J Pest Sci (2009) 82:149–154

DOI 10.1007/s10340-008-0233-x

ORIGINAL PAPER

Insecticidal and repellent activities of medicinal plant extracts against the sweet potato whiteXy, Bemisia tabaci (Hom.: Aleyrodidae) and its parasitoid Eretmocerus mundus (Hym.: Aphelinidae)

Mohammad S. Al-mazra’awi · Mazen Ateyyat

Received: 3 April 2008 / Revised: 21 October 2008 / Accepted: 27 October 2008 / Published online: 14 November 2008© Springer-Verlag 2008

Abstract Toxicity and repellent activities of aqueousextracts of nine medicinal plants were evaluated on diVer-ent life stages of the sweet potato whiteXy, Bemisia tabaci.Tomato plants infested with whiteXies were dipped in 10%(wt/wt) of each plant extract for toxicity evaluation. Repel-lency was evaluated in a choice experiment with detachedtomato leaves. All extracts evaluated were relativelyineVective against the adult stage. Extracts of Ruta chale-pensis, Peganum harmala and Alkanna strigosa were eVec-tive in reducing the numbers of B. tabaci immatures similarto the reduction observed in the imidacloprid treatment.These three extracts were not detrimental B. tabaci parasitoid,Eretmocerus mundus. In addition, the plant extracts Urticapilulifera and T. capita were repellent to B. tabaci adults.These results indicate that the extracts from the plantsR. chalepensis, P. harmala and A. strigosa could act as apotential source for natural product developed for B. tabacimanagement.

Keywords WhiteXies · Botanicals · Repellency · Ruta chalepensis · Peganum harmala · Alkanna strigosa

Introduction

The sweet potato whiteXy, Bemisia tabaci Genn. is one ofthe most notorious insect pests in the subtropical and tropi-cal parts of the world. The insect is polyphagous attackingmore than 600 plant species worldwide (Gennadius 1989).Plant damage is caused by the transmission of plant viruses,direct feeding, plant physiological disorders, honeydew pro-duction and associated fungal growth (Oliveira et al. 2001).EVective B. tabaci control relies primarily on a single classof insecticides, the neonicotinoids (McKenzie et al. 2005).Such reliance is expected to lead to increased tolerance orthe development of resistance in addition to the adverseeVects on non-target organisms (Palumbo et al. 2001).

Historically, plants and plant derived materials played animportant role in the management of pests. Plants producediVerent types of secondary metabolites that are believed tobe a corner stone in plant natural defense. Monoterpenes,sesquiterpene lactones and triterpenes are examples of suchmetabolites that may have commercial applications (Hey-wood et al. 1977; Barney et al. 2005). At present, someplant-derived products are used against wide variety ofpests (Isman 2006). For example, neem oil obtained fromthe seeds of the Indian neem tree, Azadirachta indica(Meliaceae), is eVective against soft-bodied insects andmites and is also useful in the management of phytopatho-gens (Isman 2006). Azadirachtin, one component of theneem seed extract and it is a triterpene limonoid, is widelyused as an insect antifeedant and a growth regulator (Imma-raju 1998). Plant essential oils, which have long been usedas fragrances and food Xavorings, demonstrated fumigantand contact insecticidal activities to a wide range of pests(Regnault-Roger 1997). Such activity resulted in commer-cial production of essential oils by many botanical sources(Isman 2006). Botanical pesticides are generally regarded

Communicated by C. Cutler.

M. S. Al-mazra’awi (&)Department of Plant Production and Protection, Al Balqa’ Applied University, Assalt 19117, Jordane-mail: m_mazrawi@yahoo.com; m.mazrawi@bau.edu.jo

M. AteyyatAsh-Shoubak University College, Al Balqa’ Applied University, Assalt 19117, Jordan

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as more eco-friendly than synthetic pesticides. For exam-ple, the above-mentioned botanicals are characterized bylow mammalian toxicity, reduced impact on non-targetorganisms and short persistence in the environment(Georges et al. 2007). Thus, the current study was initiatedto investigate the insecticidal and repellent activities ofselected plants on B. tabaci and its parasitoid Eretmocerusmundus Mercet. The plants under study have long beenused for medicinal and/or nutritional purposes in the Medi-terranean region (Ali-Shtayeh et al. 2000). For example, theplants Urtica pilulifera L., Ruta chalepensis L. and Alk-anna strigosa Boiss. & Hohenh, which are included in thisstudy, were mentioned by informants for use against rheu-matism and arthritis (Ali-Shtayeh et al. 2000).

