Biopesticidal value of selected essential oils against pathogenic fungus, termites, and nematodes

Biopesticidal value of selected essential oils against pathogenic fungus, termites, and nematodes
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  Biopesticidal value of selected essential oils against pathogenicfungus, termites, and nematodes Aditi Gupta, Satyawati Sharma * , S.N. Naik Centre for Rural Development and Technology, Block III, Indian Institute of Technology, IIT Delhi, Hauz Khas 110016, India a r t i c l e i n f o  Article history: Received 9 September 2010Received in revised form28 October 2010Accepted 1 November 2010Available online 7 May 2011 Keywords: Essential oilsAnti-termitic activityAnti-fungal activityNematicidal activityMortality a b s t r a c t The biopesticidal potential of six plant-derived essential oils (mint [ Mentha arvensis ], ajwain [ Carumcapticum ], lemongrass [ Cymbopogon citrates ], clove [ Eugenia caryophyllata ], cedarwood [ Cedrus deodara ],and eucalyptus [ Eucalyptus globulas ]) was evaluated against  Odontotermes obesus  (termites),  Fusariumoxysporum  (plant pathogenic fungi), and  Meloidogyne incognita  (nematodes). In the case of termites,a  “ no-choice ”  bioassay revealed that the mint oil gave the best results (100% mortality in 30 minwith 10%oil and in 10 h with 0.12% oil) followed by the lemongrass and ajwain oils. The disc diffusion method wasadopted to test the anti-fungal activity of the essential oils and it was found that the clove oil gave themaximum inhibition measured in terms of the average inhibition zone diameter (5.3  0.2 cm with 10%oil and 6.6  0.9 cmwith 20% oil), followed by the ajwain oil. To check the anti-nematicidal activity of theessential oil, in-vitro growth chamber experiments revealed that eucalyptus oil was the most ef  fi cient(100% mortality in 6 h with 1000  m l l  1 oil and in 30 h with 125  m l l  1 oil), followed by the ajwain oil. Theuse of the crude oils at low concentrations provided satisfactory results at the laboratory level againstthese pathogens, and needs further evaluation in  fi eld trials.   2011 Elsevier Ltd. All rights reserved. 1. Introduction Inrecentyears,asigni fi cantincreaseintheyieldoffoodgrainsandothercropshasbeenrequiredtofeedtheworld ’ sgrowingpopulation.However, various pests, including weeds, insects, and plant viruses,can reduce crop productionby 25 e 50% (Pimentel et al.,1991; Oerke,2006).Accordingto LevetinandMcMahon(2003),about70%ofcrop diseases are caused by fungi. The extent of diseases caused bynematodes in the agricultural systems is far from fully understood.Theyieldlossesby plantparasiticnematodes,inIndiaalone,amounttobillionsofrupeeseveryyear.Termitesalsocauseahugeamountof damagewhentheydestroywoodandwoodenproducts(Vermaetal.,2009). Control and repair costs due to Formosan subterraneantermites in New Orleans, for example, have been estimated to reach$300 million annually (Suszkiw,1998). In India, they are responsiblefor the loss of 15 e 20% of the maize yield and about 1478 millionrupees( Joshietal.,2005;Vermaetal.,2009).Othercountriesaswellexperience signi fi cant crop losses caused by these pests, so control-ling them is an important economic and agricultural issue.The green revolution introduced the use of chemical pesticidesfor managing pests. To defeat plant diseases, farmers/growers haveto use heavy doses of chemical pesticides, which, although have animmediate effect, are not always affordable, and may have delete-rious effects on plants, soil, and animals. Moreover, continued useleads to an increase in pest resistance and enhanced pest resur-gence. In this context, efforts are being made worldwide to replacethese chemicals with biological alternatives (biopesticides), whichare less toxic to the environment.Through the ages, plant-derived oils (essential as well as seedoils) have evoked interestas natural products that hold promise fortheir potential in pest management (Regnault-Roger, 1997; Isman,2000; Akhtar, 2000; Oka et al., 2000; Zhu et al., 2001; Gandhiet al., 2006; Chaieb et al., 2007; Bakkali et al., 2008). Among theplant-derived oils, essential oils have been shown to possessinsecticidal, anti-fungal, and antibacterial properties (Burt, 2004).The present paper describes testing the ef  fi cacy of selected plant-derived essential oils as biopesticides against termites ( Odonto-termes obesus ), plant pathogenic fungus ( Fusarium oxysporum ), andplant nematode ( Meloidogyne incognita ). 