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Bioefficacy of plant essential oilsagainst pulse beetles Callosobruchusspp. (Coleoptera: Bruchidae) in pigeonpea seeds with particular reference toClausena pentaphylla (Roxb.) DC.Abhay K. Pandey a , Pooja Singh a , Uma T. Palni b & N.N. Tripathi aa Bacteriology and Natural Pesticide Laboratory, Department ofBotany, DDU Gorakhpur University, Gorakhpur, Indiab Department of Botany, DSB Campus, Kumaun University,Nainital, IndiaPublished online: 07 Mar 2013.

To cite this article: Abhay K. Pandey , Pooja Singh , Uma T. Palni & N.N. Tripathi (2013):Bioefficacy of plant essential oils against pulse beetles Callosobruchus spp. (Coleoptera: Bruchidae)in pigeon pea seeds with particular reference to Clausena pentaphylla (Roxb.) DC., Archives OfPhytopathology And Plant Protection, DOI:10.1080/03235408.2013.768410

To link to this article: http://dx.doi.org/10.1080/03235408.2013.768410

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Bioefficacy of plant essential oils against pulse beetles Callosobruchusspp. (Coleoptera: Bruchidae) in pigeon pea seeds with particularreference to Clausena pentaphylla (Roxb.) DC.

Abhay K. Pandeya, Pooja Singha, Uma T. Palnib and N.N. Tripathia*

aBacteriology and Natural Pesticide Laboratory, Department of Botany, DDU GorakhpurUniversity, Gorakhpur, India; bDepartment of Botany, DSB Campus, Kumaun University,Nainital, India

(Received 7 January 2013; final version received 16 January 2013)

Thirty essential oils from higher plants of Gorakhpur Division (India) were evaluated at0.36 μl/ml against two pulse beetles, Callosobruchus chinensis L. and C. maculatus F.,causing infestation of pigeon pea seeds during storage. Clausena pentaphylla oilwas more effective and exhibited absolute repellency against both the insects fol-lowed by Ocimum canum, Salvia plebeia and Zingiber zerumbet oils. Among thesefour oils, C. pentaphylla oil was most toxic and showed 100% mortality of boththe insects at 10-μl dosage and 24-h exposure (LD50 = 2.7 μl for C. chinensis &2.4 μl for C. maculatus). Physical factors, viz. temperature, storage and autoclaving,did not cause any adverse effect on the toxicity of Clausena oil. During in vivoinvestigation, the oil protected 1 kg of pigeon pea seeds completely without reduc-ing weight loss and seed damage up to 6months when stored in gunny bags andglass containers. The oil was standardised by determining its various physicochemi-cal properties. Thus, C. pentaphylla oil can be judiciously exploited as herbal insec-ticide against pulse beetles of pigeon pea seeds during storage.

Keywords: Clausena pentaphylla; repellency; Callosobruchus spp.; essential oils;physicochemical properties

Introduction

In tropical and subtropical countries, pulse seeds suffer a great damage during storagedue to insect attack. Among the insect pests attacking stored pulses, the pulse beetle,Callosobruchus species, is the most dangerous (Adugna 2006). These insects have beenreported from Philippines, Japan, Indonesia, Sri Lanka, Burma, India and Bangladesh.They are notorious pests of chickpea, mung, cowpea, garden pea, black gram, lentil andpigeon pea. The extent of damage to pulse seeds is very high both qualitatively andquantitatively. There was a 55–69% loss in seed weight and 45.6–66.3% loss in proteincontent due to attack by the pulse beetle on pigeon pea seeds. About 100% loss of pulseseeds was found due to infestation by the pulse beetles (Borikar and Puri 1985) duringstorage. Protecting stored pulses against Callosobruchus species is known to depend onthe use of synthetic chemical pesticides (Isman 2000). However, broad-spectrum insecti-cides have been reported to cause development of resistance in insect populations(Bughio and Wilkins 2004). The use of botanical pesticides in controlling insect pests is

*Corresponding author. Email: nijendratripathi@gmail.com

Archives of Phytopathology and Plant Protection, 2013http://dx.doi.org/10.1080/03235408.2013.768410