Materials and methods

B. tabaci culture

Bemisia tabaci was cultured in a controlled greenhousecompartment at 24 § 2°C and a 16-h photoperiod on pottedcotton plants, Gossypium hirsutum L. The plants weregrown in 15 cm diameter pots Wlled with a mixture of 1:1sand and peat moss. To obtain B. tabaci immatures of uni-form ages, tomato plants (variety Guardian, Enza Zaden,Jordan) with 4–5 leaves were exposed to oviposition byplacing within the infested cotton plants in the culture.After 24–48 h oviposition period, plants were removedfrom the culture and all adult B. tabaci were aspirated fromthem. The plants were then placed in B. tabaci free green-house compartment at 24 § 2°C and a 16 h photoperiodwhere B. tabaci eggs were allowed to develop for 9–10 days to second instar nymphs, 11–12 days to third instarnymphs and 14–15 days to the pupa.

Plant extracts

Nine medicinal plants belonging to eight families (Table 1)were used in this study (Table 1). The plants were collected

from their natural habitats from diVerent parts in Jordan.Four to Wve plants were collected from each plant species.The plants were in the early Xowering stage when collectedexcept for T. capitatus that were collected before Xowersappear. The selected parts of each plant were left to air dryfor 4–5 days before grinding using a mortar and pistil toform a powder. Suspensions of 10% wt/wt of each plantpowder to sterile distilled water were prepared and thenallowed to boil for 10 min. The suspensions were allowedto cool overnight before Wltering them through a cheesecloth to separate large particles. The extracts were preparedshortly before application. Tween 80 (Tedia Company,Inc., 1000 Tedia way, FairWeld, OH, USA) at a rate of0.02% was added to the extracts before application toimprove adherence to treated plants.

EVects on B. tabaci development

The mortality of B. tabaci eggs, second and third instarnymphs and the pupa were evaluated using a leaf dip bio-assay. Whole tomato leaves infested with eggs, second andthird instar nymphs or pupa of B. tabaci as described abovewere trimmed with a razor blade so that only the terminalleaXet remained. While still attached to the plants, the ter-minal leaXets were immersed individually in one of theextracts for 5 s and were left until air dried. Additionaltomato leaXets were dipped in distilled water as a negativecontrol and in imidacloprid (ConWdor® 200SC, Bayer, Jor-dan) at a rate of 0.25 ml/l, as positive control. After drying,number of eggs, second and third instar nymphs and pupaof B. tabaci were counted on each leaXet. The number ofeggs, second and third instar nymphs and pupa ranged from55 to 90, 35 to 70, 30 to 45 and 20 to 35 per leaXet, respec-tively. There were Wve plants (replicates) for each plantextract, distilled water, imidacloprid and stage. Treatedplants were incubated at 24 § 2°C and a 16 h photoperiod.For egg mortality, numbers of unhatched eggs and newlyemerged nymphs were counted for 8 days post-application.For second and third instar nymphs, numbers of deadnymphs were counted for 3 days post-application. A nymph

Table 1 Plants species extracts evaluated on diVerent life stages of Bemisia tabaci

ScientiWc name Common name Family name Plant part used

Urtica pilulifera L. Roman nettle Urticaceae Leaves

Anthemis palaestina NA Asteraceae Leaves and stems

Astragalus oocephalus Boiss NA Leguminosae Leaves

Ruta chalepensis L. Fringed rue Rutaceae Leaves and stems

Thymus capitatus L. Wild thyme Labiatae Leaves and stems

Peganum harmala L. Harmal peganum Zygophyllaceae Leaves and stems

Hypericum perforatum L. St. John’s wort Clusiaceae Leaves

Alkanna strigosa Boiss. & Hohenh. NA Boraginaceae Leaves and stems

Rubia tenuifolia NA Rubiaceae Leaves

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J Pest Sci (2009) 82:149–154 151

was considered dead if it was shrivelled or its colorchanged. Nymphs that developed into adults were alsocounted and the percentage of adults that failed to emergewas calculated. For pupal mortality, numbers of emptypupal cases and adults that failed to emerge were countedfor 8 days post-application.

