxicity have been
well as growth regulators (Hick et al., 1999). reported (Miño et al., 2005). Eupatorium
The insecticidal activity of a large number inulifolium Kunth (“sanalotodo” or “yerba
of plant essential oils has been assayed, de Santa María”) grows in the northeast
exhibiting acute toxic effects against several of Argentina, and it is used externally for
stored-grain insect pests (Liu & Ho, 1999; the treatment of skin infections due to its
Tunç et al., 2000; Padin et al., 2000; Lee antimicrobial properties (Ferraro et al.,
et al., 2001; Kostyukovsky et al., 2002; 1977).
Papachristos et al., 2004; Wang et al., 2005; Taking into account the widespread
Tapondjou et al., 2005; Rozman et al., 2007). distribution of E. buniifolium var. buniifolium,
It has been suggested that essential oils are E. inulifolium, E. arnottii Baker, and E.
less hazardous than synthetic compounds viscidum Hook. & Arn. as well as the yield
and rapidly degraded in the environment of the essential oils recovered from stream
(Isman, 2000; Moretti et al., 2002). distillation, the purpose of this work was to
As part of a program aimed at studying investigate the toxic and repellent activities
the effects of plant secondary metabolites of the isolated essential oils toward the
(García et al., 2003; Pungitore et al., 2004a, insect-pest T. castaneum.
b; Juan H. et al., 2008; Sosa & Tonn, 2008)
and essential oils (García et al., 2005, 2007)
isolated from plants growing in Argentina MATERIAL AND METHODS
toward insect pests, we have investigated
the chemical composition and biological Biological material
effects of the essential oils isolated from four
South American Eupatorium species toward Plants
Tribolium castaneum Herbst (Coleoptera: Aerial parts of Eupatorium arnottii, E.
Tenebrionidae), a worldwide pest of stored viscidum and E. buniifolium were collected
grains. near San Luis City (33º 15´ S, 66º 20´ W) and
The Eupatorium genus includes small in Quebrada de los Cóndores (33º 14´ S,
herbs and shrubs and comprises nearly 600 66º 14´ W), San Luis Province, Argentina.
species distributed in North, Central and Voucher specimens were deposited at the
South America, Eastern Asia, Taiwan and the Herbarium of the Universidad Nacional de
Philippines (Herz, 2001). In Argentina there San Luis (voucher numbers UNSL # 499-
are 82 species growing naturally, and some of Del Vitto, 497-Del Vitto and 495-Del Vitto,
them are used in popular medicine (Cabrera respectively). Eupatorium inulifolium was
et al., 1997). Essential oils, some isolated collected near Corrientes city (27º 35´ S, 58º
secondary metabolites, and extracts prepared 50´ W), Corrientes Province, Argentina. A
from several species of the Eupatorium genus voucher sample, identified by Professors
have shown biological activities including Aurelio Schinini (IBONE, Corrientes) and Luis
antibacterial (Bailac et al., 2000; El-Seedi et Del Vitto (UNSL, San Luis), was deposited at
al., 2002), trypanocidal (Sülsen et al., 2006), the Herbarium of the Universidad Nacional
LANCELLE, H.G. et al. Chemical composition of four essential oils from Eupatorium 331
de San Luis (voucher number UNSL # 491- n-hexane as solvent. One ml of each solution
Del Vitto). was applied to the bottom surface of a 125
ml Erlenmeyer flask and uniformly dispersed
Insects to give, after one hour of evaporation at r.t.,
All experiments were conducted in the final doses ranging between 0.028, 0.056,
laboratory using established colonies from 0.141, 0.169, 0.212 mg/cm2. These doses
an insecticide-susceptible strain of Tribolium were selected after a screening between
castaneum. Adults used in the experiments, 0.010 to 0.5 mg/cm2. After that, 0.5 g of
were reared on a mixture of flour, starch and rearing food were spread in each flask and
yeast (3:3:1) at 25 ± 1 °C, 65% RH and a ten randomly selected and unsexed adults
photoperiod of 16:8 (L:D) h. of Tribolium castaneum, were introduced.
