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Industrial Crops and Products 46 (2013) 158–164

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Industrial Crops and Products

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 Ar -turmerone from Curcuma longa (Zingiberaceae) rhizomes and effects onSitophilus 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 Lião d, José Cola Zanuncio e,∗

a Departamento de Fitotecnia,Universidade Federal de Vicosa, 36570-000, Vicosa, Minas Gerais State, Brazilb Departamento de Química, Universidade Federal de Goiás, 75704-020, Catalão, Goiás State, Brazilc Departamento de Patologia, Universidade Federal de Goiás, 74001-970, Goiânia, Goiás State, Brazild Instituto de Química, Universidade Federal de Goiás, 74001-970, Goiânia, Goiás State, Brazile

Departamentode Biologia Animal, UniversidadeFederal de Vicosa, 36570-000, Vicosa, Minas Gerais State, Brazil

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

RepellenceTurmeric

a b s t r a c t

Turmeric, Curcuma longa L. (Zingiberaceae) has well-known insecticidal and repellent effects on insectpests, but its impact on the Maize weevil Sitophilus zeamais Motschulsky, 1855 (Coleoptera: Curculion-

idae) and the fall armyworm Spodoptera frugiperda J.E. Smith, 1797 (Lepidoptera: Noctuidae) is unknown.In thisstudy, 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. zeamaisdied after six days of contact withar -turmerone at 1% (m m−1), while individuals of S. frugiperda showed a 58% mortality rate after ingestion

of this compound at 1% (m v−1). The width of head capsule, and length and weight of body of survivingS. 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 foodassimilated and metabolized by surviving S. frugiperda caterpillars were lower with artificial diet with

ar -turmerone. Hatching of caterpillars from newly laid, 1- or 2-day-old S. frugiperda eggs was 48.6, 14.2and 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 non-

target organisms and also cause environmental damage (Vianaet al., 2009; Tavares et al., 2010a; Castro et al., 2012). Furthermore,they can result in the evolution of resistant individuals, necessitat-ingresearchinto newsubstances with insecticidal activity andnew

methods of controlling insect pests; for example, several studieshave examined the antifeedant and repellent activity of moleculesfrom plants of the Cerrado (Savanna-type) biome of Brazil (Pereiraet al., 2002; Tavares et al., 2009, 2011).

Turmeric, Curcuma longa L. (Zingiberaceae) is an herbaceousperennial and with long lateral ramifications that originated inSoutheast Asia, probably from India (Sharma et al., 2011). Turmericpowder is extracted from the dried ground rhizomes and has many

culinary uses (Hammerschmidt, 1997; Palaniswamy, 2001; Tilaket 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).

antibacterial, anti-inflammatory, analgesic and digestive proper-ties, and some are currently being investigated as treatments forcancer, Alzheimer’s 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 alsoshow insecticidal activity against insect pests and act as mosquitorepellents (Iqbal et al., 2010a; Sukariet al., 2010; Damalas, 2011). C.

longa is harvested when the aerialpart is lost after flowering and itsrhizomes are an intense yellow, possibly indicating the presence of more concentratedpigments (Bambirra et al., 2002; Hossain, 2010).

Geneticfactors,harvesting time, individual plants, soil type, fer-

tilization, time of collection, mode of drying the plant material,storage period and environmental factors all affect the chemicalcomposition and the content of essential oils from C. longa rhi-zomes(Bansalet al., 2002; Chane-Ming et al., 2002; Nazet al., 2011).

The composition and volatility of C. longa essential oils determinethe characteristic smell of turmeric, whereas fixed phenolic com-pounds, 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, thelatter being mainly of a form of germacrene and bisabolane (Zhanget al., 2008; Li et al., 2010; Xiao et al., 2011).

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The Maize weevil Sitophilus zeamais Motschulsky, 1855

(Coleoptera: Curculionidae) is a serious pest of grain crops, both inthe field 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., barleyHordeum vulgare L., rice

Oryza sativa L., rye Secale cereale L., wheat Triticum aestivum L. andcorn Zeamays L. (Poaceae)(Laleand Yusuf, 2000;Ukehet al.,2010).The weevil lays its eggs within the grain, where the larvae then

develop (Larrain et al., 1995). Detrimental effects result from thereduced weight and poorer physical and physiological quality of theinfectedgrains,whichresult mainlyfromthe additional effectof deterioration agents (microorganisms) (Hell et al., 2000). Because

the larvae develop inside the grain, it is difficult to use insecticidesagainst this pest; therefore, they are a promising system to use tostudy the effect of alternative repellent substances (Huang et al.,2011).