To evaluate the eVect of the plant extract on adults,B. tabaci free tomato leaves were removed from tomatoplants and trimmed with a razor blade so that only the termi-nal leaXet remained. The leaXets were treated by immersingin the tested plant extracts for 5 s. The treated leaXets wereallowed to air dry and then placed individually in leaXetcages. Each leaf cage was prepared by adhering two 9-mmPetri plates together. A 3-mm hole was cut through the twoplates. The tomato leaXets were inserted through the holesso that the leaf blade was placed in the upper plate and theleaf petiole in the lower plate. Another 2 £ 2 cm openingwas made in the cover of the upper plate and covered withultra Wne mesh to provide ventilation. The bottom of thelower plate was Wlled with water amended with N–P–K(20–10–20) fertilizer mixture at a rate of 0.2% to providewater and nutrients for tomato leaXets. A total of 20 B. tab-aci adults immobilized temporarily by placing in a fridgefor 15 min were placed inside each cage. There were Wvereplicates (leaf cages) for each plant extract, imidaclopridand distilled water which served as a control. The cageswere incubated at 24 § 2°C and a 16 h photoperiod. Num-bers of dead B. tabaci adults were recorded for 3 days post-application. An adult was considered dead if it did notmove after probing with a camel hair brush.

Adult repellency

Detached tomato leaXets were prepared as above. Half ofthe leaXets were treated individually with one of the testedextracts by immersing for 5 s. The treated leaXets were thenallowed to air dry. After drying, both treated and untreatedleaXets were individually inserted into 25 ml sterile glassvials Wlled with sterile distilled water. To evaluate therepellent eVect of the plant extracts, treated and anuntreated leaXets were placed inside a clear plastic jar(30 £ 20 £ 25 cm height) covered with Wne netting mate-rial. After immobilization in a fridge for 15 min, 50 B. tab-aci adult were placed in a Petri plate in the middle distancebetween the two leaXets. The number of B. tabaci adultsattracted to each leaXet was recorded after 3 h. There weresix replicates for each plant extract repellency test.

Mortality of E. mundus

Based on the results from the previous bioassays, extractsfrom the plants R. chalepensis, P. harmala and A. strigosawere evaluated for their toxicity against B. tabaci parasitoid,

Eretmocerus mundus. B. tabaci pupae that were naturallyparasitized by E. mundus on bean plants, Phaseolus vulga-ris L. were used in the tests. The tests were conducted usinga laboratory glass-slide bioassay (Avery et al. 2004). Fromeach extract, ten droplets (10 �l each) were placed on asterile glass slide as two rows on each side of the slide.Slides with droplets of sterile distilled water acted as thecontrol. B. tabaci parasitized pupae were placed individu-ally on each droplet. After drying in a laminar hood, theslides were placed in sterile Petri plates lined with moistWlter paper. The plates were incubated in a growth chamberat 24 § 2°C and a 16 h photoperiod. There were six plates(replicates) for each tested plant extract. The numbers ofdead parasitized pupae was counted 48 h post-application.A parasitized pupa was considered dead if it was shrivelledor its color changed. The parasitized pupae were kept for10 days until the parasitoids emerged from them. The num-bers of emerged parasitoids was recorded and the identiW-cation of the parasitoid was conWrmed.

