Ar-turmerone from Curcuma longa (Zingiberaceae) rhizomes and effects on Sitophilus zeamais (Coleoptera: Curculionidae) and Spodoptera frugiperda (Lepidoptera: Noctuidae)

Industrial Crops and Products 46 (2013) 158–164

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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 Lião d , José Cola Zanuncio e,∗ a

Departamento de Fitotecnia, Universidade Federal de Vic¸osa, 36570-000, Vic¸osa, Minas Gerais State, Brazil Departamento de Química, Universidade Federal de Goiás, 75704-020, Catalão, Goiás State, Brazil c Departamento de Patologia, Universidade Federal de Goiás, 74001-970, Goiânia, Goiás State, Brazil d Instituto de Química, Universidade Federal de Goiás, 74001-970, Goiânia, Goiás State, Brazil e Departamento de Biologia Animal, Universidade Federal de Vic¸osa, 36570-000, Vic¸osa, 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 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 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 artificial 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 ramifications 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: [email protected] (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-inflammatory, analgesic and digestive properties, and some are currently being investigated as treatments for cancer, 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 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 flowering 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 fixed 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).

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The Maize weevil Sitophilus zeamais Motschulsky, 1855 (Coleoptera: Curculionidae) is a serious pest of grain crops, both in the 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., 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 difficult 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 first feed on the remains of their eggshells, where they stay undisturbed for 10–12 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 40–45 days following germination. Pesticides and insecticides can only be applied when approximately 20% of the plants are affected and the caterpillars are 10–12 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 purified 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 (GC–MS). The GC–MS analyzes were performed using a gas chromatograph [GC-17A Shimadzu, GC–MS/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

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for approximately 15 years and its caterpillars are fed on an artificial 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 Goiás (UFG) in Catalão, Goiás State, Brazil. The insects were collected on a farm in Catalão where no synthetic chemicals are used. The insects were reared for five 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 Macaúba farm, Catalão, Goiás 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 fine 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 filtered 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, 60–270 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 identified standard. 2.5. Repellence of S. zeamais by ar-turmerone The repellent activity of ar-turmerone against S. zeamais was evaluated in five arenas of five circular plastic pots (6 cm diameter × 2.1 cm height). The central pot of each arena, with a diameter sufficient 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 between–1.00 and–0.10; neutral, between–0.10 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 five 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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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 filled 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 five replications with 0.1% and 1% (m m−1 ) 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 efficacy 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 five pieces of paper each containing 20 eggs were used per experimental group. An 8-g cube of solid artificial 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 v−1 ) 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 five 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 Mann–Whitney 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 artificial 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 v−1 ) 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 Mann–Whitney 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 artificial diet were placed in an oven at 55–60 ◦ 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 final of feeding period (T) was recorded to determine weight gain (P) of caterpillars. Ten plastic 50-mL cups with artificial 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; I–F, food assimilated (g) during T and M = (I–F)–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; efficiency of conversion of food ingested (%) (ECI) = (B ÷ I) × 100; efficiency 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 Mann–Whitney 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 m−1 ) (1.93 g) and the yield of ar-turmerone obtained from this essential oil was 82% (m m−1 ) 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 Catalão, Goiás 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 São Tomé and Príncipe (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 purified 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 ı 1.85 (d, J = 1.3 Hz, 3H) and ı 2.10 (d, J = 1.3 Hz, 3H), compatible with methyl attached to unsaturated carbon ␤ to carbonyl group and signs at ı 1.23 (d, J = 1.3 Hz, 3H) and ı 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 ı 2.30 (s, 3H) indicate a methyl attached to the aromatic ring (Table 1). Double doublets at ı 2.60 (dd, J = 15.61, 8.1 Hz) and ı 2.70 (dd, J = 5.61, 6.3 Hz) compatible with diastereotopic CH2 neighboring of carbonyl and methine groups,

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

1

Position

ı 1 H (multiplicity, J Hz)

ı 13 C

Position

ı 1 H (multiplicity, J Hz)

ı 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 olefinic and ␣-carbonyl hydrogen signal at ı 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 officinale (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 flour beetle Tribolium castaneum Herbst, 1797 (Coleoptera: Tenebrionidae) (Iqbal et al., 2010b) and the housefly 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 uniflora 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 m−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. zeamais with ar-turmerone at 1% and 0.1% (m m−1 ) 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 ± 3.16E−05 0.0025 ± 4.90E−05 0.0025 ± 3.74E−05

0.0025 ± 0.00002 0.0023 ± 5.83E−05 0.0024 ± 3.74E−05

0.0025 ± 8.6E−05 NC NC

0.0025 ± 3.16E−05 0.0024 ± 5.83E−05 0.0023 ± 7.07E−05

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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Table 4 Dead individuals (mean ± standard error of mean) of Sitophilus zeamais (Coleoptera: Curculionidae) after treatment with ar-turmerone and efficacy (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

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

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). 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 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 (Mann–Whitney 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 × 10−3 and 52.2 × 10−3 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 efficacy (Ea ) (%) of the intake activity of ar-turmerone by Spodoptera frugiperda (Lepidoptera: Noctuidae) in artificial diet.