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considered to be the most viable and environmentally safe approach to offset everincreasing danger caused by synthetic pesticides (White and Leesch 1995). In thisregard, natural products (essential oils) are generally preferred because of their innatebiodegradability and less harmful compounds affecting non-target organisms (Burt2004). Plants have acquired effective defence mechanisms that ensure their survivalunder adverse environmental factors. In addition to morphological mechanisms, plantshave also developed chemical defence mechanisms towards organisms, such as insects,that affect biochemical and physiological functions (Prakash and Rao 1997). Essentialoils are usually extracted from various parts of the plant which have potential for theusage as insecticides and are repellent against stored-product insects (Sahaf and Mohar-ramipour 2008; Islam et al. 2009; Saroukolai et al. 2010; Yang et al. 2010; Amri et al.2012). The family Rutaceae contains plants with very strong aroma, and their essentialoils contain constituents with which the insecticidal activity has already been studied.From this family, the genus Clausena consists of six species, viz. C. anisata Willd.,C. excavata Burm. f., C. indica Oliver, C. lansium (Lour.) Skeel, C. pentaphylla (Roxb.)DC. and C. heptaphylla (Roxb.) DC., in Indian flora, of which, only C. pentaphylla isfound in the forests of Gorakhpur Division (Uttar Pradesh, India). These plant speciesand their extracts are known to have various effects on insect pests, including stored-product insects. Several studies have assessed the ability of the Clausena essential oilsand their constituents as fumigants and repellents against a number of insect pests (Ham-mond et al. 2000; Ndomo et al. 2008; Nukenine et al. 2010). However, there are noreports concerning the toxicity of the C. pentaphylla essential oil against stored-productinsects. Therefore, the objective of this investigation was to explore the repellency of theC. pentaphylla along with essential oils of 29 other higher aromatic plants against thestored pulse beetles of pigeon pea seeds. Insecticidal activity of potent oils was also car-ried out in present investigation. Further, in vivo efficacy of C. pentaphylla oil in storageof pigeon pea seeds was carried out. Besides, C. pentaphylla oil was also standardisedby determining its various physicochemical properties.

Materials and methods

Insect rearing

Rearing of both Callosobruchus species was done separately in glass containers at Bac-teriology and Natural Pesticide Lab, Department of Botany, DDU Gorakhpur University,Gorakhpur under the environment conditions of 28 ± 2 °C and 75 ± 5% RH. To obtainnewly emerged bruchids of same generation, 40 adults were released in a container hav-ing 250 g of pigeon pea seeds covered by a muslin cloth. The insects that emerged after3–4weeks were used for the entire experiments.

Extraction of essential oils from higher plants

Thirty higher plant species were collected from Gorakhpur Division (U.P., India) during2008–2009, and identified with the help of Flora Gorakhpurensis (Srivastava 1976) aswell as by matching their specimens lodged in the herbarium of BSI (NRC) Dehradun.Essential oils from fresh parts of collected plant species (300 g each) were extractedseparately using Clevenger’s apparatus at 90 ± 2 °C for 4 h. Each essential oil was driedover anhydrous sodium sulphate and was stored separately at 4 °C in clean glass vialfor further experimentation.

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Repellency test

Repellent activity of each isolated essential oil was evaluated against Callosobruchuschinensis and C. maculatus following Tripathi and Kumar (2007) using “Y” tube Olfac-tometer separately. Requisite amount of oil (0.36 μl/ml) from each plant was soaked incotton swab and introduced in one arm of “Y” tube of Olfactometer separately. Water-soaked cotton swab was placed in other arm as control set. Ten pairs of adults of eachtest insect were obtained from reared culture, and introduced separately into basal armof “Y” tube Olfactometer in four batches at interval of 10min each to avoid mutualinterference. The repellent activity of oil was recorded in terms of per cent repellency(Per cent repellency =NC�NT/NC� 100, where NC and NT are number of individualin control and treatment arms of Olfactometer, respectively) after 30min of interval at28 ± 2 °C and 75 ± 5% RH.

