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Acaricidal Activities of Plant Essential Oils from Three Plants on the Mushroom Mite, Luciaphorus perniciosus Rack (Acari: Pygmephoridae).

Byline: Jarongsak Pumnuan, Angsumarn Chandrapatya* and Ammorn Insung

Abstract.- Essential oils of Litsea cubeba, Litsea salicifolia and Melaleuca cajuputi were tested against

Luciaphorus perniciosus by contact and fumigation methods. Contact toxicity bioassay was made by dropping essential oils at rates of 0, 0.06, 0.33, 0.66, 3.3, 6.6, 33, 66 and 99 ul/cm2 into special mite cages. Fumigation was done in a knockdown chamber of 2.5x104 cm3 in size at the concentrations of 0, 0.0012, 0.006, 0.012, 0.06, 0.12, 0.6 and 1.2 ug/cm3. The essential oil of L. cubeba was found to be the most toxic to L. perniciosus by both contact and fumigation methods with LD50 values equaling to 0.932 and 0.166 ug/cm3, respectively, followed by essential oil of L. salicifolia whose LD50 values of 2.793 and 0.410 u g/cm3 were recorded. Essential oil of M. cajuputi demonstrated a low effect on L. perniciosus as compared to those of L. cubeba and L. salicifolia. Essential oil formulations were delivered by using citronella grass or black pepper oils as major components and L. cubeba as minor component. Mite mortality rate increased when 0.01% L.

cubeba oil was added to either citronella grass or black pepper oil at all treatments by contact method.

Keywords: Essential oil, wild plant, fumigant, mushroom mite, Luciaphorus perniciosus

INTRODUCTION

Several mites are known to attack cultivated mushrooms in Thailand.Luciaphorus perniciosus Rack (Family Pygmephoridae) is considered to be the most important mite causing yield losses in mushroom production. They often cause 10-20% yield loss and occasionally total crop loss. Control of mite populations in mushroom farms is remarkably limited and chemical substances are sometimes used during the beginning of growing period. Therefore, only sanitary measures are to be appropriately applied in the mushroom house.

Plant essential oils may provide an alternative means of controlling mushroom mites since they contain a rich array of bioactive chemicals that can be used to control several agricultural pests. To date, there have been many reports regarding the use of essential oils or crude extracts from plants for controlling several, especially phytophagous and parasitic mites.

The essential oil of Chenopodium ambrosioides L. is known to increase the mortality of adults and eggs of two-spotted spider mite,

Tetranychus urticae Koch (Chiasson et al., 2004). Chang et al. (2001) reported that the essential oil of Taiwania cryptomerioides Hayata at the rate of 12.6

ug/cm2 caused 67% and 36.7% mortalities of the house dust mite, Dermatophagoides pteronyssinus (Trouessart) and D. farinae Hughes, respectively. Kim et al. (2003) found that eugenol and its derivatives, acetyleugenol, isoeugenol and methyleugenol showed much lower LD50 values of 0.67, 1.55, 3.71 and 5.41 ug/cm2, respectively, in controlling D. pteronyssinus. In 2008, Insung and Pumnuan reported that fumigation by clove and cinnamon oils at a concentration of 1.2 ug/cm3 completely killed D. pteronyssinus. These two oils demonstrated the LD50 values of 0.092 and 0.232 ug/cm3, respectively.

Raynaud et al. (2000) stated that the acaricidal activity of a dichloromethane extract of Uvaria pauciovulata Hook. F. andamp; Thoms against D. pteronyssinus which had an EC50 of 0.028 g/m2. Akendengue et al. (2003) found that methanol and hexane extracts of U. versicolor Pierre ex Engl. andamp; Diels gave EC50 values of 0.095 and 0.12 g/m2, respectively, and dichloromethane extract of U. klaineana Engler andamp; Diels yielded EC50 value of 0.85 g/m2 in controlling D. pteronyssinus.

Lee (2004) compared the components of oils derived from Foeniculum vulgare fruit oil with benzyl benzoate against D. farinae and D. pteronyssinus. He found that most toxic compound to D. farinae was p-anisaldehyde (11.3 mg/m2) while p-anisaldehyde (10.1 mg/m2) was much more effective against D. pteronyssinus than benzyl benzoate (67.5 mg/m2).

To date, several crude extracts of many plant species were tested against stored product mites,

Tyrophagus putrescentiae Schrank (Kwon et al., 2003; Kim et al., 2003), pig mange mites (Magi et al., 2006) as well as house dust mites (Kim et al., 2006; Rim and Jee, 2006; Saad et al., 2006). As for the mushroom mite, Pumnuan et al. (2008) reported that clove and cinnamon extracts induced 88.7% mortality of L. perniciosus when applied at the rate of 125 ug/cm2. Moreover, dichloromethane extracts of clove and cinnamon showed the highest toxicity against L. perniciosus with the LD50 values of 34.97 and 35.57 ug/cm2, respectively.