The fall armyworm Spodoptera frugiperda J.E. Smith, 1797 (Lepi-doptera: Noctuidae) is a major corn pest in Brazil (Cruz et al., 1999;Senna et al., 2003; Tavares et al., 2010b). Caterpillars of S. frugiperdafirst feed on the remains of their eggshells, where they stay undis-

turbed for 10–12 h, at which point they begin to feed on the greenand succulent tissues of the plant, leaving the membranous epi-

dermis intact (Barros et al., 2010). Fresh droppings indicate thepresence of caterpillars inside the maize cartridge (Busato et al.,

2004). Maize is more sensitive toS. frugiperda40–45 days followinggermination. Pesticides and insecticides can only be applied whenapproximately 20% of the plants are affected and the caterpillarsare 10–12 mm long to reduce any adverse effects on natural ene-

mies of this species (Figueiredo et al., 1999). Contact insecticidesare effective against the eggs and young S. frugiperda caterpillarson the outside of the plant, whereas compounds with antifeedantproperties 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 wasto identify the compound

ar -turmerone, extracted and purified fromC. longa rhizomes andtodetermine its insecticidal and repellent effects on S. zeamais and S.

 frugiperda.

2. Material and methods

 2.1. Experimental procedures

1H,  13 C, HSQC and HMBC NMR measurements were carried outon a Bruker Avance III 500 instrument (operating at 500.13MHzfor 1 H) equipped with a 5 mm triple Resonance broadband inverse

probehead (TBI) with Z-gradient. CDCl3  was used as solvent andtetramethylsilane (TMS) as the internal standard. Mass spectrawere obtained by gaschromatographycoupled to a mass spectrom-etry (GC–MS). The GC–MS analyzes were performed using a gas

chromatograph [GC-17A Shimadzu, GC–MS/QP5,000 Shimadzu,DB-5 column (30mm×0.32mm)], with ionization by electronicimpact, under the followingconditions: 60 ◦Cfor3min;5 ◦C/min to240 ◦C, for 8 min; with an injector temperature of 180◦C, a detector

temperature of 260◦C and an injection volume of 1L. Mass spec-tra were compared with the National Institute of Standards andTechnology database 62 (NIST-62).

 2.2. Trial sites

Thetoxicity of C. longa to S. frugiperdawasevaluated in theLabo-ratory of Insect Rearing (LACRI) of the National Research Center forMaize and Sorghum (EMBRAPA) in Sete Lagoas, Minas Gerais State,

Brazil at 24±2 ◦C, 70±5% relative humidity and a 12-h photope-

riod. A population of S. frugiperdahas been maintained at the LACRI

for approximately 15 years and its caterpillars are fed on an arti-

ficial diet composed of 1 L water, 59.3g wheat germ (T. aestivum),38g yeast extract, 3.82g ascorbic acid, 1.23g sorbic acid, 1.3mL propionic acid, 0.131mL  phosphoric acid, 2.36g 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 per-

formed in the Laboratory of Natural Products and Environment(LPNMA) of the Chemistry Department (DQ) of the Federal Uni-

versity of Goiás (UFG) in Catalão, Goiás State, Brazil. The insectswere collected on a farm in Catalão where no synthetic chemicalsare used. The insects were reared for five generations at 25±3 ◦Cin3 L glass potson 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 cropgrown on the Macaúba farm, Catalão, Goiás State, Brazil (18◦08S,

47◦57W, 515 m above sea level). The farm uses no synthetic chem-ical 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 fine reddish-yellow powder. Thepowder was extracted by steeping in hexane freshly distilled at3±25 ◦C with occasional stirring for a period of 6 h . The plantmaterial:hexane ratio was 500 g rhizomes per 1000mL  hexane.

The solution obtained was filtered and the solvent recovered ina rotary evaporator under low pressure, yielding a light-yellowoil. The oil was separated by column chromatography on silicagel (Vetec, 60–270 mesh), eluting with hexane:ethyl acetate (9:1).