Treated Erlenmeyer flasks were sealed with
Extraction of essential oil a cotton plug and kept at 25 ± 1 °C with a
Fresh aerial parts of Eupatorium arnottii photoperiod of 16:8 (L:D) h. Each treatment
(2.95 kg), E. buniifolium (3.45 kg), E. viscidum was independently replicated five times.
(3.20 kg), and E. inulaefolium (3.00 kg) were Insect mortality was recorded at 24, 48
cut into small pieces and subjected to steam- and 72 hs, and mortality (%) was corrected
distillation at 96 ºC for 3 h using a Clevenger- according to Abbott (1925). Data were
type apparatus. The recovered essential oils analyzed using Two Way ANOVA Test at
were dried over anhydrous sodium sulfate and P≤ 0.05 to determine significant differences
stored in cold (4°C). Yield of dried essential among treatments and time of exposure
oils was 1.81, 2.97, 1.11 and 1.35 g/kg, (Graph Pad InStat, Version 3.0). ED values
50
respectively. The essential oil composition were determined from linear regression.
was determined gas chromatography-mass
spectrometry (GC-MS). The GC-MS analyses Repellency
were carried out using a Shimadzu QP 5000 The experiments employed a two-choice
mass spectrometer coupled with a Shimadzu bioassay. Test arenas were two joined
GC-17A gas chromatograph. Analyses were Erlenmeyer flasks of 125 ml with a glass tube
performed using Ultra-2, 30 m, 0.25 mm i.d., of 1,5 cm long and 0,5 cm diameter fused
0.25 μm film thickness, fused-silica capillary to the base of the side wall of each flask.
column. The oven temperature program Five n-hexane solutions with increasing oil
was 50°C for 4 min, rising to 180°C at 2°C/ concentrations were prepared to give final
min, then to 290 °C at 6 °C/min; the injector doses ranging between 0.028, 0.056, 0.141,
temperature was 240 °C; the carrier gas was 0.169, 0.212 mg/cm2.
helium at 10 PSI; the injection mode was Each solution was homogeneously
splitless for 2 min and then it was split with distributed on the bottom of the flasks,
a ratio of 1:40; the sample volume injected allowed to evaporate for one hour, and
was 0.2 μL (1.0 mg/ml, ethyl acetate); the then 0.5 g of rearing food were spread in
interface temperature 250 °C, and the each flask. Controls were treated with the
acquisition mass range was 40–700 m/z at solvent alone. The side glass tube for each
70 eV. Mass spectral data were compared Erlenmeyer flask (treated and controlled) was
with the MS instrument library and NIST joined to the other using a rubber tube with a
library. Relative percentages of the major hole in the middle (0.5 cm diameter). Once
components were calculated by integrating the flasks were joined by the rubber tube,
the registered peaks. ten unsexed adults of Tribolium castaneum,
randomly selected, were released carefully
Bioassays in the hole. The hole was covered using a
piece of sello tape to ensure a hermetic seal.
Contact toxicity Each treatment was replicated five times.
From a mother solution (4 mg/ml) four Bioassays were conducted in complete
essential oil solutions were prepared using darkness at 25 ± 1°C and 65 % RH. After 30,
332 Rev. Soc. Entomol. Argent. 68 (3-4): 329-338, 2009
60, 90, 150 and 210 minutes, a Response β-caryophyllene (27.72%), germacrene D
Index (RI) for beetles in the two-choice (13.66%), δ-elemene (10.57%), limonene
bioassays was calculated using RI=(T-C/Tot) (9.73%), patchoulene (9.24%) and
x100, where T is the number of insects in viridiflorol (9.16%) were the most important
the treated flasks; C is the number of insects components. The sesquiterpenes fraction
distributed in the control flasks, and Tot is accounted for 84.97 % of the total oil. The
the total number of insects released. Positive essential oils of E. arnottii showed notable
RIs indicate attraction to the treatment, and compositions because the species was mainly
negative RIs indicate repellency. Values constituted by sesquiterpene compounds.