Insecticidal activity of potent essential oils

This experiment was conducted following the method of Kumar et al. (2008). Differentamounts of each potent oil (5, 10 and 20 μl) were soaked in filter paper discs (10mmdiameter) separately and pasted on inner surface of the cover of the pre-sterilised Petriplates containing 5 g of pigeon pea seeds along with five pairs of insects. Similarly, acontrol set was also kept without oil. In order to get cidal nature of the oil, the insectrevival was observed after transferring them onto fresh Petri plate. Experimental set-upfor both insects was done separately. The incubation temperature was at 28 ± 2 °C and75 ± 5% RH. The percentage mortality of insects was recorded at interval of 24 h ofexposure.

Effect of physical factors on toxicity of C. pentaphylla oil

Expiry of toxicity of oil was studied by storing the oil at room temperature and testingits insecticidal activity at a regular interval of threemonths. Effect of temperature on thetoxicity of oil was examined by incubating the oil at 40–120 °C in closed airtight glassvials in an electric oven and then tested against test insects separately. Similarly, auto-claving of the oil was done in sealed vial for 20min at 15 lb/inch2 pressure and thentested against test insects. During all the experiments, the incubation temperature was at28 ± 2 °C and 75 ± 5% RH.

In vivo toxicity of C. pentaphylla oil against pulse beetles

Freshly harvested pigeon pea seeds of a local variety (Ramarhara) were collected inpolyethylene bags from a village (Koraiya) of Gorakhpur district during 2009–2010.The moisture content of the seeds was determined by oven drying method. Differentamounts of C. pentaphylla oil were soaked in cotton swabs so as to procure the concen-tration of 0.29 and 0.58 μl/ml and introduced separately in pre-sterilised gunny bagsand glass containers (35 cm diameter� 16 cm) with 1 kg pigeon pea seeds for fumiga-tion. Likewise, two other sets were prepared by treating pigeon pea seeds with syntheticfumigants (aluminium phosphide and ethylene dibromide) for comparison purpose. Thenon-fumigated seeds were kept as the control set. The containers were made airtightand stored in a seed storage cabinet in laboratory at 28 ± 2 °C and 75 ± 5% RH for sixmonths. Each set was kept in triplicates. Efficacy of oil and synthetic fumigants on

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pigeon pea seed infestation was assessed by weight loss, seed damage (Parkin 1956)and by calculating feeding deterrency index (Isman et al. 1990).

Physicochemical properties of C. pentaphylla oil

Various physicochemical properties (specific gravity, specific rotation, refractive index,acid value, saponification number, ester number, phenolic content and solubility in vari-ous organic solvents) of the oil were studied for its standardisation (Langenau 1948).

Statistical analysis

All the experiments were carried out in triplicates and data were statistically analysed.Data were also subjected to analysis of variance (p < 0.05). Probit analysis was used forthe estimation of LD50.

Results and discussion

During Olfactometer repellency bioassay, oil from C. pentaphylla demonstrated absoluterepellent activity against C. chinensis and C. maculatus followed by Ocimum canum(83.63 & 78.27), Salvia plebeia (86.67 & 89.09) and Zingiber zerumbet (84.78 &80.00), respectively. The repellent activity of these four oils were found to be signifi-cantly different (p< 0.05) from other essential oils used during bioassay (Table 1). Thisdifference of toxicity among the oils may be due to differences in their chemical con-stituents. In earlier research using same pathogens and Olfactometer, Paranagama et al.(2002) recorded the repellent activities of Cymbopogon citratus and Murraya koenigiion C. maculatus were 35 and 32%, respectively. On the contrary, C. pentaphylla,O. canum, S. plebeia and Z. zerumbet essential oils were more toxic on C. maculatus inpresent investigation. In research conducted by Kheradmand et al. (2010), Jojoba oilrepelled C. maculatus to an extent of 21.4 ± 3.44% which also adds to the evidence thatour tested four oils can be better repellents than the earlier oils used. The repellentplants may contain certain active volatile compounds that elicit anti-feedant behaviourby the visiting insects.