2. Materials and methods  2.1. Essential oils Six different essential oils were selected based on a literaturesurvey, as well as their availability and use in traditional medicine. *  Corresponding author. Tel.:  þ 91 11 2659 1116,  þ 91 11 2659 1121. E-mail address: (S. Sharma). Contents lists available at ScienceDirect International Biodeterioration & Biodegradation journal homepage: 0964-8305/$  e  see front matter    2011 Elsevier Ltd. All rights reserved.doi:10.1016/j.ibiod.2010.11.018 International Biodeterioration & Biodegradation 65 (2011) 703 e 707  Cedarwood oil was procured from Aum Aromatics Pvt. Ltd., Mandi,H.P., India, and eucalyptus, mint, clove, ajwain, and lemongrass oilswere procured from Gogia Chemicals, Okhla, New Delhi. Theseessential oils were analyzed for their major constituents using gaschromatography e mass spectrometry (GC e MS) (Gogia Chemicals,Okhla, New Delhi).  2.2. Test organismsO. obesus  termites were collected from the local environment of the Indian Institute of Technology (IIT), Delhi, and acclimatized forabout 24 h by keeping them in a BOD incubator at 28    1   C andrelative humidity of 80 e 85%.  F. oxysporum  was procured from IARI,Delhi.  M. incognita  nematodes were collected from the infectedbrinjal roots at the micromodel, IIT, Delhi, and incubated in a BODincubator at 28  1   C and 80 e 85% RH.  2.3. Anti-termitic assay The  “ no-choice ”  bioassay method of  Kang et al. (1990) was fol-lowed to evaluate the anti-termitic activity of the six selectedessentialoils.Petridishes(5cmdiameterand1cmhigh) fi lledwithapproximately 15 g of sterilized sand were used to test the toxicityof the selected oils against the workers of the  O. obesus  termites.Samples of 0.12, 0.25, 0.5, 1.0, and10% oil solutions were made inpolypropyleneglycol(PPG)and500- m laliquots(suf  fi cienttospreadoverthewhole fi lterpaper)wereappliedtothe fi lterpapersamples(Whatman No.1, 4.5 cm in diameter). A blank  fi lter paper and  fi lterpapertreated with solventonly were usedas the controls. After the fi lter papers were placed in their respective petri plates,15 workertermites were added to each plate. The dishes were incubated inthe dark at 28    1   C and 80 e 85% RH. A few drops of water wereperiodically sprinkled onto the sterilized sand in the dishes tomaintainsuf  fi cientmoistureforthetermites.Filterpaperandwaterserved as the food for the termites. The whole experiment wasperformed in triplicate and the mean mortality rate was countedafter speci fi c time intervals for 72 h. The data were collected intriplicate.  2.4. Anti-fungal assay Screening of the oils was done by the disc diffusion method(Baueretal.,1966)totesttheanti-fungalactivityoftheselectedoilsagainst the fungal strain  F. oxysporum . The fungal strain wascultured in potato dextrose broth (PDB) at 28   C and 250 rpm for5 e 7 days. The cultures were adjusted to approximately10 8 CFU ml  1 . One hundred microliters of this solution was spreadover the plates containing PDA using a sterile spreader in order toget uniform fungal growth on the plates. Samples of 10 and 20% oilsolution were prepared in PPG for the essential oils and a 30- m laliquot (suf  fi cient to spread over the sterile disc) was pipetted ontoa 6-mm sterile disc (HIMedia Laboratories, Mumbai, India) placedon the agar medium in the petri plates. A blank sterile disc with nooil treatment was used as the control. The petri dishes were incu-bated in a BOD incubator at 28  1   C and 80 e 85% RH for about 5days until maximum growth of the fungus was achieved. Inhibitionzones, if any, were measured using a caliper. The experiments wereperformed in triplicate.  