could theoretically range from -100 for a In these samples, 16 components
complete repellency, to +100 for complete representing 71.40% of the whole oil were
attraction (Phillips et al., 1993). Data were identified. The principal constituents were
analyzed using Two Way ANOVA Test at P≤ (-)-spathunelol (10.57%), germacrene D
0.05. (9.83%), caryophyllene (7.92%), γ-elemene
(5.92%) and (+)-δ-cadinene (5.83%). Finally,
in the essential oil of E. viscidum the main
RESULTS AND DISCUSSION identified constituents were (-)-spathunelol
(25.16%), (-)-δ-cadinol (2.67%), α-santalene
The aim of this work was to investigate (2.53%), β-cubebene (1.64%), (+)-nerolidol
toxic and repellent properties of Eupatorium (1.63%) and germacrene D (1.46%).
buniifolium, E. inulaefolium, E. arnottii and The biological effects of Eupatorium
E. viscidum essential oils against Tribolium buniifolium, E. inulaefolium, E. arnottii, and
castaneum adults. These essential oils E. viscidum essential oils on T. castaneum
contain a variety of terpenoids, although adults were evaluated through two kinds of
one of them (E. viscidum) presented a non- bioassays. Results are shown in Tables II-III.
terpenoid compound (6-methyl-5-hepten-2- The essential oils obtained from
one). The identified constituents and their Eupatorium buniifolium, E. inulaefolium,
composition (percentage), listed in order of and E. arnotti exhibited greater repellent and
elution, are shown in Table I. toxic effects against the T. castaneum adults.
Several of the identified compounds were The essential oils of these species caused
also present in other Eupatorium species 98% of mortality after 24 hs of exposure oil
which grow wild in the Amazon region at 0.212 mg/cm2. High mortality in contac
(Maia et al., 2002). Table I shows a different toxicity test could also be due to the the
composition for each assayed essential presence of constituents such as α-pinene,
oil. However, a set of four compounds limonene, β-cariophilene and germacrene.
was common in all oil samples, namely The toxic effects of E. bunifolium essential
β-caryophyllene (range 1.11-27.72%), oil might be attributed to its major
α-caryophyllene (0.25-5.90 %), germacrene components (mainly α-pinene), as well as
D (0.95-13.66 %), and (-)-spathunelol (0.48- other major and/or trace compounds. A
25.16 %). previous research using Tribolium castaneum
When the essential oil of Eupatorium adults, reported by the same working team,
buniifolium was analyzed, 19 compounds provides clear support for this assumption.
were identified accounting for 92.98 % of the In these experiments, limonene (present in
total oil. The most abundant component was the essential oil under analysis) showed a
α-pinene (50.98 %) with significant amounts bioactivity similar to α−pinene (LD = 1.16
50
of D-limonene (9.63 %) and (+)-sabinene µM/cm2 and LD = 1.12 µM/cm2 at 24 h
50
(7.45 %). β-caryophyllene (5.22%), of exposition, respectively) (García et al.,
(-)-spathunelol (4.93%), and ocimene 2005). Ojimelukwe & Adler (1999) found
(4.78 %) were also present. A total of 21 α-pinene was toxic to Tribolium confusum
compounds were identified representing du Val., and exhibited negative chemotaxis
97.36% of the whole oil of E. inulaefolium. against Periplaneta americana (Ngoh et
LANCELLE, H.G. et al. Chemical composition of four essential oils from Eupatorium 333
Table I. Chemical composition of essential oils of Eupatorium species.
334 Rev. Soc. Entomol. Argent. 68 (3-4): 329-338, 2009
Table II. Contact mortality data of Eupatorium species essential oils on Tribolium castaneum adults at
different times (hours) in a contact toxicity bioassay.
Each value is expressed as mean ± S.E.M from five replicates with 10 adults each (n=50). Means within
a column followed with * are significantly different from the control at P ≤ 0.05.
LANCELLE, H.G. et al. Chemical composition of four essential oils from Eupatorium 335
al., 1998). The antifeedant and growth from aromatic plants. This response might
inhibitory effects of this monoterpene toward be due to an activation of octopaminergic
T. castaneum were observed by Huang et al. receptors by several terpenes (Kostyukovsky
(1998). Taking into account the bioactivity et al., 2002).
of α-pinene toward other insect orders, i.e. In conclusion, contact toxicity bioassays
Lycoriella mali Fitch (Choi et al., 2006), this showed that E. arnottii, E. inulaefolium, and
monoterpene seems to be a non selective E. buniifolium essential oils caused the main
allelochemical. deleterious effect after 24 hs of treatment. The
In the essential oil recovered from dosage of ED demonstrated that the insects
50
Eupatorium inulaefolium the main detected were susceptible at 0.10-0.15 mg/cm2 .