The fractions of interest were analyzed by thin-layer chromatogra-phy (0.20 mm thickness, 60-mesh silica gel; Macherey-Nagel) andrevealed with iodinevapor (sublimation) with a previouslyisolated

and identified standard.

 2.5. Repellence of S. zeamais by ar-turmerone

The repellent activity of ar -turmerone against S. zeamais wasevaluated in five arenas of five circular plastic pots (6cm diame-ter×2.1 cm height). The central pot of each arena, with a diametersufficient to allow the passage of the insects, was interconnected

symmetricallyto the other pot with plastic tubes. Grains of  Z. mays,without residues of synthetic chemicals and harvested at the UFGfarm, were mixed with ar -turmerone whereas control grain wasuntreated; the grains were put in two diagonally opposite pots

within the arena. Thirty non-sexed adults of S. zeamais that hadbeen without food for 24h were released into the central pot and,

after 24h, the total number of individuals per pot was counted.The data were analyzed using the preference index (PI), as fol-

lows: PI= %TPI–%tpI/(%TPI+ %tpI), where %TPI is the percentage of insects in the treatment pot and %tpI is the percentage of insectsin the control pot. The compound is considered repellent with a

PI of between–1.00 and–0.10; neutral, between–0.10 and 0.10 andattractive 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 50L of ar -turmerone per 20g

 Z. mays grains with five replications, each one with an arena and 30insects released. The containers with the corn grains were storedand, after 15,30 and 45 days, the residual repellent effect was eval-

uated.The arrangementwas factorial.The PI valueswere submitted

to an analysis of variance (ANOVA) and the means compared by F 

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 Table 11H and  13 C NMR spectral data for ar -turmerone in CDCl3.

Position ı  1 H (multiplicity, J Hz) ı  13 C Position ı 1 H (multiplicity, J Hz) ı 13 C

1 2.10 (d, 1.3) 20.7 8 1.85 (d, 1.3) 27.4

2 – 155.1 9 – 143.7

3 6.02 (sept , 1.3) 124.1 10 7.09 (m) 126.7

4 – 199.5 11 7.09 (m) 129.15a 2.60 (dd, 15.61; 8.1) 52.7 12 – 135.2

5b 2.70(dd, 15.61; 6.3) 52.7 13 7.09 (m) 129.1

6 3.28(ddq, 8.1; 6.9; 6.3) 35.4 14 7.09 (m) 126.77 1.23(d, 1.3) 21.9 15 2.30 (s) 20.9

1H and  13 C NMR assignmentsare basedon  1 H, HSQC andHMBC spectra.

 Table 2

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

Day 10L 20L 30L 40L 50L 

1 −0.323 ± 0.145 −0.351 ± 0.153 −0.468 ± 0.189 −0.269 ± 0.173 −0.279 ± 0.16515 −0.485 ± 0.059 −0.456 ± 0.172 −0.209 ± 0.272 −0.232 ± 0.210 −0.245 ± 0.088

30 −0.196 ± 0.175 −0.148 ± 0.162 −0.145 ± 0.136 −0.238 ± 0.207 −0.087 ± 0.202

45 −0.224 ± 0.174 −0.179 ± 0.025 −0.270 ± 0.184 −0.155 ± 0.141 −0.173 ± 0.080

Means between the solutions of ar -turmerone, within each line per storage period, do notdiffer by theF test (P <0.05) of theANOVA.

suggests that the aliphatic part is a bisabolane-type sesquiterpene

(Table 1). This carbon skeleton was corroborated by the olefinicand-carbonyl hydrogen signal at ı 6.02 (septet, J = 1.3 Hz, 1H) andthe multiplet in aromatic region. The HSQC and HMBC correlationspectra and peaks [m/z  55 (C4H7

+); m/z  83 (C5H7O+, 100%); m/z 119 (C9H11

+)], supported the proposed structure. The data are inagreement with Lee et al. (2001).

 Ar -turmerone showed repellent activity against S. zeamais dur-ing the 45-day period of exposure as shown by the PI values

(Table 2). The PI values of −0.087 (50L,30 days) to−0.485 (10L,15 days), negatives and <−0.1, characterized the compound asbeing a repellent,except forthe 50L concentration during the 30-dayexposure period(−0.087±0.202),consideredneutral (Table2).

