Industrial Crops and Products 46 (2013) 158164

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Industrial Crops and Products

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Ar-turmerone from Curcuma longa (Zingiberaceae) rhizomes and effects on

Sitophilus zeamais (Coleoptera: Curculionidae) and Spodoptera frugiperda
(Lepidoptera: Noctuidae)
Wagner de Souza Tavares a , Silvia de Sousa Freitas b , Geisel Hudson Grazziotti b ,
Leila Maria Leal Parente c , Luciano Morais Lio d , Jos Cola Zanuncio e,
a

Departamento de Fitotecnia, Universidade Federal de Vicosa, 36570-000, Vicosa, Minas Gerais State, Brazil
Departamento de Qumica, Universidade Federal de Gois, 75704-020, Catalo, Gois State, Brazil
c
Departamento de Patologia, Universidade Federal de Gois, 74001-970, Goinia, Gois State, Brazil
d
Instituto de Qumica, Universidade Federal de Gois, 74001-970, Goinia, Gois State, Brazil
e
Departamento de Biologia Animal, Universidade Federal de Vicosa, 36570-000, Vicosa, Minas Gerais State, Brazil
b

a r t i c l e

i n f o

Article history:
Received 15 June 2012
Received in revised form 22 October 2012
Accepted 12 January 2013
Keywords:
Antifeedant
Contact
Fall armyworm
Maize weevil
Nutritional indexes
Repellence
Turmeric

a b s t r a c t
Turmeric, Curcuma longa L. (Zingiberaceae) has well-known insecticidal and repellent effects on insect
pests, but its impact on the Maize weevil Sitophilus zeamais Motschulsky, 1855 (Coleoptera: Curculionidae) and the fall armyworm Spodoptera frugiperda J.E. Smith, 1797 (Lepidoptera: Noctuidae) is unknown.
In this study, we evaluated the insecticidal and repellent effects of ar-turmerone, extracted from rhizomes
of C. longa, on the S. zeamais and S. frugiperda. Individuals of S. zeamais died after six days of contact with
ar-turmerone at 1% (m m1 ), while individuals of S. frugiperda showed a 58% mortality rate after ingestion
of this compound at 1% (m v1 ). The width of head capsule, and length and weight of body of surviving
S. frugiperda caterpillars exposed to ar-turmerone were 60.0, 59.6 and 93.8% lower than those of control
caterpillars, respectively. Dry weight of ingested food, feces produced, weight gain and dry weight of food
assimilated and metabolized by surviving S. frugiperda caterpillars were lower with articial diet with
ar-turmerone. Hatching of caterpillars from newly laid, 1- or 2-day-old S. frugiperda eggs was 48.6, 14.2
and 48.5%, respectively. Ar-turmerone is highly toxic to S. zeamais and S. frugiperda at low doses.
2013 Published by Elsevier B.V.

1. Introduction
Persistent, broad-spectrum insecticides can be toxic to nontarget organisms and also cause environmental damage (Viana
et al., 2009; Tavares et al., 2010a; Castro et al., 2012). Furthermore,
they can result in the evolution of resistant individuals, necessitating research into new substances with insecticidal activity and new
methods of controlling insect pests; for example, several studies
have examined the antifeedant and repellent activity of molecules
from plants of the Cerrado (Savanna-type) biome of Brazil (Pereira
et al., 2002; Tavares et al., 2009, 2011).
Turmeric, Curcuma longa L. (Zingiberaceae) is an herbaceous
perennial and with long lateral ramications that originated in
Southeast Asia, probably from India (Sharma et al., 2011). Turmeric
powder is extracted from the dried ground rhizomes and has many
culinary uses (Hammerschmidt, 1997; Palaniswamy, 2001; Tilak
et al., 2004). Compounds formed by the plant also have antioxidant,

Corresponding author. Tel.: +55 31 3899 2924; fax: +55 31 3899 4012.
E-mail address: zanuncio@ufv.br (J.C. Zanuncio).
0926-6690/$ see front matter 2013 Published by Elsevier B.V.
http://dx.doi.org/10.1016/j.indcrop.2013.01.023