2.5. Nematicidal assay In-vitro growth chamber experiments were monitored to studythe effect of the selected oils on the mortality of   M. incognita second-stage juvenile nematodes. Culturingof the nematodes fromthe infected soil was done according to Cobb (1918). The infectedsoil was mixed with water and allowed to settle for 1 e 2 h. Waterwas decanted and passed through a cascade of sieves of decreasingsize. Retentate from the sieve with mesh size 350 was collected.This mesh size traps the J2 nematode larvae. Culturing of thenematodes was done using double distilled water (DDW), as thenematodes have a tendency to move toward fresh water. Second-stage juveniles were then collected after 48 h in DDW. Populationcounts of the nematodes, done using a stereomicroscope, gave, onaverage, approximately 150 juveniles in 500  m l of the water solu-tion. Approximately 280 e 300 juveniles in 1 ml were introduced ineachwellofthesterilized24-wellplates.Asuitablediluentthathadnil/minimum toxicity to the nematodes had to be chosen to makethe desired oil concentrations of 1000, 500, 250, and 125  m l l  1 .Studies on nematodes are generally performed using water as thesolvent. Since oils are hydrophobic, a suitable surfactant had to beadded to act as a stabilizer to dissolve the oils in the water.Therefore, the essential oils were  fi nally diluted with water con-taining0.5%Tween80v/v,asthesurfactanttoobtainthedesiredoilconcentrations. To each well, 500  m l of the oil solution of a givenconcentration was added and incubated at 28    1   C and 80 e 85%RH. Each treatment had three replicates. The concentration of Tween 80 in the control was equivalent to that in the oils. Thenumber of juveniles that became immotile on exposure to the oilconcentrations and on further dilution with the fresh DDW wereconsidered dead. The mean mortality rate measurements weredone after speci fi c time intervals for 48 h after which the resultsweresubjected toalotoferroras thejuveniles coulddie becauseof agingandnotbecauseof theoilexposure.The datawascollectedintriplicate.  2.6. Statistical analyses The data collected were analyzed by one-way analysis of vari-ance (ANOVA) using SPSS for Windows (version 18.0). Themeasurement of difference was determined according to Duncan ’ smultiple range test (DMRT). Values of   P   <  0.05 were consideredsigni fi cant. Vertical bars in the  fi gures indicate the values of means  standard deviation (SD). 3. Results and discussion  3.1. Chemical components of the essential oils Analyses of the essential oils using GC e MS gave their compo-sitions, which are listed in Table 1.  3.2. Anti-termicidal activity of essential oils Theresultsshowedthatat10%concentrationofessentialoils,allthe termite workers were killed within 30 min. Varying mortalityrates were observed with the oils at concentrations less than 10%.However, essential oil concentrations as low as 0.12% were suf  fi -cient to kill the termite workers within a span of 18 h (Fig.1). Fig. 2 shows the maximum mortality rates of the termite workers withdifferentconcentrationsoftheoils.Itcanbeconcludedfromthebargraph that mint oil is superior to the other oils as it takescomparatively the least amount of time to kill the termite workers,at all concentrations tested. This may be due to the presence of theactive component menthol present in the mint oil. After the mintoil, lemongrass seems to be better than the other oils at 1 and 0.5%butnotattheotheroilconcentrations,asajwainoiltakestheupperhand at 0.25% and at 0.12% both oils show the same results. Eventhough clove oil falls next in the order, it gave the maximummortality, i.e. 100%, at the same time as does lemongrass at 0.5,0.25, and 0.12%. Cedarwood and eucalyptus oil fall last in the  A. Gupta et al. / International Biodeterioration & Biodegradation 65 (2011) 703 e 707  704  ef  fi cacy order. In the present case, the mortality of the termiteworkers might have been caused by the contact with the  fi lterpaper impregnated with the essential oils (Prates et al., 1998). Ascan be seen from the gas chromatography analysis, each essentialoil contains some active terpenoid among their major components(Table 1). A number of different terpenoids in essential oils havebeen known to possess anti-termitic activity (Sharma et al., 1994;Cornelius et al., 1997; Park and Shin, 2005; Koul et al., 2008). Thetoxicity of the mint and ajwain oils may be attributed to the pres-ence of the phenolic components menthol and thymol, respec-tively, while that of the clove oil can be attributed to eugenol(Cornelius et al.,1997; Chen et al., 2002; Park and Shin, 2005; Koulet al., 2008), which contains an ether linkage and a hydroxylattached to the benzene ring (Table 1). The compounds containingan aldehyde group also show signi fi cantly high levels of anti-termitic activity (Chang and Cheng, 2002), and therefore the anti-termitic activity of the lemongrass oil can be explained due to thepresence of an aldehyde group in its major compound citral.Cedarwood oil is known to act as a natural repellant to termiteworkers due to the presence of the active components himachaloland  b -himachalene (Singh and Agarwal,1988), while the activity of the eucalyptus oil might be due to the presence of the oxygenatedcompound cineole in it. According to Seo et al. (2009), phenolicsubstances tend to exhibit stronger anti-termitic activity than thealcohol and aldehyde groups. These results support Seo et al.