Statistical analysis

Data were corrected for control mortality using Abbott’s(1925) formula before analysis. PROC univariate, residualanalysis was applied to test if the data met the assumptionsof analysis of variance (ANOVA). When assumptions werenot met, the data were arcsine transformed. Percent mortalityof B. tabaci adults, immatures and parasitized pupae byE. mundus as well as the percentage of adults that failed toemerge were arcsine square-root transformed before sub-jecting to one-way ANOVA (PROC GLM, SAS Institute2002). Means were separated using the Student–Newman–Keuls test (SNK) multiple range test. To calculate the over-all mortality, percentages of unhatched eggs, mortality ofsecond and third instar nymphs and adults were averagedfor each plant extract. Repellency data were analyzed usingpaired t tests in which the repellency eVect for each plantextract was analyzed separately. Repellency was consideredsigniWcant if the calculated t value exceeded the tabulatedt value. The type I error rate (%) was set at 0.05 level for alltests. Mortality data were back-transformed to their originalscales for presentation in tables.

Results

B. tabaci mortality

Statistical analysis of mortality data showed that theselected medicinal plants have a signiWcant eVect on B. tab-aci egg hatching (F9,40 = 10.2, P < 0.01) and mortality ofthe second instar nymph (F9,40 = 6.9, P < 0.01), the thirdinstar nymph (F9,40 = 9.4, P < 0.01) and the adult

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(F9,40 = 6.8, P < 0.01). Percentage of unhatched eggstreated with the medicinal plants ranged between 0 and33% (Table 2). The highest percentage of unhatched eggswas achieved by the imidacloprid treatment. However, theimidacloprid treatment was not signiWcantly diVerent thanA. strigosa, and R. tenofolia extracts treatments (Table 2).

For the second instar nymph, the extracts of P. harmala,A. palaestina and R. chalepensis resulted in 80, 77 and 67%mortality, respectively. These mortalities were not signiW-cantly diVerent than imidacloprid (Table 2). For the thirdinstar nymph, R. chalepensis and A. strigosa resulted inmore than 50% mortality (Table 2). These mortalities weresigniWcantly lower than the imidacloprid treatment whichresulted in 87% mortality (Table 2). Adults treated with thetested plant extracts suVered signiWcantly low mortalitycompared to those treated with imidacloprid. The highestadult mortality of 27% was achieved by exposing adults tothe extract of R. chalepensis which did not diVer signiW-cantly than the rest of the tested extracts (Table 2). Whenthe eVect of each plant extract was averaged over mortalityof B. tabaci eggs, second and third instar nymph and adultsfor each plant extract results showed that the highest overalleVect was for imidacloprid followed by R. chalepensis,P. harmala and A. strigosa. The overall mortality for imi-dacloprid and the plant extracts were 71, 41, 39 and 39%,respectively (Table 2).

Adult emergence

Adult emergence from the pupal stage was signiWcantlyaVected after treatment of the second instar nymph(F9,40 = 5.7, P < 0.01), the third instar nymph (F9,40 = 4.1,P < 0.01) and the pupa (F9,40 = 5.8, P < 0.01) with thetested plant extracts. Percentage of adults that failed toemerge reached 73 and 70% after treating second instarnymph with A. oocephalus and P. harmala, respectively(Table 3). These percentages did not diVer signiWcantlyfrom imidacloprid treatment but were signiWcantly higherthan the rest of the plant extracts which resulted in failure toemerge percentages that ranged from 0 to 22% (Table 3).For the third instar nymph, failures to emerge percentageswere low and ranged from 1 to 18% with no signiWcantdiVerences among the tested extracts and imidacloprid(Table 3). Similarly, treating pupal stage resulted in lowfailure of emergence percentages that were signiWcantlylower than imidacloprid but with no signiWcant diVerencesamong the tested extracts (Table 3).

Adult repellency

In choice experiments, fewer B. tabaci adults were signiW-cantly attracted to tomato leaves treated with U. piluliferaand T. capita extracts 3 h post-application compared tountreated leaves. No signiWcant diVerence in repellency toB. tabaci adults was found for rest of the tested plantextracts (Table 4).