terpenes were β-caryophyllene (27.72 %), In the two-choice bioassays the essential
germacrene (13.66 %), δ-elemene (10.57 oils exhibited repellent activity at the
%), and limonene (9.73 %). The essential oil concentrations tested. However, the biggest
of E. betonicaeforme, which includes in its activity was produced at 0.056 and 0.141 g/
composition the compound β-caryophyllene, cm2 from E. buniifolium and E. inulaefolium
has been reported as larvicidal toward Aedes essential oils (Table III). There were no
egyptii (L) (Albuquerque et al., 2004). In a significant statistical differences between all
previous search of biopesticides using T. concentrations for each essential oil after
castaneum adults, whereas the sesquiterpene 150 minutes of exposure. Remarkably, the E.
germacrene was inactive in both bioassays, buniifolium essential oil showed the highest
the monoterpene limonene showed both concentration of monoterpenes (78.49 %)
insecticidal and repellent bioactivities with a lower concentration of sesquiterpenes
(García et al., 2005). (Table I), and it was the only one revealing the
In our experiments the exposure to E. presence of α-pinene. We have previously
buniifolium and E. inulaefolium essential oils reported the noteworthy repellent and toxic
led to liberation of defensive secretions used activities of this compound toward the insect
by T. castaneum as repellents and irritants here assayed (García et al., 2005). Besides, it
(benzoquinones) (Unruh et al., 1998). The has been observed that α-pinene possesses
presence of these quinones was recognizable important repellent effects toward Tribolium
because the food present in the treated flask confusum du Val (Tapondjou et al., 2005).
acquired a pinkish color, caused by quinone In the test for the two-choice bioassay,
binding in flour to form conjugates with E. viscidum was significantly different in
amino groups (Hodge et al., 1996; García et relation to the most active E. buniifolium (P≤
al., 2005). 0.05). This observation could be ascribed
The essential oil recovered from E. with the fact that its essential oil showed
viscidum, which showed the minor toxic the minor concentration of β-caryophyllene
bioactivity in the first 24 h, did not exhibit and, in addition, α-pinene was absent.
the monoterpenes α-pinene, limonene, and Essential oils obtained from E. inulaefolium
δ-elemene. and E. arnottii induce a notable mortality at
Some authors have suggested that the toxic high doses but with lower repellent activity
activity of essential oils may be attributed than that described for E. buniifolium. These
to a reversible competitive inhibition of results could be explained keeping in mind
acetylcholinesterase by the occupation of some synergistic effects.
hydrophobic site of the enzyme active center Since the structural characteristics
(Tapondjou et al., 2005). In our experiments, of monoterpenoids can influence their
aimed at determining the contact toxicity, insecticidal properties, the degree of
it was possible to observe that the insects penetration into the insect cuticle and the
showed symptoms, including convulsion and ability to move to and interact with an active
tremors followed by paralysis (namely knock- site (Rice & Coats, 1994), the bioactivities
down) (data not shown), similar to those here described cannot be accounted for the
produced by some essential oils isolated major components, and the existence of
336 Rev. Soc. Entomol. Argent. 68 (3-4): 329-338, 2009
Table III. Response Index data of Eupatorium species essential oils on Tribolium castaneum adults at
different times (min) in a two-choice bioassay.
Each data point represents the mean of five replicates with 10 adults each (n=50). Means within a
column followed with * are significantly different from the control at P ≤ 0.05
synergistic effects is possible. ACKNOWLEDGEMENTS
Financial support from CONICET (112-
CONCLUSIONS 200801-00628), UNSL (Project 7301), and
ANPCyT (PICT-2007-00352) is gratefully
In conclusion, this study suggests that acknowledged. Thanks to Lic. Cristina
Eupatorium buniifolium, E. inulaefolium, E. Devia for helping in the statistical analysis.
arnottii, and E. viscidum essential oils may This work is a part of the Doctoral thesis of
act as potential grain protectant due to their H.G.L.
combined contact toxicity and repellency
against Tribolium castaneum. However,
further investigations for the insecticidal
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