(2009), too. The activity of the individual components needsto be evaluated to support the reasoning as there is generallya difference between the activity of the individual component andthe crude oil, which contains many other components that mightact synergistically.  3.3. Anti-fungal activity of essential oils The anti-fungal activity of the six selected essential oils against F. oxysporum  were measured in terms of the average inhibition zonediameters of the fungus at 10 and 20% concentrations of each oiltested. The results revealed that the oils had anti-fungal activity of varying magnitudes. Among the essential oils, clove oil showed thebest results, giving the maximum diameter of the zone of inhibition(5.3  0.2 cmwith 10% oil and 6.6  0.9 cmwith 20% oil) followed bythe ajwain, lemongrass, mint, cedarwood, and eucalyptus oil, in thatorder(Fig.3).Also,itcanbeconcludedthateventhoughcloveoilgivesthe maximum zone of inhibition at both 10 and 20% concentrations,lemongrass gives the highest percentage increase in the averageinhibition zone diameter, on increasing the oil concentration from 10to20%,followedbythecloveandthentheajwainoil.Otheroilsdidnotshow any signi fi cant increase on doubling the oil concentrations.Thegreateractivityofthecloveoilmaybeattributedtoitsmajorcomponent, eugenol (Table 1), which is known to possess anti-fungal activity against a variety of species (Tampieri et al., 2005;Chaieb et al., 2007). Ajwain oil is also known to exhibit a broadrange of fungitoxic behavior (Singh et al., 2004), which may beattributed to the presence of its phenolic component thymol. Theanti-fungal activity of the lemongrass oil may be due to the pres-ence of its aldehyde containing the active constituent citral, whilethe impact of the mint oil may be in fl uenced by its cyclohexanolmoiety. These results are in agreement with those obtained by Fig.1.  Plot of percentage mortality of termite workers vs. time with 0.12% oil. Verticalbars in the  fi gure indicate the standard deviation (SD). Fig. 2.  Bar graph showing maximum mortality rates of   O. obesus  workers withdifferent concentrations of selected essential oils.  Table 1 Components of the essential oils.Essential oil Components (%)Cedarwood oil Beta-himachalene (43.9), alpha-himachalene (16.5), gamma-himachalene (11.3),atlantone (17.5), himachalol (2.9), othersMint oil Menthol (80.1), menthone (5.9), neo-menthol (4.3), iso-menthone (2.9),pulegol þ menthyl acetate (1.3), terpeneol (0.3)Eucalyptus oil Cineole (81.9), limonene (6.6), alpha-pinene (5.7), cymene (3.1), beta-pinene (1.5),gamma-terpenene (0.6), myrcene (0.3), othersClove oil Eugenol (86.5), trans-caryophyllene (10.9), alpha-caryophyllene (1.5), othersAjwain oil Thymol (35.9), gamma-terpenene (33.6), cymene (18.8), beta-pinene (1.9),carvacrol (1.2), alpha-pinene (0.4), othersLemongrass oil Citral (77.8), limonene þ traces of eucalyptol (4.0), geraniol (2.7),6-methyl-5-hepten-2-one (2.4), geranyl acetate (1.1), camphene (0.3), othersNumbers in the brackets indicates the percentage of the components present in the plant essential oil.  A. Gupta et al. / International Biodeterioration & Biodegradation 65 (2011) 703 e 707   705  Pandey et al. (2003). Lemongrass, mint, clove, ajwain, and euca-lyptus oils have already been known to exhibit strong fungitoxicbehavior against a number of fungi (Guynot et al., 2003; Suhr andNielsen, 2003; Bansod and Rai, 2008; Kishore et al., 2009). Theresults obtained with the mint and the eucalyptus oil can also besupported by the work of  Matan et al. (2009), in which mint andeucalyptus oil as well as their major constituents have been foundeffective against certain fungal molds. An important observationwas that the clove, ajwain, lemongrass, and mint oils, rather than just inhibiting the growth, also tend to inhibit the fungal sporula-tion, as evidenced by the decrease in the pink color intensity of thefungalgrowth.TheresultsareinaccordancewiththoseobtainedbyTzortzakisandEconomakis(2007),inwhichlemongrassoilinhibitsthe fungal spore production of   Colletotrichum coccodes ,  Botrytiscinerea ,  Cladosporium herbarum , and  Rhizopus stolonifer  . The resultsobtained in these anti-fungal tests clearly indicate that the oilscontaining phenolic moieties in their active constituents performbetter than the others (Manohar et al., 2001).  