The purpose of this study was to investigate the acaricidal activities of some plant essential oils and their formulations on controlling the mushroom mite, L. perniciosus under the laboratory conditions.

MATERIALS AND METHODS

Stock culture of mushroom mites

Colonies of L. perniciosus were obtained from the Department of Agriculture, Ministry of Agriculture and Co-operatives, Bangkok. They were reared on sorghum grain infested with mycelia of Lentinus polychrous Le'v and kept at 27+-2degC.

Plant species and essential oils extraction

Mature fruits of L. cubeba and L. salicifolia were collected at Doi Ang-khang (19o54'N, 99o2'E), Fang district, Chiang Mai province in June 2007. Fresh leaves of M. cajuputi were collected at Kasetsart University, Bangkhen campus, (13o98'N, 48o18'E) in June 2007. The voucher specimens (#CHKU 00022, #CHKU 00023 and #CHKU 00028) were deposited at the Bangkok Herbarium,

Botanical Research Unit, Department of Agriculture, Bangkok, Thailand.

The essential oil was extracted by water-distillation using a Clevenger-type apparatus for 6 h. The superior phase was collected from the condenser, dried over anhydrous sodium sulphate and stored in amber-colored vials at 10-12oC for further experiments.

Experimental treatments Contact toxicity bioassay

A glass tube, 0.4 cm in diameter and 3 cm long with fine nylon mesh on both ends, was used to confine the mite samples. Each glass tube was treated internally with 25 ul of essential oil at various concentrations (0, 0.001, 0.005, 0.01, 0.05, 0.1, 0.5, 1.0 and 1.5% equaling to 0, 0.066, 0.33 0.66, 3.3, 6.6, 33, 66 and 99 ul/cm2, respectively) and 95% ethanol was used as the control. The solution was then distributed evenly around the inner wall of the test tube and allowed to air dry before 10 non-physogastric mites were introduced into each glass tube. Observations were made 12 and 24 h after treatment and the number of dead mites was recorded.

Fumigation

Samples of 10 non-physogastric mites were transferred to the mite cage made out of an acrylic sheet (3x5x0.45 cm) perforated into frustum of cone. The base of cone was 0.25 cm in diameter and covered with a filter paper; the top was 0.5 cm in diameter and covered with a cover glass (1 x 1 cm). All mite cages were placed into the 2.5x104 cm3 knockdown chamber (Burkard Co., England). Essential oils at concentrations of 0 (10% tween-20 in distilled water), 0.002, 0.01, 0.02, 0.1, 0.2, 1.0 and 2.0% with volume of 1.5 ml (or 0, 0.0012, 0.006, 0.012, 0.06, 0.12, 0.6 and 1.2 ug/cm3, respectively) were sprayed into the chamber. The mite cages were left in the chamber for 1 h after the treatment, and mortality of mushroom mites were observed at 12 and 24 h thereafter.

As for commercial use, various essential oil formulations were tested by using essential oils of citronella grass (Cymbopogon nardus (Linn.) Rendle) or black pepper (Piper nigrum Linn.) as a major component and 0.01% L. cubeba as a minor component. As described earlier, the contact toxicity bioassy was used to determine percentage of mite mortality.

Mites were considered dead if their appendages did not move when probed with a small hair brush. Abbot's formula (Abbott, 1925) was used to calculate the actual death rates. The experiment was designed in three completely randomized replicates. The data obtained were statistically analyzed by applying analysis of variance (ANOVA) and Duncan's multiple range tests (DMRT). The LD50 was calculated by the probit method.

RESULTS

The essential oils obtained from three plant species could be used to reduce L. perniciosus numbers under laboratory conditions. Using the contact method, the essential oil of L. cubeba at the rate of 99 ug/cm2 showed the highest toxicity to L. perniciosus, causing 97.5+-4.1% mortality at 12 h, while 97.0+-4.7 and 91.9+-8.9% mortality induced by

L. salicifolia and M. cajuputi were recorded at the same rate (Table I). At this rate, the essential oils of L. cubeba and L. salicifolia caused significantly higher mortality rates as compared to those induced by M. cajuputi oil. Furthermore, L. cubeba and L. salicifolia showed LD50 values of 0.932 and 2.793 ug/cm2 where up to 19.705 ug/cm2 was recorded for M. cajuputi oil.

As the time passed, mortality rates of L. perniciosus increased in all treatments. L. cubeba and L. salicifolia essential oils still induced significantly higher mortality rate at the concentration of 33 ug/cm2 (96-97%) as compared to M. cajuputi oil which caused its highest mortality rate (99%) at the concentration of 66 ug/cm2. However, the activity of all essential oils at the rate of 33 ug/cm2 did not differed significantly (Table I).