Table 2 Percent mortality of diVerent life stages of Bemisia tabacitreated with plant extracts and imidacloprid

A Data were arcsine transformed before analysis and back-trans-formed in the table. Mortality percentages were corrected for controlmortality by using Abbott’s formulaB Overall mortality was calculated by averaging the percentages of un-hatched eggs, mortality of second and third instar nymphs and adultsfor each plant extractC Mean within columns with diVerent letters diVer signiWcantly at 0.05level using Student–Newman–Keuls (SNK) multiple range test

Treatment % MortalityA

Life stage

Egg Second Third Adult OverallB

Imidacloprid 49Ca 90a 87a 59a 71a

P. harmala 26bcd 80a 49bcd 1b 39ab

A. palaestina 14bcd 77a 18def 6b 29ab

R. chalepensis 9bcd 67ab 60b 27b 41ab

A. strigosa 33ab 49bc 53bc 20b 39ab

A. oocephalus 1cd 48bc 14ef 6b 17b

U. pilulifera 8cd 43bc 23def 3b 19b

H. perforatum 13bcd 41bc 28cdef 12b 24b

R. tenofolia 28abc 27c 10f 0b 17b

T. capita 0d 21c 44bcde 14b 20b

Table 3 Percent of Bemisia tabaci pupae that failed to emerge to theadult stage following treatment of diVerent life stages with plantextracts and imidacloprid

A Data were arcsine transformed before analysis and back-trans-formed in the table. Mortality percentages were corrected for controlmortality by using Abbott’s formulaB Mean within columns with diVerent letters diVer signiWcantly at 0.05level using Student–Newman–Keuls (SNK) multiple range test

Treatment % MortalityA

Stage

Second Third Pupa

Imidacloprid 66a 6a 28a

A. oocephalus 73Ba 3a 0b

P. harmala 70a 6a 3b

A. palaestina 22b 12a 0b

H. perforatum 20b 7a 4b

T. capita 4b 2a 0b

R. tenofolia 2b 3a 0b

A. strigosa 0b 15a 2b

R. chalepensis 0b 1a 0b

U. pilulifera 0b 18a 0b

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J Pest Sci (2009) 82:149–154 153

Morality of E. mundus

The extracts of R. chalepensis, P. harmala and A. strigosashowed higher eYcacy against B. tabaci than the othertested plant extracts. Thus, they were tested for their eVecton E. mundus. Analysis of variances showed that there wasno signiWcant diVerence in mortality of E. mundus(F2,15 = 1.0, P = 0.38) and in adult emergence (F2,15 = 2.4,P = 0.13) when treated with any of the extracts. The mor-tality of E. mundus was 24, 12 and 8% for R. chalepensis,P. harmala and A. strigosa, respectively. Percentages ofE. mundus adults that failed to emerge were 28, 15 and 7%for A. strigosa P. harmala and R. chalepensis, respectively.

Discussion

With the increasing demand for more eco-friendly productsfor pest management, plants may be valuable sources fornatural pest control products. The current study demon-strated that extracts from the plants R. chalepensis, P. har-mala and A. strigosa were the most promising for thecontrol of B. tabaci resulting in more than 50% mortality ofthe immature stages. A previous study showed that an artiW-cial diet containing 10% R. chalepensis extract caused 46%mortality to the feeding mahogany shoot borer larvae, Hyp-sipyla grandella (Zeller) (Mancebo et al. 2001). Similarly,extracts from P. harmala showed insecticidal eVects on thestored grain pest Tribolium castaneum (Herbst) (Jbilouet al. 2006) and the desert locust Schistocerca gregaria(Forskal) (Abbassi et al. 2003). The insecticidal activity inP. harmala was attributed to alkaloid compounds whichreduced female fecundity and egg hatching of the locust

(Abbassi et al. 2003). For A. strigosa, insecticidal activityhas not been previously reported. The insecticidal activityof these promising plant extracts were mainly against thesecond and third nymphal stages of B. tabaci. Low eYcacywas noticed against the egg stage of B. tabaci (Table 2).Eggs are usually regarded less susceptible to insecticidescompared to other stages. For example, the hatching rate ofthe mosquito, Culex molestus was unaVected by sequiter-pene alcohol derived from Australian sandalwood, Santa-lum spicatum which reduced the survivorship and longevityof the mosquito larvae (SpaVord Jacob et al. 2007). Simi-larly, the tested plant extracts did not aVect the emergenceof the adults after treating the second and third instarnymphs and the pupa. The exception was the treatment ofthe second instar nymph with A. oocephalus and P. har-mala (Table 3). Again, pupal stage is usually regarded moreresistant to insecticides and other mortality factors.