During insecticidal bioassay, C. pentaphylla oil at 5-μl dosage caused significant(p< 0.05) mortality of test insects within 24-h treatment as compared to other potentoils used (Table 2). Among other three oils, O. canum was more toxic with LD50 valueof 5.8 μl for C. chinensis and 7.9 μl for C. maculatus followed by S. plebeia(LD50 = 14.5 μl for C. chinensis & 16.4 μl for C. maculatus) and Z. zerumbet(LD50 = 16.8 μl for C. chinensis & 18.5 μl for C. maculatus) oils.

Plant essential oils contain many volatile compounds. Jointly or independently, theymight contribute to the insecticidal activity; however, the use of crude plant essentialoils instead of purified or synthetic compounds may result in beneficial effect beyondmere pest control and may, therefore, convey additional economic benefits (Kim andPark 2008). The death of insects might be recognised in regard to the contact toxicityor to the abrasive effect on the pest cuticle (Mathur et al. 1985) which might also inter-fere with the respiratory mechanism of insects (Kim et al. 2003). Raja et al. (2001)found that 10-μl dosage and 24-h exposure of Mentha arvensis oil caused 55% mortal-ity of C. maculatus. In the present study, 10-μl dosage of C. pentaphylla oil was ableto cause 100% mortality after 24 h of exposure. Rajapakse (2006) investigated that at0.05 and 0.17 μl concentrations (24-h exposure) of Ocimum sanctum oil exhibited

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100% mortality of C. chinensis and C. maculatus, respectively. On the contrary, in thepresent study, 100% mortality was observed by increasing the concentration of the oil.This might be due to the different essential oils and differences in host range.

It is mentioned in the literature that octopamine plays an important broad-spectrumbiological roles in insects (Evans 1980). Octopamine exerts its effects through contactwith at least two classes of receptors which, on the basis of pharmacological criteria,have been designated as octopamine-1 and octopamine-2 (Evans 1981). Deactivatingthe octopamine function, results in total breakdown of nervous system in insects. There-fore, octopaminergic system of insects represents a biorational target for insect control.Little is known about the physiological effect of essential oils on insects, but treatmentswith various essential oils or their constituents cause symptoms that suggest a neuro-toxic mode of action (Kostyukovsky et al. 2002). A monoterpenoid, linalool, has beendemonstrated to act on the nervous system, affecting ion transport and the release of

Table 1. Repellent activity of essential oils against Callosobruchus species.

Plant species(essential oils)⁄Partused Family

Percentage repellency#

C. chinensisL.

C. maculatusF.

Aegle marmelos (L.) Corr. L Rutaceae 52.17 ± 1.52 45.00 ± 1.52Anethum graveolens Linn. S Apiaceae 54.55 ± 1.15 47.83 ± 2.00Blumea membranacea DC. S Asteraceae 10.70 ± 0.50 64.00 ± 1.00B. mollis (D. Don) Merr. S Asteraceae 71.42 ± 2.30 59.09 ± 1.02Callicarpa macrophylla (L.) Vahl L Verbenaceae 58.33 ± 1.52 47.83 ± 1.57Cannabis sativa Linn. T Cannabinaceae 40.00 ± 2.00 26.04 ± 1.15Citrus limon (L) Burm. L Rutaceae 78.94 ± 0.57$ 65.38 ± 1.00Clausena pentaphylla (Roxb.) DC. L Rutaceae 100 ± 0.00$ 100 ± 0.00$

Clerodendrum viscosum (L) Vent. L Verbenaceae 65.22 ± 0.57 57.17 ± 1.52Colebrookea oppositaefolia Sm. L Lamiaceae 59.09 ± 1.05 54.54 ± 0.58Coleus aromaticus Benth. L Lamiaceae 52.63 ± 1.23 55.55 ± 1.52Cyperus brevifolius (Rottb.) Hassk. W Cyperaceae 47.37 ± 0.58 59.09 ± 1.00C. monocephalus Endl. W Cyperaceae 61.53 ± 0.57 61.90 ± 1.15Eucalyptus citriodora Hook L Myrtaceae 47.62 ± 1.52 68.18 ± 1.52Eupatorium adenophorum Spreng. T Asteraceae 34.78 ± 1.53 65.00 ± 0.58E. cannabinum Linn. W Asteraceae 52.17 ± 0.58 31.81 ± 3.60E. odoratum Linn. T Asteraceae 44.44 ± 1.52 56.55 ± 3.05Glycosmis pentaphylla (Retz.) Corr.;