3.4. Nematicidal activity of the essential oils The mortality rates of   M. incognita  second-stage juveniles withdifferent concentrations of the six selected essential oils aresummarizedinFig.4andFig.5.Theresultsshowdifferentmortality rates with different concentrations of oils. Comparisons show thateucalyptusandajwainoilaresigni fi cantlybetterthantheotheroils,as they show maximum mortality in minimum time at all theconcentrations tested, with eucalyptus oil showing slightly betterresultsat1000 m ll  1 and125 m ll  1 concentrations.Eucalyptusoilisa complex mixtureof phenols, oxides, aldehydes, ketones,alcohols,andethersanditstoxicin fl uencemaybeasynergisticeffectofallitsconstituents. The results obtained here are in agreement with theones obtained by Pandey et al. (2000) and Ibrahim et al. (2006). Ajwain oil is also known to possess good nematicidal activity (Parketal.,2007)andagainthiscanbeattributedtoitsmajorcomponent,thymol.Cloveoilcomesnextintheef  fi cacyorder,followedbymint,cedarwood, and lemongrass oil. Some of the essential oils used inour study have already shown potent nematicidal activity againstthepinewoodnematode(Parketal.,2005).Again,itisexpectedthatthe nematicidal activity of all these oils against  M. incognita  may bedue to their major components, but further studies are still neces-sary to validate this. 4. Conclusions From the present study, it can be concluded that oils are a goodalternative to the harmful chemical pesticides and can be effec-tively used as an ef  fi cient biopesticide against many pathogens liketermites, fungus and nematodes. While mint oil showed compar-atively better results in case of termites and eucalyptus oil for thenematodes, clove oil proved to be the best for inhibiting the fungalgrowth. Ajwain oil showed very good results in each case and thuscan be considered as a viable alternative for other pathogens aswell. The activities of the various oils are attributed to their majorconstituents and that the oils containing phenolic moieties in themshow bettertoxicity than the others tothe pathogens studied. Such fi ndings have been supported by the literature as well. Furtherstudies would still be required for better understanding of thestructure activity relationship as the presence of the otherconstituents in the crude oil de fi nitely modi fi es the in fl uence of itsmajorconstituentalone.Webelievethatthepresentstudytogetherwiththepreviousstudiesonoilssupportthebiopesticidalnatureof the plant derived essential oils. These oils can be used as a cheap,safe and ef  fi cient alternative as well as a supplement, in thedeveloping countries to protect the crops against the various plantpathogens. Additional  fi eld level studies would be needed tofurther validate their potential.  Acknowledgments The authors are grateful to CSIR and NOVOD for their  fi nancialassistance and to Gogia Chemicals, Okhla, New Delhi, for providingthe essential oils and for their GC and GC e MS analysis. Fig. 4.  Plot of percentage mortality of nematode juveniles vs. time with 1000  m l l  1 oil.Vertical bars in the  fi gure indicate the standard deviation (SD). Fig. 5.  Plot of percentage mortality of nematode juveniles vs. time with 125  m l l  1 oil.Vertical bars in the  fi gure indicate the standard deviation (SD). Fig. 3.  Bar graph showing average inhibition zone diameters of two differentconcentrations of the selected essential oils used. Vertical bars in the  fi gure indicatethe standard deviation (SD).  A. Gupta et al. / International Biodeterioration & Biodegradation 65 (2011) 703 e 707  706  References Akhtar, M., 2000. Nematicidal potential of the neem tree  Azadirachta indica  (A. 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