antibacterial, anti-inammatory, analgesic and digestive properties, and some are currently being investigated as treatments for
cancer, Alzheimers disease and liver problems (Chattopadhyay
et al., 2004; Ali et al., 2006; Mariyappan and Vijayaragavan, 2007).
The fresh juice, water extracts and essential oils of C. longa also
show insecticidal activity against insect pests and act as mosquito
repellents (Iqbal et al., 2010a; Sukari et al., 2010; Damalas, 2011). C.
longa is harvested when the aerial part is lost after owering and its
rhizomes are an intense yellow, possibly indicating the presence of
more concentrated pigments (Bambirra et al., 2002; Hossain, 2010).
Genetic factors, harvesting time, individual plants, soil type, fertilization, time of collection, mode of drying the plant material,
storage period and environmental factors all affect the chemical
composition and the content of essential oils from C. longa rhizomes (Bansal et al., 2002; Chane-Ming et al., 2002; Naz et al., 2011).
The composition and volatility of C. longa essential oils determine
the characteristic smell of turmeric, whereas xed phenolic compounds, such as curcumin and its derivatives, are responsible for
the intense yellow color of the rhizomes. Volatile essential oils of C.
longa contain a mixture of ketones and sesquiterpene alcohols, the
latter being mainly of a form of germacrene and bisabolane (Zhang
et al., 2008; Li et al., 2010; Xiao et al., 2011).

W.d.S. Tavares et al. / Industrial Crops and Products 46 (2013) 158164

The Maize weevil Sitophilus zeamais Motschulsky, 1855

(Coleoptera: Curculionidae) is a serious pest of grain crops, both in
the eld and in storage units, where it can lead to cross-infestation
(Tigar et al., 1994; Demissie et al., 2008; Vazquez-Castro et al.,
2009). Larvae and adults of this pest damage whole and healthy
grains, including oat Avena sativa L., barley Hordeum vulgare L., rice
Oryza sativa L., rye Secale cereale L., wheat Triticum aestivum L. and
corn Zea mays L. (Poaceae) (Lale and Yusuf, 2000; Ukeh et al., 2010).
The weevil lays its eggs within the grain, where the larvae then
develop (Larrain et al., 1995). Detrimental effects result from the
reduced weight and poorer physical and physiological quality of
the infected grains, which result mainly from the additional effect of
deterioration agents (microorganisms) (Hell et al., 2000). Because
the larvae develop inside the grain, it is difcult to use insecticides
against this pest; therefore, they are a promising system to use to
study the effect of alternative repellent substances (Huang et al.,
2011).
The fall armyworm Spodoptera frugiperda J.E. Smith, 1797 (Lepidoptera: Noctuidae) is a major corn pest in Brazil (Cruz et al., 1999;
Senna et al., 2003; Tavares et al., 2010b). Caterpillars of S. frugiperda
rst feed on the remains of their eggshells, where they stay undisturbed for 1012 h, at which point they begin to feed on the green
and succulent tissues of the plant, leaving the membranous epidermis intact (Barros et al., 2010). Fresh droppings indicate the
presence of caterpillars inside the maize cartridge (Busato et al.,
2004). Maize is more sensitive to S. frugiperda 4045 days following
germination. Pesticides and insecticides can only be applied when
approximately 20% of the plants are affected and the caterpillars
are 1012 mm long to reduce any adverse effects on natural enemies of this species (Figueiredo et al., 1999). Contact insecticides
are effective against the eggs and young S. frugiperda caterpillars
on the outside of the plant, whereas compounds with antifeedant
properties are more effective against caterpillars within the plant
(Adamczyk et al., 1999; Al-Sarar et al., 2006; Blessing et al., 2010).
The objective of the current study was to identify the compound
ar-turmerone, extracted and puried from C. longa rhizomes and to
determine its insecticidal and repellent effects on S. zeamais and S.
frugiperda.
2. Material and methods
2.1. Experimental procedures
1 H, 13 C,

HSQC and HMBC NMR measurements were carried out

on a Bruker Avance III 500 instrument (operating at 500.13 MHz
for 1 H) equipped with a 5 mm triple Resonance broadband inverse
probehead (TBI) with Z-gradient. CDCl3 was used as solvent and
tetramethylsilane (TMS) as the internal standard. Mass spectra
were obtained by gas chromatography coupled to a mass spectrometry (GCMS). The GCMS analyzes were performed using a gas
chromatograph [GC-17A Shimadzu, GCMS/QP5,000 Shimadzu,
DB-5 column (30 mm 0.32 mm)], with ionization by electronic
impact, under the following conditions: 60 C for 3 min; 5 C/min to
240 C, for 8 min; with an injector temperature of 180 C, a detector
temperature of 260 C and an injection volume of 1 L. Mass spectra were compared with the National Institute of Standards and
Technology database 62 (NIST-62).
2.2. Trial sites
The toxicity of C. longa to S. frugiperda was evaluated in the Laboratory of Insect Rearing (LACRI) of the National Research Center for
Maize and Sorghum (EMBRAPA) in Sete Lagoas, Minas Gerais State,
Brazil at 24 2 C, 70 5% relative humidity and a 12-h photoperiod. A population of S. frugiperda has been maintained at the LACRI