The multivariate statistical analysis (ANOVA, F test, P <0.05) asfunction of the concentration and application time showed sim-

ilarity between treatments, characterizing the ar -turmerone as apowerful natural repellent, even at low concentrations (10L per

20gcorngrain)(Table 2). The repellenceof S. zeamaisby PI suggeststhat ar -turmerone could be used in integrated management of thispest in stored grain, with only 5 g of this compound required pertonof corn. The insecticide andrepellent activity of aromatic plants

of the Zingiberaceae family[alligator pepper Aframomummelegueta(Rosk) K. Schum,joint-whip ginger Alpinia conchigeraGriff, zedoary

Curcuma zedoaria (Berg.) Roscoe, ginger Zingiber officinale (Roscoe)and shampoo ginger  Zingiber zerumbet Smitt] and their essential

oils have been testedwith success against S. zeamais in storedgrains(Ukeh et al., 2010; Suthisut et al., 2011). The repellent activity of essential oils of C. longa was demonstrated against the red flourbeetle Tribolium castaneum Herbst, 1797 (Coleoptera: Tenebrion-

idae) (Iqbal et al., 2010b) and the houseflyMusca domesticaL., 1758(Diptera: Muscidae) (Kumar et al., 2011). The turmerones and ar -turmerone of C. longa are known repellents (Zhang et al., 2008;Li et al., 2010; Xiao et al., 2011). Essential oils from C. longa rhi-

zomes 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 oryzaeL., 1763 (Coleoptera: Curculionidae) and the lesser grain borer

Rhyzopertha dominica F., 1792 (Coleoptera: Bostrychidae) (Matteret al., 2008). The repellence of essential oils from plant products

with insecticide properties [e.g. Surinam cherry Eugenia uniflora L.,1753 (Myrtaceae), eugenol of clove Syzygiumaromaticum (L.) Mer-rill & Perry (Myrtaceae), green fruits of the Brazilian pepper-tree

Schinus terebinthifoliusRaddi, 1820 (Anacardiaceae), marigold pep-

per Piper marginatum L. (Piperaceae), boldo Peumus boldus Molina(Monimiaceae), Piper hispidinervum C. DC. (Piperaceae), cajuputtree Melaleuca leucadendron L. (Myrtaceae), orange peel and limeplants (Rutaceae)] showed a lowresidual effect on S. zeamais, espe-

cially under sunlight because of the effects of UV (Betancur et al.,2010; Coitinho et al., 2010). Essential oil of cardamom Elettaria car-

damomumMaton. (Zingiberaceae) at high concentrations, reducedthe feeding preference of S. zeamais and T. castaneum (Huang

et al., 2000). The essential oil of C. longa at higher concentrations(165mg/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 oilshowed no antifeedant activity on this insect (Table 3).

The mortality of S. zeamais with ar -turmerone at 1% (mm−1)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. zeamaiswith ar -turmerone at 1% and 0.1% (m m−1) increased with thehigher concentration of this essential oil, although the oil had noantifeedant activity on S. zeamais. The mortality of adult S. zeamais

resulted from ingestion of the compound by the insect, suggest-ing a toxic effect of  ar -turmerone on S. zeamais. The mortalityof R. dominica was 83.3% with extract of C. longa in acetone, butthis 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 survivalindividuals± standard errorof mean)of adultsof Sitophilus zeamais (Coleoptera:Curculionidae) after insecticidal activity of ar -tumeroneduring

15 days.

Day Control Control solvent 1% 0.1%

0 0.0025 ± 3.16E−05 0.0025 ± 0.00002 0.0025±8.6E−05 0.0025 ± 3.16E−05

7 0.0025 ± 4.90E−05 0.0023 ± 5.83E−05 NC 0.0024 ± 5.83E−0515 0.0025 ± 3.74E−05 0.0024 ± 3.74E−05 NC 0.0023 ± 7.07E−05

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

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 Table 4

Dead individuals (mean± standard error of mean) of Sitophilus zeamais (Coleoptera: Curculionidae) after treatment withar -turmerone and efficacy (Ea) (%) for theconcen-

trations of ar -turmerone.

Day Control Control solvent 1% E%a 0.1% E%a

3 0.2±0.4 0.0±0.0 01.0±1.20 03.99 00.6±0.50 01.99

7 0.4±0.5 1.8±1.8 20.0±0.00 97.98 05.0±3.10 22.98

15 5.4±5.8 7.0±4.7 20.0±0.00 72.73 10.0±6.30 22.73

a 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

efficacy (Ea) (%) by eggs age.