Using the fumigation method, the highest mortality rate (78-91%) of L. perniciosus occurred when 1.2 ug/cm3 of L. cubeba, L. salicifolia and M. cajuputi was applied (Table II). In addition, L. cubeba caused significantly higher mortality of L. perniciosus as compared to those mites treated with L. salicifolia and M. cajuputi oils. The LD50 values confirmed this result where 0.16, 0.41 and 0.4 ug/cm3 were recorded for L. cubeba, L. salicifolia and M. cajuputi oils, respectively. At 24 h post treatment, mortality rates of L. perniciosus increased tremendously at all lower concentrations. However, L. cubeba and L. salicifolia oils caused 93-95% mite mortality at the rate of 0.12 ug/cm3 where the higher dose (0.6 ug/cm3) was required for M. cajuputi oil to induced 93% mortality.

Essential oils of either P. nigrum or C. nardus alone could cause death of L. perniciosus adult within 12 h by contact method. However, the mortality rates of L. perniciosus caused by P. nigrum and C. nardus at the rate of 3.3 ug/cm3 was relatively low comparing to those of higher concentrations (Table III). Adding 0.01% L. cubeba oil to P. nigrum and C. nardus oils could increase the mortality rate of the mushroom mite in all treatments where 16% and 45% increases in mortality rates were observed in the formulations of P. nigrum+0.01% L. cubeba oil and C. nardus+0.01% L. cubeba oil at the rate of 3.3 ug/cm2, respectively (Table III).

DISCUSSION

Our results indicated that essential oils of L. cubeba , L. salicifolia and M. cajuputi showed contact and fumigation toxicities against L. perniciosus adults. Similar results were found by Ko Ko (2009) and Ko Ko et al. (2009) where fumigant and contact toxicity effects of L. cubeba,

L. salicifolia and M. cajuputi against Sitophilus zeamais Motschulsky and Tribolium castaneum (Herbst) were shown. Noosidum et al. (2008) reported that Aedes aegypti L. demonstrated clear behavioral escape responses to these three essential oils in both contact and non-contact trials in excito-repellency test chamber.

Insung and Pumnuan (2008) stated that the essential oil of citronella grass (C. nardus) was remarkably toxic to D. pteronyssinus with LD50 value of 0.935 ug/cm3 24 h after fumigation. Moreover, essential oil of P. nigrum showed acaricidal effect on the spider mite, Eotetranychus cendanai Rimando with LC50 of 23.6 ml/l (Sornlek, 2001). George et al. (2009) also reported that essential oil of black pepper at 0.14 mg/cm3 could be used to repel the red mite Dermanyssus gallinae (De Geer) during the first 2 days. Insung et al.

Table I.- Effect of wild plant essential oils on the mortality of Luciaphorus perniciosus Rack by contact toxicity bioassay at 12 and 24 h.

Concentration###12 h###24 h###

([?] g/cm2)###M. cajuputi###L. cubeba###L. salicifolia###%CV###M. cajuputi###L. cubeba###L. salicifolia###%CV

0 (Control)###0.0[?] 0.0 gA1###0.0[?] 0.0 gA###0.0[?] 0.0 hA###-###0.0[?] 0.0 fA###0.0[?] 0.0 dA###0.0[?] 0.0 dA###-

0.066###30.5[?] 12.4 fB###45.6[?] 13.2 fA###44.6[?] 9.0 gA###28.2###89.9[?] 9.1 eA###92.3[?] 7.3 cA###87.9[?] 8.5 cA###9.2

0.33###37.6[?] 12.1 eB###52.3[?] 10.1 eA###50.7[?] 11.2 fA###23.7###92.6[?] 6.4deA###91.9[?] 7.6 cA###90.9[?] 8.8 cA###8.4

0.66###44.9[?] 12.0 dB###59.4[?] 13.6 dA###59.0[?] 11.7 eA###22.7###92.9[?] 7.5deA###91.9[?] 7.6 cA###90.9[?] 8.0 cA###8.4

3.3###49.3[?] 11.6cdC###70.8[?] 14.8 cA###63.4[?] 11.0eB###20.4###93.9[?] 6.2 cA###95.6[?] 7.3 bA###94.6[?] 6.3 bA###7.0

6.6###53.0[?] 13.0 cB###75.2[?] 15.3 cA###74.2[?] 14.8dA###21.3###96.3[?] 5.6bcA###94.9[?] 7.3bcA###95.3[?] 7.3 bA###7.1

33###72.5[?] 12.0 bB###86.6[?] 11.5 bA###83.6[?] 10.7cA###14.1###96.6[?] 4.8bcA###96.6[?] 5.5abA###97.6[?] 5.0abA###5.3