159

for approximately 15 years and its caterpillars are fed on an articial diet composed of 1 L water, 59.3 g wheat germ (T. aestivum),
38 g yeast extract, 3.82 g ascorbic acid, 1.23 g sorbic acid, 1.3 mL
propionic acid, 0.131 mL phosphoric acid, 2.36 g methyl paraben
(Nipagin), 123.6 g bean [Phaseolus vulgaris L. (Fabaceae)], 15.35 g
agar and 3.1 g formaldehyde (Tavares et al., 2009).
Toxicity and repellence tests of C. longa on S. zeamais were performed in the Laboratory of Natural Products and Environment
(LPNMA) of the Chemistry Department (DQ) of the Federal University of Gois (UFG) in Catalo, Gois State, Brazil. The insects
were collected on a farm in Catalo where no synthetic chemicals
are used. The insects were reared for ve generations at 25 3 C
in 3 L glass pots on Z. mays var. everta (Sturtev.) L.H. Bailey without
residues of synthetic chemical products.
2.3. Plant material
Rhizomes of C. longa were collected from a commercial crop
grown on the Macaba farm, Catalo, Gois State, Brazil (18 08 S,
47 57 W, 515 m above sea level). The farm uses no synthetic chemical products.
2.4. Extraction and structural characterization of ar-turmerone
Rhizomes of C. longa were air-dried in a chamber at 40 C for
three days and ground into a ne reddish-yellow powder. The
powder was extracted by steeping in hexane freshly distilled at
3 25 C with occasional stirring for a period of 6 h. The plant
material:hexane ratio was 500 g rhizomes per 1000 mL hexane.
The solution obtained was ltered and the solvent recovered in
a rotary evaporator under low pressure, yielding a light-yellow
oil. The oil was separated by column chromatography on silica
gel (Vetec, 60270 mesh), eluting with hexane:ethyl acetate (9:1).
The fractions of interest were analyzed by thin-layer chromatography (0.20 mm thickness, 60-mesh silica gel; Macherey-Nagel) and
revealed with iodine vapor (sublimation) with a previously isolated
and identied standard.
2.5. Repellence of S. zeamais by ar-turmerone
The repellent activity of ar-turmerone against S. zeamais was
evaluated in ve arenas of ve circular plastic pots (6 cm diameter 2.1 cm height). The central pot of each arena, with a diameter
sufcient to allow the passage of the insects, was interconnected
symmetrically to the other pot with plastic tubes. Grains of Z. mays,
without residues of synthetic chemicals and harvested at the UFG
farm, were mixed with ar-turmerone whereas control grain was
untreated; the grains were put in two diagonally opposite pots
within the arena. Thirty non-sexed adults of S. zeamais that had
been without food for 24 h were released into the central pot and,
after 24 h, the total number of individuals per pot was counted.
The data were analyzed using the preference index (PI), as follows: PI = %TPI%tpI/(%TPI + %tpI), where %TPI is the percentage of
insects in the treatment pot and %tpI is the percentage of insects
in the control pot. The compound is considered repellent with a
PI of between1.00 and0.10; neutral, between0.10 and 0.10 and
attractive between 0.10 and 1.00 (Iqbal et al., 2010b; Fouad et al.,
2011).
The repellent activity of ar-turmerone against S. zeamais was
performed using 10, 20, 30, 40 and 50 L of ar-turmerone per 20 g
Z. mays grains with ve replications, each one with an arena and 30
insects released. The containers with the corn grains were stored
and, after 15, 30 and 45 days, the residual repellent effect was evaluated. The arrangement was factorial. The PI values were submitted
to an analysis of variance (ANOVA) and the means compared by F

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W.d.S. Tavares et al. / Industrial Crops and Products 46 (2013) 158164