Day P valueb Mean± standard error of mean E%a

0 0.0081 02.8 ± 1.46 48.63

Control 12.6 ± 2.38 00.00

1 0.0586 00.6 ± 0.60 14.18

Control 03.6 ± 2.20 00.00

2 0.0045 00.8 ± 0.80 48.53

Control 10.6 ± 1.88 00.00

a Abbott (1925).b Mann–Whitney, 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 fromnewly 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 at1% resulted in lower hatching rates than in the control, except for1-day-old eggs (Mann–Whitney test, P < 0.05) (Table 5). The hatch-ing rate of S. frugiperda caterpillars shows a lower susceptibility of 

older eggs toar -turmerone, which might be the resultof thethickerouter membrane of the egg at this stage, which is formed mainlyof lipids (Tavares et al., 2009). Therefore, ar -turmerone could beused 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 mem-brane because of its lipophilic character, with a similar percentageof caterpillars hatching from newly laid or 1-day-old S. frugiperdaeggs. Thus,ar -turmerone could be a promising agent forthe controlof S. frugiperda.

The ar -turmerone caused a 58.3% mortality of S. frugiperdacaterpillars (Table 6). At 100g/caterpillar (0.1 mL  in solution

of 1% of  ar -turmerone) the compound reduced the developmentof this insect (Table 6). The diameter of the head capsule of  S. frugiperda that had been exposed to ar -turmerone was reducedin 60% of caterpillars compared with control (0.099 and 0.245cm,

respectively) (Table 6). The length of caterpillars was reduced in59.6% (0.59 and 1.46cm, respectively) and the weight in 93.8%

(3.2×10−3

and 52.2×10−3

g, respectively) in comparison withcontrols (Table 6). The lower values of the biological parameters of 

 Table 6

Biological parameters (mean± standard error of mean) and efficacy (Ea) (%)of the

intake activity of ar -turmerone by Spodoptera frugiperda (Lepidoptera: Noctuidae)in artificial diet.

 Ar -turmerone Control

Efficacy (%)a 58.33 00.00

Width of head capsule (mm) 0.99±0.420 a 02.45±0.14 b

Body weight (mg) 3.20±0.766 a 52.20±5.80 b

Body length (mm) 5.90±0.520 a 14.60±0.75 b

Meansfollowedby thesamelow letterper line do notdiffer by theMann–Whitneytest, P < 0.0001, BioEstat 5.0.

a

Abbott (1925).

caterpillars exposed to ar -turmerone confirm the high toxicity of thiscompoundto S. frugiperdaandthe fact that, although notlethal,

it can reduce the development and so the damage and number of offspring produced by this insect.Individuals descended fromthosethat 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 extractsreduced by 69% the weight of caterpillars of cotton bollwormHeli-coverpa armigeraHübner, 1805 (Lepidoptera: Noctuidae) (Kathuriaand Kaushik, 2006). The pupal progeny of the fly Bactrocera zonataSaunders,1841 (Diptera:Tephritidae) were reduced in 67.90, 60.74and 51.96% of treatments with extracts of C. longa at 1000, 500and 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 inhi-bition of S. frugiperdagrowth in the treatments with ar -turmeroneapplied on the artificial diet (Table 7). The dry weight of food

ingested, feces produced, weight gain and dry weight of foodassimilated 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 andlarva period studied (1- to 11-day of larva period). The evalu-ation of RCR indicated that antogenins from  Annona cherimoyaMill. (Annonaceae) were not antifeedant, but squamocin from this

plant reduces the efficiency to convert food into biomass by S. frugiperda caterpillars (Colom et al., 2007). The botanical insec-

ticide rotenone showed non-lethal post-ingestive effects on thedigestion/absorption of food and on its conversion to biomass by

S. frugiperda caterpillars. This suggests relative resistance of thisinsect to this insecticide (Wheeler et al., 2001).

 Table 7

Dryweight of food ingested (g), feces produced (g)and weight gain (g); dryweight

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), rela-

tive growth rate (RGR) (g/g/day), approximate digestibility (AD) (%), conversionefficiency of ingested food (ECI) (%), conversion efficiency of ingested food (ECD)

(%) and metabolic cost (100–ECD) of survival Spodoptera frugiperda (Lepidoptera:

Noctuidae) caterpillarsfed with artificial diet treated or notwith ar -turmerone.