Hook.L Rutaceae 45.00 ± 2.08 62.50 ± 1.00

Grangea maderaspatana (L.) Poir. T Asteraceae 48.96 ± 2.19 23.04 ± 1.20Leonotis nepetaefolia R. Br. T Lamiaceae 71.43 ± 1.15 57.14 ± 0.58Leonurus sibiricus Linn. L Lamiaceae 52.00 ± 2.00 53.84 ± 2.40Lippia alba Rich. L Verbenaceae 60.87 ± 1.57 55.00 ± 1.00Nepeta hindostana Linn. W Lamiaceae 70.00 ± 1.00 35.00 ± 2.08Ocimum canum Sims W Lamiaceae 83.63 ± 2.51$ 78.27 ± 1.52$

O. gratissimum Linn. W Lamiaceae 59.09 ± 1.12 52.17 ± 1.52Polygonum glabrum Willd. T Polygonaceae 13.40 ± 1.52 40.00 ± 2.00Salvia plebeia R. Br. W Lamiaceae 86.67 ± 0.58$ 89.09 ± 1.00$

Severinia buxifolia Tenore W Rutaceae 56.52 ± 1.52 15.79 ± 3.21Siegesbeckia orientalis Linn. T Asteraceae 9.50 ± 0.40 45.73 ± 2.51Zingiber zerumbet (L.) Sm. L Zingiberaceae 84.78 ± 1.0$ 80.00 ± 0.58$

Note: T – twig, S – shoot, L – leaf, W – whole part. ⁄Oil concentration – 0.36μl/ml. #Values given are meanof three replicates ± Standard Deviation. $Significantly different at p< 0.05.

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acetylcholine esterase in insects (Re et al. 2000). Our recent report on chemical analysisof C. pentaphylla oil revealed that it is a mixture of methyl eugenol (38.1%), sabinene(24.7%), α-terpinolene (13.8%), limonene (7.8%) and safrole (6.7%) (Pandey et al.2012). The insecticidal constituents of many essential oils are mainly terpenes. Theoutstanding position of sabinene, α-terpinolene, DL-limonene, safrole, β-myrcene andZ-β-ocimene for the control of stored product pests has already been investigated(Regnault-Roger and Hamraoui 1995; Lopez et al. 2010) which confirms that strongtoxic property of Clausena oil is mainly due to the presence of aforesaid components.These active compounds present in the oil might show neurotoxic mode of action byaffecting the octopaminergic system of pulse bruchids and cause their mortality.

Essential oils are a mixture of organic substances of heterogeneous groups, levelof which may vary with plants growing in different ecological situations. Hence, thequality of biologically active essential oils must be standardised in order to get thereproducible results (Rehman et al. 2007). In present study, therefore, quality of the oilwas standardised by its various physicochemical properties. Oil was light yellow incolour and had a specific gravity of 1.2415; it was dextrorotatory (+0.12°28′ at 22 °C),slightly acidic, showed presence of phenols and good solubility in various organicsolvents but was insoluble in water (Table 4). The toxicity of the oil persisted for12months of storage and thermostable up to 120 °C against both the test insects.Further, the autoclaving of the oil did not affect on its toxicity.

The moisture content of the collected seeds was found to be 11.9%, which is nearthe safe level for storage. The Clausena oil showed its efficacy in control of pests asso-ciation with pigeon pea seed samples when it was tested as fumigant. The oil signifi-cantly protected pigeon pea seeds up to six months from insects’ infestation and noindividual of insect species was recorded. The seed samples of control sets exhibitedpresence of C. chinensis and C. maculatus. There was 35 and 28% weight loss and 41and 38% seeds damage due to pulse bruchids in control sets when stored in gunny bagsand glass containers, respectively (Table 3). Thus, in conclusion, present results

Table 2. Insecticidal activity of potent essential oils against Callosobruchus species.