test (P < 0.05) using the program BioEstat5.0 (Supplier: UFG) (Ayres
et al., 2007).
2.6. Mortality of S. zeamais resulting from ar-turmerone
Plastic arenas (6 cm diameter 2.1 cm height) were hermetically sealed and lled with 20 g Z. mays grains that had been
harvested from the UFG farm without any chemical residues.
Twenty non-sexed S. zeamais adults that had been without food
for 24 h were placed in each arena. The assay was performed with
ve replications with 0.1% and 1% (m m1 ) of the essential oil (pure
ar-turmerone) on corn grains; control grains had no oil added (0%).
The experiment was evaluated over 15 days by counting the total
number of dead insects per arena after 3, 4 and 15 days from the
start of the experiment. The efcacy of the concentrations of arturmerone was obtained by correcting the insect mortality (Abbott,
1925).
Individuals of S. zeamais were weighed before starting the experiment and after 7 and 15 days. Surviving insects were weighed to
obtain the feeding inhibitory activity of ar-turmerone. The arrangement was factorial. The data were submitted to an ANOVA and the
means compared by F test (P < 0.05) using the program BioEstat5.0
(Supplier: UFG) (Ayres et al., 2007).
2.7. Hatching of S. frugiperda caterpillars from eggs treated with
ar-turmerone
Sheets of white A4 paper, used as oviposition sites in the rearing
cages, with newly deposited, 1- or 2-day-old S. frugiperda eggs were
cut up and ve pieces of paper each containing 20 eggs were used
per experimental group. An 8-g cube of solid articial diet (Tavares
et al., 2009) was placed in plastic 50-mL cups, to which a group
with 20 eggs was added. Ar-turmerone was diluted (1% in acetone,
m v1 ) and 50 L of this solution applied using a manual volumetric
pipette to the groups of S. frugiperda. The egg groups were left for
4 h at 24 2 C to evaporate the acetone and the cups were then
sealed with a transparent acrylic cover. The control pot had only
50 L acetone added. The number of caterpillars that had hatched
was counted 4 days following application of the solution.
The design was entirely randomized with ve replications, each
one with a group of 20 S. frugiperda eggs. The data of mortality of
caterpillars were corrected (Abbott, 1925), submitted to an ANOVA
and the means compared with the MannWhitney test (P < 0.05)
using the program BioEstat5.0 (Supplier: UFG) (Ayres et al., 2007).
2.8. Intake of ar-turmerone by S. frugiperda
Eight grams of a liquid articial diet suitable for S. frugiperda
(Tavares et al., 2009) were placed per 50-mL plastic cup and left to
dry for 24 h. Ar-turmerone was diluted in acetone at 1% (m v1 ) and
100 L of this solution was added to the diet in each cup. The cups
were left at 24 2 C for 4 h to evaporate the acetone. A single 1day-old S. frugiperda caterpillar was added to each cup. The control
cup had only 100 L acetone added. The design was entirely randomized with 24 replications, with one caterpillar of S. frugiperda
per replication. The effects of ar-turmerone were evaluated after
10 days from the beginning of the experiment and the mortality of
the caterpillars corrected (Abbott, 1925).
Surviving S. frugiperda caterpillars with 11-days-old were then
killed in 70% ethanol so that the width of the head capsule, and
their overall length and weight could be measured. The data were
analyzed using an ANOVA and the means compared with the
MannWhitney test (P < 0.0001) using the program BioEstat5.0
(Supplier: UFG) (Ayres et al., 2007).

2.9. Nutritional indexes of S. frugiperda

Dead caterpillars from assay 2.8, feces produced and remains
of articial diet were placed in an oven at 5560 C until constant
weight. Weight of food consumed and weight gain by caterpillars
were obtained. Body mass of caterpillars was discarded (considered
zero) for being too low. Weight at the nal of feeding period (T) was
recorded to determine weight gain (P) of caterpillars.
Ten plastic 50-mL cups with articial diet and no caterpillars
were separated to obtain the initial dry weight of the diet (Af) to
calculate consumption indexes and food utilization.
The quantitative nutrition indexes of caterpillars were obtained
with the parameters: T, duration of the feeding period (days); Af,
weight of food provided to insects (g); Ar, weight of food remains
after insect feeding (g) after T; F, weight of feces produced (g) during
mean weight of
T; B, weight gain of caterpillars (g) during T; B,
caterpillars (g) during T; I, weight of food ingested (g) during T;
IF, food assimilated (g) during T and M = (IF)B, food metabolized
during the feeding period.
The consumption and utilization indexes of food were determined with the formulas: relative rate of consumption (g/g/day)
(RCR) = I (B T ); rate of relative growth (g/g/day) (RGR) = B
(B T ); relative metabolic rate (g/g/day) (RMR) = M (B T );
digestibility approximate (%) (AD) = [(I F) I] 100; efciency
of conversion of food ingested (%) (ECI) = (B I) 100; efciency
of conversion of food ingested (%) = 100 ECD and metabolic cost
(%) = 100 ECD (Waldbauer, 1968; Scriber and Slansky Junior,
1981).
The design was entirely randomized with a caterpillar per
replication. The data were analyzed with ANOVA and the means
compared with the MannWhitney test (P < 0.0001) with the program BioEstat5.0 (Supplier: UFG) (Ayres et al., 2007). Data were

transformed to x + 0.5 whenever necessary.