Parametersevaluated Artificial dietwithar -turmerone

Artificial diet withoutar -turmerone

Food ingested 0.019±4.725E−04 b 0.308±7.700E−03 a

Feces produced 0.010±3.226E−04 b 0.165±5.323E−03 a

Weigh gain 3.253E−03±1.162E−04 b 0.053±1.893E−03 a

Food assimilated 8.900E−03±9.536E−04 b 0.143±0.015 aFood metabolized 5.647E−03±8.057E−04 b 0.090±0.012 a

Larva period studied 11 11

RCR 0.537±0.016 a 0.536±0.015 a

RMR  0.160±0.017 a 0.157±0.016 a

RGR 0.092±0.002 a 0.092±0.002 a

AD 47.090±1.236 a 46.429±1.225a

ECI 17.212±0.291 a 17.208±0.288 a

ECD 36.551±3.156 a 37.063±3.162a

100–ECD 63.449±3.156 a 62.937±3.162a

Mean± standard error of themean. Meansfollowed by thesame lowletter perline

do not differ by theMann–Whitneytest,P < 0.0001, BioEstat 5.0.

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164   W.d.S. Tavares et al. / Industrial Crops andProducts 46 (2013) 158–164

Pereira, L.G.B., Petacci, F., Fernandes, J.B., Correa, A.G., Vieira, P.C., Silva, M.F.G.F.,Malaspina, O., 2002. Biological activity of astilbin from Dimorphandra mollisagainst  Anticarsia gemmatalis and Spodoptera frugiperda. Pest Manag. Sci. 58,503–507.

Qin, N.Y., Yang, F.Q., Wang, Y.T., Li, S.P., 2007. Quantitative determination of eightcomponentsin rhizome(Jianghuang) andtuberousroot (Yujin)of Curcumalongausing pressurized liquid extraction and gas chromatography-mass spectrome-try. J. Pharmaceut. Biomed. 43, 486–492.

Raina, V.K., Srivastava, S.K., Syamsundar, K.V., 2005. Rhizome and leaf oil compo-sition of Curcuma longa from the lower Himalayan region of northern India. J.Essent. Oil Res. 17, 556–559.

Scriber, J.M., Slansky Junior, F., 1981. The nutritional ecology of immature insects.Annu. Rev. Entomol. 26, 183–211.

Senna, D.Q., Pinto, F.A.C., Queiroz, D.M., Viana, P.A., 2003. Fall armyworm damagedmaize plant identification using digital images. Biosyst. Eng. 85, 449–454.

Sharma,G.J.,Chirangini,P., Kishor, R.,2011.Gingers ofManipur: diversityand poten-tials as bioresources. Genet. Resour. Crop Evol. 58, 753–767.

Siddiqi, A.R., Rafi, A., Naz, F., Masih, R., Ahmad, I., Jilani, G., 2011. Effects of Cur-cuma longa extracts on mortality and fecundity of Bactrocera zonata (Diptera:Tephritidae). Ciênc. Agrotec. 35, 1110–1114.

Sigrist, M.S., Pinheiro, J.B., Azevedo, J.A., Zucchi, M.I., 2011. Genetic divergenceamong Brazilian turmeric germplasm using morpho-agronomical descriptors.Crop Breed. Appl. Biotechnol. 11, 70–76.

Sukari, M.A., Rashid, N.Y., Neoh, B.K., Abu Bakar, N.H., Riyanto, S., Ee, G.C.L., 2010.Larvicidal activity of some Curcuma and Kaempferia rhizome extracts againstdengue fever mosquito  Aedes aegypti Linnaeus (Diptera: Culicidae). Asian J.Chem. 22, 7915–7919.

Suthisut, D., Fields, P.G.,Chandrapatya, A., 2011. Contact toxicity, feeding reduction,and repellency of essential oilsfrom three plants fromthe ginger family (Zingib-eraceae) and their major components against Sitophilus zeamais and Triboliumcastaneum. J. Econ. Entomol. 104, 1445–1454.

Tavares, W.S., Costa, M.A. , Cruz , I ., Silveira, R.D., Serrão, J .E. , Zanu ncio, J .C. ,2010a. Selective effects of natural and synthetic insecticides on mortality of Spodoptera frugiperda (Lepidoptera:Noctuidae) and its predatorEriopisconnexa(Coleoptera: Coccinellidae). J. Environ. Sci. Health B 45, 557–561.