Efficacy (%)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 Mann–Whitney test, P < 0.0001, BioEstat 5.0. a Abbott (1925).

caterpillars exposed to ar-turmerone confirm 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 Hübner, 1805 (Lepidoptera: Noctuidae) (Kathuria and Kaushik, 2006). The pupal progeny of the fly 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 artificial 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 efficiency 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 efficiency of ingested food (ECI) (%), conversion efficiency of ingested food (ECD) (%) and metabolic cost (100–ECD) of survival Spodoptera frugiperda (Lepidoptera: Noctuidae) caterpillars fed with artificial diet treated or not with ar-turmerone. Parameters evaluated

Artificial diet with ar-turmerone

Artificial diet without ar-turmerone

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

0.019 ± 4.725E−04 b 0.010 ± 3.226E−04 b 3.253E−03 ± 1.162E−04 b 8.900E−03 ± 9.536E−04 b 5.647E−03 ± 8.057E−04 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 ± 7.700E−03 a 0.165 ± 5.323E−03 a 0.053 ± 1.893E−03 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 Mann–Whitney test, P < 0.0001, BioEstat 5.0.

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4. Conclusions The ar-turmerone is highly toxic to S. zeamais and S. frugiperda at low doses. This sesquiterpene has significant 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 Goiás in Catalão, Goiás State, Brazil) that died on June 15, 2012 and Professor Sérgio de Freitas (Faculty of Agriculture and Veterinary Sciences, Paulista Estadual University “Júlio de Mesquita Filho” in Jaboticabal, São 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. Aristônio Magalhães Teles (Institute of Biological Sciences – General Biology Department – Federal University of Goiás in Goiânia, Goiás State, Brazil) to identify C. longa (Zingiberaceae). To M.Sc. Amauri Alves de Souza Júnior (Institute of Chemistry – Paulista Estadual University “Júlio de Mesquita Filho” in Araraquara, São Paulo State, Brasil) for help in conducting the experiments. To Macaúba farm, Catalão, Goiás State, Brazil by C. longa rhizomes. To “Conselho Nacional de Desenvolvimento Científico e Tecnológico” (CNPq), “Coordenac¸ão de Aperfeic¸oamento de Pessoal de Nível Superior (CAPES)” and “Fundac¸ão de Amparo à Pesquisa do Estado de Goiás (FAPEG)” for grants. This research project (Notice: 01/2011–Universal Demand) was supported by the “Fundac¸ão 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. References Abbott, W.S., 1925. A method of computing the effectiveness of an insecticide. J. Econ. Entomol. 18, 265–267. Adamczyk, J.J., Leonard, B.R., Graves, J.B., 1999. Toxicity of selected insecticides to fall armyworms (Lepidoptera: Noctuidae) in laboratory bioassay studies. Fla. Entomol. 82, 230–236. Ajaiyeoba, E.O., Sama, W., Essien, E.E., Olayemi, J.O., Ekundayo, O., Walker, T.M., Setzer, W.N., 2008. Larvicidal activity of turmerone-rich essential oils of Curcuma longa leaf and rhizome from Nigeria on Anopheles gambiae. Pharm. Biol. 46, 279–282. Al-Sarar, A., Hall, F.R., Downer, R.A., 2006. Impact of spray application methodology on the development of resistance to cypermethrin and spinosad by fall armyworm Spodoptera frugiperda (JE Smith). Pest Manag. Sci. 62, 1023–1031. Ali, B.H., Marrif, H., Noureldayem, S.A., Bakheit, A.O., Blunden, G., 2006. Some biological properties of curcumin: a review. Nat. Prod. Commun. 1, 509–521. Ayres, M., Ayres Júnior, M., Ayres, D.L., Santos, A.A., 2007. BIOESTAT – Aplicac¸ões estatísticas nas áreas das ciências biomédicas. ONG Mamiraua, Belém, Pará. Bambirra, M.L.A., Junqueira, R.G., Gloria, M.B., 2002. Influence of post-harvest processing conditions on yield and quality of ground turmeric (Curcuma longa L.). Braz. Arch. Biol. Technol. 45, 423–429. Bansal, R.P., Bahl, J.R., Garg, S.N., Naqvi, A.A., Kumar, S., 2002. Differential chemical compositions of the essential oils of the shoot organs, rhizomes and rhizoids in the turmeric Curcuma longa grown in indo-grangetic plains. Pharm. Biol. 40, 384–389. Barros, E.M., Torres, J.B., Bueno, A.F., 2010. Oviposition, development, and reproduction of Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae) fed on different hosts of economic importance. Neotrop. Entomol. 39, 996–1001. Betancur, J., Silva, G., Rodriguez, J.C., Fischer, S., Zapata, N., 2010. Insecticidal activity of Peumus boldus Molina essential oil against Sitophilus zeamais Motschulsky. Chil. J. Agr. Res 70, 399–407. Blessing, L.D., Colon, O.A., Popich, S., Neske, A., Bardon, A., 2010. Antifeedant and toxic effects of acetogenins from Annona montana on Spodoptera frugiperda. J. Pest Sci. 83, 307–310. Busato, G.R., Gurtzmacher, A.D., Garcia, M.S., Giolo, F.P., Nornberg, S.D., 2004. Consumption and utilization of food by Spodoptera frugiperda (J. E. Smith, 1797)

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