3. Results and discussion

The extraction yield of C. longa essential oil with hexane was
0.39% (m m1 ) (1.93 g) and the yield of ar-turmerone obtained
from this essential oil was 82% (m m1 ) after the chromatographic
separations from starting material (1.58 g). These values indicate
that 3.2 g of ar-turmerone is present per 1000 g rhizomes of this
plant grown in Catalo, Gois State, Brazil. High percentages of
ar-turmerone in nonpolar extracts and essential oils of C. longa
have also been reported from China, India, Nigeria, Pakistan and
the islands of So Tom and Prncipe (Martins et al., 2001; Raina
et al., 2005; Qin et al., 2007; Ajaiyeoba et al., 2008). The quantitative and qualitative composition of secondary metabolites depends
on genetic factors and on the environmental conditions of the area
where the plant is grown, with variations in the essential oils of C.
longa occurring at different localities (Bansal et al., 2002; ChaneMing et al., 2002; Naz et al., 2011). C. longa can be cultivated at low
cost and sustainable in Brazil using familiar manpower, period of
plantation and spacing adequate and organic fertilization with 50
t of cattle manure per ha (Sigrist et al., 2011).
The NMR spectroscopy of the puried oil suggest an ,unsaturated ketone structure with a para-disubstituted aromatic
ring (Table 1). The 1 H NMR spectrum showed signals of aliphatic
hydrogens at 1.85 (d, J = 1.3 Hz, 3H) and 2.10 (d, J = 1.3 Hz, 3H),
compatible with methyl attached to unsaturated carbon to carbonyl group and signs at 1.23 (d, J = 1.3 Hz, 3H) and 3.28 (ddq,
J = 8.1, 6.9, 6.3 Hz, 1H), referring to a methyl linked to a benzylic
methine group. A singlet in 2.30 (s, 3H) indicate a methyl attached
to the aromatic ring (Table 1). Double doublets at 2.60 (dd,
J = 15.61, 8.1 Hz) and 2.70 (dd, J = 5.61, 6.3 Hz) compatible with
diastereotopic CH2 neighboring of carbonyl and methine groups,

W.d.S. Tavares et al. / Industrial Crops and Products 46 (2013) 158164

161

Table 1
1
H and 13 C NMR spectral data for ar-turmerone in CDCl3 .

Position

1 H (multiplicity, J Hz)

13 C

Position

1 H (multiplicity, J Hz)

13 C

1
2
3
4
5a
5b
6
7

2.10 (d, 1.3)

6.02 (sept, 1.3)

2.60 (dd, 15.61; 8.1)

2.70 (dd, 15.61; 6.3)
3.28 (ddq, 8.1; 6.9; 6.3)
1.23 (d, 1.3)

20.7
155.1
124.1
199.5
52.7
52.7
35.4
21.9

8
9
10
11
12
13
14
15

1.85 (d, 1.3)

7.09 (m)
7.09 (m)

7.09 (m)
7.09 (m)
2.30 (s)

27.4
143.7
126.7
129.1
135.2
129.1
126.7
20.9

H and 13 C NMR assignments are based on 1 H, HSQC and HMBC spectra.

Table 2
Residual repellent activity (mean standard error of the value of preference index) of ar-turmerone on Sitophilus zeamais (Coleoptera: Curculionidae) during 45 days.
Day

10 L

1
15
30
45

0.323
0.485
0.196
0.224

20 L

0.145
0.059
0.175
0.174

0.351
0.456
0.148
0.179

30 L

0.153
0.172
0.162
0.025

0.468
0.209
0.145
0.270

40 L

0.269
0.232
0.238
0.155

0.189
0.272
0.136
0.184

50 L

0.279
0.245
0.087
0.173

0.173
0.210
0.207
0.141

0.165
0.088
0.202
0.080

Means between the solutions of ar-turmerone, within each line per storage period, do not differ by the F test (P < 0.05) of the ANOVA.