Tavares, W.S., Cruz, I., Fonseca, F.G., Gouveia, N.L., Serrão, J.E., Zanuncio, J.C., 2010b.Deleterious activity of natural products on postures of Spodoptera frugiperda(Lepidoptera: Noctuidae) and Diatraea saccharalis (Lepidoptera: Pyralidae). Z.Naturforsch. C 65, 412–418.

Tavares,W.S., Cruz, I.,Petacci,F., Freitas,S.S., Serrão,J.E., Zanuncio,J.C.,2011. Insecti-cide activity of piperine:toxicity to eggs of Spodoptera frugiperda (Lepidoptera:Noctuidae) andDiatraea saccharalis (Lepidoptera: Pyralidae) and phytotoxicityon several vegetables. J. Med. PlantsRes. 5, 5301–5306.

Tavares, W.S., Cruz, I., Petacci, F., Assis Júnior, S.L., Freitas, S.S., Zanuncio, J.C.,Serrão, J.E., 2009. Potential use of Asteraceae extracts to control Spodoptera frugiperda (Lepidoptera: Noctuidae) and selectivity to their parasitoids Tri-chogramma pretiosum (Hymenoptera: Trichogrammatidae) and Telenomusremus (Hymenoptera: Scelionidae). Ind. Crop. Prod. 30, 384–388.

Tigar, B.J.,Key, G.E., Flores, M.E., Vazquez,M., 1994. Fieldand post-maturation infes-tation of maize by stored-product pests in Mexico. J. StoredProd. Res. 30, 1–8.

Tilak, J.C.,Banerjee, M., Mohan, H., Devasagayam, T.P.A., 2004. Antioxidant availabil-ityof turmeric in relation to its medicinal andculinary uses.Phytother. Res. 18,798–804.

Tripathi,A.K.,Prajapati,V., Verma,N., Bahl, J.R., Bansal,R.P., Khanuja,S.P.S., Kumar,S.,2002. Bioactivitiesof theleaf essential oil of Curcuma longa(Var. Ch-66) on threespecies of stored-product beetles (Coleoptera). J. Econ. Entomol. 95, 183–189.

Ukeh, D.A., Birkett, M.A., Bruce, T.J.A., Allan, E.J., Pickett, J.A., Mordue, A.J., 2010.Behavioural responses of the maize weevil, Sitophilus zeamais, to host (stored-grain)and non-host plant volatiles. Pest Manag. Sci. 66, 44–50.

Vazquez-Castro, J.A., Baptista, G.C., Trevisan, L.R.P., Gadanha, C.D., 2009. Flightactivity of Sitophilus oryzae (L) and Sitophilus zeamais Motsch (Coleoptera: Cur-culionidae) and its relationship with susceptibility to insecticides. Neotrop.Entomol. 38, 405–409.

Vianna, U.R., Pratissoli, D., Zanuncio, J.C., Lima, E.R., Brunner, J., Pereira, F.F., Serrão, J.E., 2009. Insecticide toxicity to Trichogramma pretiosum (Hymenoptera: Tri-chogrammatidae) females and effect on descendant generation. Ecotoxicology18, 180–186.

Xiao, Y.C., Xie, J.,Yu, M., Ran,J., Xi, Z., Li, W., Huang, J., 2011. Bisabocurcumin, a newskeleton curcuminoid from the rhizomes of Curcuma longa L. Chin. Chem. Lett.22, 1457–1460.

Waldbauer, G.P., 1968. The consumption and utilization of food by insects. Adv.Insect Physiol. 5, 229–288.

Wheeler, G.S., Slansky, F., Yu, S.J., 2001. Food consumption, utilization and detox-ification enzyme activity of larvae of three polyphagous noctuid moth specieswhen fed the botanical insecticide rotenone. Entomol. Exp. Appl. 98, 225–239.

Zhang, J.S., Guan, J., Yang, F.Q., Liu, H.G., Cheng, X.J., Li, S.P., 2008. Qualitative andquantitative analysis of four species of Curcuma rhizomes using twice develop-ment thin layer chromatography. J. Pharmaceut. Biomed. 48, 1024–1028.