All tested plant extracts were ineVective against the adultB. tabaci (Table 2). In this experiment, adult whiteXieswere not immersed directly in the tested extracts as did theimmatures. This might suggests that the toxic substances inextracts act as contact poisons rather than stomach poisons.Most of the extensively used botanicals such as pyrethrum,neem and essential oils act as contact insecticides althoughneem has some systemic action (Thoeming et al. 2003).

The search for deterrents or repellents is imperative fordeveloping less toxic pest management tools. The remark-able success of azadirachtin as an antifeedant in the 1980sincreased the attention towards such compounds (Isman2006). The current study showed that the plant extractsU. pilulifera and T. capita were repellent to B. tabaciadults. Thymus spp. have long been known for their repel-lent eVect on insects. For example, thyme oil provided 135and 105 min protection against Aedes aegypti and Anophe-les albimanus, respectively (Curtis 1990). Repellency ofT. vulgaris is attributed to monoterpenes such as carvacrol,�-terpinene and thymol derived from the essential oil ofthyme (Park et al. 2005). Similarly, R. chalepensis at 50%concentration resulted in 91.6% protection of test subjectsfrom mosquitoes outperforming the commercial repellentneem (Hadis et al. 2003). Urtica dioica L. was also foundto be repellent to the bean weevil, Acanthoscelides obtectusSay (Jovanovic et al. 2007).

The family Aphelinidae contains many B. tabaci para-sitic wasps including the most important genus Eretmoce-rus mundus is indigenous to the Mediterranean region andis used commercially for B. tabaci management in manyparts of the world (Urbaneja et al. 2007). The three mostpromising plant extracts (A. strigosa, P. harmala andR. chalepensis) were tested to determine if they adverselyaVect E. mundus. The results showed that the extractsP. harmala and R. chalepensis were not detrimental for theparasitoid; however, A. strigosa adversely aVected the

Table 4 Mean number (§SE) of Bemisia tabaci adults attracted totomato leaXets 3 h post-treatment or no treatment with diVerent plantextracts

a The diVerence between treated and untreated was considered signiW-cant if calculated t value exceeded tabular t value. Tabular t value =1.94 (�� = 0.05 and n = 6)

Plant Mean number of adults

Treated Untreated t valuea

P. harmala 16.2 (0.98) 16.5 (1.91) 0.15

H. perforatum 12.0 (1.29) 11.0 (3.93) ¡0.29

A. strigosa 8.7 (2.78) 10.0 (1.34) 0.79

R. tenofolia 12.0 (2.88) 16.3 (2.95) 1.24

U. pilulifera 11.5 (1.41) 15.3 (2.62) 2.16

A. palaestina 12.3 (1.82) 14.3 (1.48) 0.82

A. oocephalus 10.5 (1.23) 8.3 (1.12) ¡1.19

R. chalepensis 5.7 (1.33) 9.2 (2.12) 1.31

T. capita 14.2 (1.25) 18.8 (1.78) 3.02

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emergence of E. mundus from B. tabaci parasitized pupa.The identiWcation of selective chemicals with little or noharmful eVects on the B. tabaci parasitoid is a desirablegoal for the development of sound and eVective manage-ment strategies.

The current study screened nine plant extracts for theireYcacy against diVerent stages of B. tabaci as well as therepellency for the adult stage. A. strigosa, P. harmala andR. chalepensis showed substantial insecticidal activityagainst B. tabaci immature stages. In addition, T. capitaand R. chalepensis showed a repellent eVect against B. tab-aci adults. This work identiWes these plant extracts aspotential sources for natural products to be developed forB. tabaci management. It also opens avenues for more stud-ies on the isolation, identiWcation and evaluation of eYcacyof insecticidal compounds in these plants.

Acknowledgments This research was supported by the Deanship ofScientiWc Research, Al Balqa’ Applied University. We thank EbtisamAl-awamleh for her help in the research work.

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