suggests that the aliphatic part is a bisabolane-type sesquiterpene

(Table 1). This carbon skeleton was corroborated by the olenic
and -carbonyl hydrogen signal at 6.02 (septet, J = 1.3 Hz, 1H) and
the multiplet in aromatic region. The HSQC and HMBC correlation
spectra and peaks [m/z 55 (C4 H7 + ); m/z 83 (C5 H7 O+ , 100%); m/z
119 (C9 H11 + )], supported the proposed structure. The data are in
agreement with Lee et al. (2001).
Ar-turmerone showed repellent activity against S. zeamais during the 45-day period of exposure as shown by the PI values
(Table 2). The PI values of 0.087 (50 L, 30 days) to 0.485 (10 L,
15 days), negatives and <0.1, characterized the compound as
being a repellent, except for the 50 L concentration during the 30day exposure period (0.087 0.202), considered neutral (Table 2).
The multivariate statistical analysis (ANOVA, F test, P < 0.05) as
function of the concentration and application time showed similarity between treatments, characterizing the ar-turmerone as a
powerful natural repellent, even at low concentrations (10 L per
20 g corn grain) (Table 2). The repellence of S. zeamais by PI suggests
that ar-turmerone could be used in integrated management of this
pest in stored grain, with only 5 g of this compound required per
ton of corn. The insecticide and repellent activity of aromatic plants
of the Zingiberaceae family [alligator pepper Aframomum melegueta
(Rosk) K. Schum, joint-whip ginger Alpinia conchigera Griff, zedoary
Curcuma zedoaria (Berg.) Roscoe, ginger Zingiber ofcinale (Roscoe)
and shampoo ginger Zingiber zerumbet Smitt] and their essential
oils have been tested with success against S. zeamais in stored grains
(Ukeh et al., 2010; Suthisut et al., 2011). The repellent activity of
essential oils of C. longa was demonstrated against the red our
beetle Tribolium castaneum Herbst, 1797 (Coleoptera: Tenebrionidae) (Iqbal et al., 2010b) and the housey Musca domestica L., 1758
(Diptera: Muscidae) (Kumar et al., 2011). The turmerones and arturmerone of C. longa are known repellents (Zhang et al., 2008;
Li et al., 2010; Xiao et al., 2011). Essential oils from C. longa rhizomes repelled T. castaneum (Chander et al., 2000; Tripathi et al.,

2002) and a nonpolar extract in acetone, petroleum, ether and

chloroform of this plant repelled the rice weevil Sitophilus oryzae
L., 1763 (Coleoptera: Curculionidae) and the lesser grain borer
Rhyzopertha dominica F., 1792 (Coleoptera: Bostrychidae) (Matter
et al., 2008). The repellence of essential oils from plant products
with insecticide properties [e.g. Surinam cherry Eugenia uniora L.,
1753 (Myrtaceae), eugenol of clove Syzygium aromaticum (L.) Merrill & Perry (Myrtaceae), green fruits of the Brazilian pepper-tree
Schinus terebinthifolius Raddi, 1820 (Anacardiaceae), marigold pepper Piper marginatum L. (Piperaceae), boldo Peumus boldus Molina
(Monimiaceae), Piper hispidinervum C. DC. (Piperaceae), cajuput
tree Melaleuca leucadendron L. (Myrtaceae), orange peel and lime
plants (Rutaceae)] showed a low residual effect on S. zeamais, especially under sunlight because of the effects of UV (Betancur et al.,
2010; Coitinho et al., 2010). Essential oil of cardamom Elettaria cardamomum Maton. (Zingiberaceae) at high concentrations, reduced
the feeding preference of S. zeamais and T. castaneum (Huang
et al., 2000). The essential oil of C. longa at higher concentrations
(165 mg/g) had antifeedant activity against S. oryzae (Tripathi et al.,
2002).
The weight of individuals of S. zeamais was similar between
treatments across a 15-day period. Thus, the C. longa essential oil
showed no antifeedant activity on this insect (Table 3).
The mortality of S. zeamais with ar-turmerone at 1% (m m1 )
was 100% in only 6 days and 50% with a concentration of 0.1%
after 15 days of exposure (Table 4). The mortality of S. zeamais
with ar-turmerone at 1% and 0.1% (m m1 ) increased with the
higher concentration of this essential oil, although the oil had no
antifeedant activity on S. zeamais. The mortality of adult S. zeamais
resulted from ingestion of the compound by the insect, suggesting a toxic effect of ar-turmerone on S. zeamais. The mortality
of R. dominica was 83.3% with extract of C. longa in acetone, but
this product was not effective against S. oryzae, resulting in only a
low mortality (20.4%) at a concentration of 4% in petroleum ether,

Table 3
Weight (g) (mean of survival individuals standard error of mean) of adults of Sitophilus zeamais (Coleoptera: Curculionidae) after insecticidal activity of ar-tumerone during
15 days.
Day

Control

Control solvent

1%

0.1%

0
7
15

0.0025 3.16E05
0.0025 4.90E05
0.0025 3.74E05

0.0025 0.00002
0.0023 5.83E05
0.0024 3.74E05

0.0025 8.6E05
NC
NC

0.0025 3.16E05
0.0024 5.83E05
0.0023 7.07E05

Means between the treatments, within each line per activity period of ar-turmerone, do not differ by the F test (P < 0.05) of the ANOVA. NC = not counted.