Essentialoils

Oilconcentration

(μl)

Pulse bruchids#

C. chinensis C. maculatus

Percentagemortality

LD50 value(μl)

Percentagemortality

LD50 value(μl)

C. pentaphylla 5 81.60 ± 0.00a 2.7 89.30 ± 0.00a 2.410 100 ± 0.00a 100 ± 0.00a

20 100 ± 0.00a 100 ± 0.00a

O. canum 5 42.60 ± 0.57c 5.8 37.67 ± 0.57c 7.910 74.62 ± 1.52b 67.51 ± 1.52b

20 94.35 ± 0.57a 89.68 ± 2.00a

S. plebeia 5 23.56 ± 0.57d 14.5 21.98 ± 0.39d 16.410 42.29 ± 0.27c 45.14 ± 1.51c

20 68.33 ± 2.00b 58.97 ± 1.72b

Z. zerumbet 5 16.58 ± 0.57d 16.8 32.61 ± 0.39c 18.510 34.71 ± 1.20c 42.74 ± 1.51c

20 63.94 ± 2.00b 55.62 ± 1.74b

Note: #Values given are mean of three replicates ± Standard Deviation, within individual row values withdifferent superscript are significantly different with each other at p< 0.05.

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Table3.

Percentageweigh

tloss

andseed

damageof

stored

pigeon

peaseedstreatedwith

C.pentap

hylla

oilandsynthetic

fumigants.

Treatment

Con

centratio

nin

μl/m

l

Percentageweigh

tloss

Percentageseed

damage

FDIindex(%

)

Gun

nybag

Glass

container

Gun

nybag

Glass

container

Gun

nybag

Glass

container

Clausenaoil

0.29

0.00

±0.00

a0.00

±0.00

a0.00

±0.00

a0.00

±0.00

a10

0±0.00

a10

0±0.00

a

0.58

0.00

±0.00

a0.00

±0.00

a0.00

±0.00

a0.00

±0.00

a10

0±0.00

a10

0±0.00

a

Aluminium

phosph

ide(56%

)0.29

25.00±0.50

c14

.00±0.00

b28

.00±2.00

c21

.60±1.20

c16

.6±0.57

d33

.3±1.30

c

0.58

14.00±0.25

b5.00

±0.29

b16

.00±1.12

c18

.90±0.57

c42

.8±0.94

c69

.70±3.10

b

Ethylenedibrom

ide(83%

)0.29

6.00

±0.24

b6.00

±0.00

a10

.00±0.00

b8.00

±1.15

b70

.70±2.20

b64

.70±1.20

b

0.58

4.00

±0.00

a0.00

±0.00

a5.00

±0.90

b0.00

±0.00

a79

.50±1.10

b10

0±0.00

a

Con

trol

35.00±1.00

d28

.00±1.80

c41

.00±2.00

d38

.00±1.80

d

Note:

#Valuesgivenaremeanof

threereplicates±StandardDeviatio

n,with

inindividual

row

values

with

differentsuperscriptaresignificantly

differentwith

each

otherat

p<0.05.

FDI%

(Feeding

DeterrencyIndex)=C�T

�10

0/C+T,

where

CandTaretheweightloss

incontrolandfumigated

sets,respectiv

ely.

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revealed that essential oil of C. pentaphylla could be used as an alternative to developless toxic treatment systems in protecting pigeon pea seeds from insect invasion atfarmer level.

AcknowledgementsThe authors thank the head, Department of Botany, DDU Gorakhpur University, Gorakhpur forproviding necessary lab facilities, to CST UP Lucknow for financial support and to staff, BSIDehradun to validate the authentication of plant specimens.

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Table 4. Physicochemical properties of Clausena oil.

Parameters Properties

Colour Light yellowSpecific gravity 1.2415 at 25 °CSpecific rotation +0.12°28′ at 22 °CRefractive index 1.529 at 26 °CAcid value 2.992Saponification number 52.36Ester number 49.37Phenolic content PresentSolubility 1:1 soluble in 90% alcohol, 1:1 in benzene, chloroform, hexane and

ethyl acetate,1:2 in acetone and ether but insoluble in water

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