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W.d.S. Tavares et al. / Industrial Crops and Products 46 (2013) 158164

Table 4
Dead individuals (mean standard error of mean) of Sitophilus zeamais (Coleoptera: Curculionidae) after treatment with ar-turmerone and efcacy (Ea ) (%) for the concentrations of ar-turmerone.
Day

Control

Control solvent

1%

E%a

0.1%

E%a

3
7
15

0.2 0.4
0.4 0.5
5.4 5.8

0.0 0.0
1.8 1.8
7.0 4.7

01.0 1.20
20.0 0.00
20.0 0.00

03.99
97.98
72.73

00.6 0.50
05.0 3.10
10.0 6.30

01.99
22.98
22.73

Abbott (1925).

Table 5
Number of caterpillars (mean standard error of mean) of Spodoptera frugiperda
(Lepidoptera: Noctuidae) hatched after treatment with ar-turmerone at 1% and
efcacy (Ea ) (%) by eggs age.
Day

P valueb

Mean standard error of mean

0
Control
1
Control
2
Control

0.0081

02.8
12.6
00.6
03.6
00.8
10.6

a
b

0.0586
0.0045

E%a

1.46
2.38
0.60
2.20
0.80
1.88

48.63
00.00
14.18
00.00
48.53
00.00

Abbott (1925).
MannWhitney, P < 0.05, BioEstat 5.0.

although it had a greater effect (90.8%) on R. dominica (Matter et al.,

2008).
Ar-turmerone reduced the hatching rate of caterpillars from
newly laid, 1- or 2-day-old S. frugiperda eggs to 77.77, 83.33 and
92.45%, respectively (Table 5). The treatment with ar-turmerone at
1% resulted in lower hatching rates than in the control, except for
1-day-old eggs (MannWhitney test, P < 0.05) (Table 5). The hatching rate of S. frugiperda caterpillars shows a lower susceptibility of
older eggs to ar-turmerone, which might be the result of the thicker
outer membrane of the egg at this stage, which is formed mainly
of lipids (Tavares et al., 2009). Therefore, ar-turmerone could be
used as a means of controlling the hatching of S. frugiperda eggs,
thus reducing the impact of the caterpillars on crops (Tavares et al.,
2010a, 2010b, 2011). Ar-turmerone crosses this outer egg membrane because of its lipophilic character, with a similar percentage
of caterpillars hatching from newly laid or 1-day-old S. frugiperda
eggs. Thus, ar-turmerone could be a promising agent for the control
of S. frugiperda.
The ar-turmerone caused a 58.3% mortality of S. frugiperda
caterpillars (Table 6). At 100 g/caterpillar (0.1 mL in solution
of 1% of ar-turmerone) the compound reduced the development
of this insect (Table 6). The diameter of the head capsule of S.
frugiperda that had been exposed to ar-turmerone was reduced
in 60% of caterpillars compared with control (0.099 and 0.245 cm,
respectively) (Table 6). The length of caterpillars was reduced in
59.6% (0.59 and 1.46 cm, respectively) and the weight in 93.8%
(3.2 103 and 52.2 103 g, respectively) in comparison with
controls (Table 6). The lower values of the biological parameters of
Table 6
Biological parameters (mean standard error of mean) and efcacy (Ea ) (%) of the
intake activity of ar-turmerone by Spodoptera frugiperda (Lepidoptera: Noctuidae)
in articial diet.

Efcacy (%)a
Width of head capsule (mm)
Body weight (mg)
Body length (mm)

Ar-turmerone

Control

58.33
0.99 0.420 a
3.20 0.766 a
5.90 0.520 a

00.00
02.45 0.14 b
52.20 5.80 b
14.60 0.75 b

Means followed by the same low letter per line do not differ by the MannWhitney
test, P < 0.0001, BioEstat 5.0.
a
Abbott (1925).

caterpillars exposed to ar-turmerone conrm the high toxicity of

this compound to S. frugiperda and the fact that, although not lethal,
it can reduce the development and so the damage and number of
offspring produced by this insect. Individuals descended from those
that ingested ar-turmerone showed developmental abnormalities,
slower development and were generally weaker; therefore, they
are more likely to be easy prey. The supply of C. longa leaf extracts
reduced by 69% the weight of caterpillars of cotton bollworm Helicoverpa armigera Hbner, 1805 (Lepidoptera: Noctuidae) (Kathuria
and Kaushik, 2006). The pupal progeny of the y Bactrocera zonata
Saunders, 1841 (Diptera: Tephritidae) were reduced in 67.90, 60.74
and 51.96% of treatments with extracts of C. longa at 1000, 500
and 250 ppm and the adult mortality in 84.68, 79.03 and 67.74%,
respectively (Siddiqi et al., 2011).
Feeding nutritional indexes of survival caterpillars showed inhibition of S. frugiperda growth in the treatments with ar-turmerone
applied on the articial diet (Table 7). The dry weight of food
ingested, feces produced, weight gain and dry weight of food
assimilated and metabolized were lower for caterpillars fed with
ar-turmerone. Moreover, the parameters RCR, RMR, RGR, AD, ECI,
ECD and metabolic cost were similar between treatments, which
may be due to the low number of caterpillars evaluated and
larva period studied (1- to 11-day of larva period). The evaluation of RCR indicated that antogenins from Annona cherimoya
Mill. (Annonaceae) were not antifeedant, but squamocin from this
plant reduces the efciency to convert food into biomass by S.
frugiperda caterpillars (Colom et al., 2007). The botanical insecticide rotenone showed non-lethal post-ingestive effects on the
digestion/absorption of food and on its conversion to biomass by
S. frugiperda caterpillars. This suggests relative resistance of this
insect to this insecticide (Wheeler et al., 2001).

Table 7
Dry weight of food ingested (g), feces produced (g) and weight gain (g); dry weight
of food assimilated (g) and metabolized (g); larva period studied (days); relative
consumption rate (RCR) (g/g/day), relative metabolic rate (RMR) (g/g/day), relative growth rate (RGR) (g/g/day), approximate digestibility (AD) (%), conversion
efciency of ingested food (ECI) (%), conversion efciency of ingested food (ECD)
(%) and metabolic cost (100ECD) of survival Spodoptera frugiperda (Lepidoptera:
Noctuidae) caterpillars fed with articial diet treated or not with ar-turmerone.
Parameters evaluated

Articial diet with

ar-turmerone

Articial diet without

ar-turmerone

Food ingested
Feces produced
Weigh gain
Food assimilated
Food metabolized
Larva period studied
RCR
RMR
RGR
AD
ECI
ECD
100ECD

0.019 4.725E04 b
0.010 3.226E04 b
3.253E03 1.162E04 b
8.900E03 9.536E04 b
5.647E03 8.057E04 b
11
0.537 0.016 a
0.160 0.017 a
0.092 0.002 a
47.090 1.236 a
17.212 0.291 a
36.551 3.156 a
63.449 3.156 a

0.308 7.700E03 a
0.165 5.323E03 a
0.053 1.893E03 a
0.143 0.015 a
0.090 0.012 a
11
0.536 0.015 a
0.157 0.016 a
0.092 0.002 a
46.429 1.225 a
17.208 0.288 a
37.063 3.162 a
62.937 3.162 a

Mean standard error of the mean. Means followed by the same low letter per line
do not differ by the MannWhitney test, P < 0.0001, BioEstat 5.0.

W.d.S. Tavares et al. / Industrial Crops and Products 46 (2013) 158164

4. Conclusions
The ar-turmerone is highly toxic to S. zeamais and S. frugiperda
at low doses. This sesquiterpene has signicant repellent action
against S. zeamais and can persist in the environment for 45 days at
a dose of 10 L per 20 g corn grain. Therefore, ar-turmerone could
be a lower cost and sustainable alternative in Brazil for integrated
pest management of these species.
Dedication
To Professor Fernando Petacci (Chemistry Department, Federal
University of Gois in Catalo, Gois State, Brazil) that died on June
15, 2012 and Professor Srgio de Freitas (Faculty of Agriculture and
Veterinary Sciences, Paulista Estadual University Jlio de Mesquita
Filho in Jaboticabal, So Paulo State, Brazil) that died on February
21, 2012. Our sincere feelings.
Acknowledgements
To Dr. Ivan Cruz (EMBRAPA Maize and Sorghum in Sete Lagoas,
Minas Gerais State, Brazil) for providing logistical support. To Dr.
Aristnio Magalhes Teles (Institute of Biological Sciences General Biology Department Federal University of Gois in Goinia,
Gois State, Brazil) to identify C. longa (Zingiberaceae). To M.Sc.
Amauri Alves de Souza Jnior (Institute of Chemistry Paulista
Estadual University Jlio de Mesquita Filho in Araraquara, So
Paulo State, Brasil) for help in conducting the experiments. To
Macaba farm, Catalo, Gois State, Brazil by C. longa rhizomes.
To Conselho Nacional de Desenvolvimento Cientco e Tecnolgico (CNPq), Coordenaco de Aperfeicoamento de Pessoal de
Nvel Superior (CAPES) and Fundaco de Amparo Pesquisa do
Estado de Gois (FAPEG) for grants. This research project (Notice:
01/2011Universal Demand) was supported by the Fundaco de
Amparo a Pesquisa do Estado de Minas Gerais (FAPEMIG). The
English of this manuscript has been revised and edited by Asia
Science Editing of Republic of Ireland.
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