66###76.2[?] 9.6 bB###95.5[?] 5.1 aA###91.3[?] 11.1bA###10.2###99.0[?] 3.1abA###99.7[?] 1.8 aA###99.0[?] 3.1 aA###2.7

99###91.9[?] 8.9 aB###97.5[?] 4.1 aA###97.0[?] 4.7aA###6.5###100.0[?] 0.0aA###99.3[?] 2.5 aA###99.7[?] 1.8 aA###1.8

%CV###21.4###17.0###16.3###6.7###7.0###7.4

LD50###19.705###0.932###2.793###-###-###-

Slope###0.019###0.027###0.023###-###-###-

SE###0.002###0.003###0.002###-###-###-

1 Means in row with the same contact time followed by the same capital letters are not significantly different and means in column followed by the same common letters are not significantly different at the 5% level as determined by LSD (a=0.05)

Table II.- Effect of wild plant essential oils on the mortality of Luciaphorus perniciosus Rack by fumigation method at 12 and 24 h.

Concentration###12 h###24 h

([?] g/cm3)###M. cajuputi###L. cubeba###L. salicifolia###%CV###M. cajuputi###L. cubeba###L. salicifolia###%CV

0 (Control)###0.0[?] 0.0 fA1###0.0[?] 0.0 gA###0.0[?] 0.0 gBA###-###0.0[?] 0.0 eA###0.0[?] 0.0 fA###0.0[?] 0.0 eA###-

0.0012###22.4[?] 9.1 eB###35.4[?] 8.2 fA###26.5[?] 8.6 fB###29.2###68.3[?] 12.0 dA###76.8[?] 10.8 eA###71.1[?] 7.0 dA###13.8

0.0060###27.2[?] 7.4 eC###43.5[?] 5.2 eA###32.7[?] 7.4 efB###18.8###78.2[?] 10.3 cA###85.9[?] 7.2 dA###78.2[?] 7.0 cA###10.2

0.012###35.4[?] 7.2 dB###53.7[?] 9.2 dA###36.1[?] 5.9 eB###17.6###81.7[?] 8.8 cA###88.0[?] 6.4cdA###82.4[?] 7.2 cA###8.9

0.06###36.7[?] 7.7 dC###54.4[?] 6.4 dA###43.5[?] 10.6 dB###18.3###88.7[?] 8.8 bA###92.3[?] 5.9bcA###90.1[?] 8.8 bA###8.8

0.12###46.3[?] 8.8 cB###63.9[?] 7.4 cA###51.7[?] 8.8 cB###15.3###89.4[?] 7.bA###95.8[?] 5.1abA###93.0[?] 7.2abA###7.2

0.6###59.2[?] 6.5bC###79.6[?] 13.1 bA###67.3[?] 10.8 bB###15.1###93.7[?] 6.3abA###99.3[?] 2.6 aA###97.2[?] 4.6 aA###4.9

1.2###80.3[?] 7.0aB###91.2[?] 8.3 aA###78.2[?] 11.9 aB###11.1###98.6[?] 3.5 aA###100.0[?] 0.0 aA###97.2[?] 4.6 aA###3.4

%CV###18.4###15.0###20.4###10.6###7.4###8.3

LD50###0.476###0.166###0.410###-###-###-

Slope###1.331###1.565###1.243###-###-###-

SE###0.124###0.150###0.123###-###-###-

(2008) studied the acaricidal activities of eight plants leaf extracts against L. perniciosus by a filter paper contact toxicity bioassay and demonstrated that methanolic extract of L. cubeba caused the death of L. perniciosus with a LD50 value of 19.58 ug/cm2. We also found that the essential oil of this plant was even more effective than its leaf extract by having the LD50 value of only 0.93 ug/cm2 in the contact bioassay.

In order to promote the use of plant essential oils, a small amount of L. cubeba essential oil was added to black pepper or citronella grass oils and greatly improved their effectiveness, even though these two oils had their own contact toxicity against L. perniciosus. The results clearly demonstrated that formulations of either black pepper or citronella grass oils at the rate of 3.3 ug/cm2 with 0.01% L. cubeba oil could enhance the mite mortality rate up

Table III.- Effect of various essential oil formulations on the mortality of Luciaphorus perniciosus Rack by contact toxicity bioassay at 12 h.

Concentration main###P. nigrum +###C. nardus +

component ([?] g/cm2)###P. nigrum###C. nardus###L. cubeba (0.01%)###L. cubeba (0.01%)###%CV###

0(Control)###0.0[?] 0.0 dA1###0.0[?] 0.0 dA###0.0[?] 0.0 dA###0.0[?] 0.0 cA-

3.3###62.2[?] 15.3 cC###59.5[?] 10.0 cC###72.3[?] 12.8 cB###85.8[?] 9.1 bA###17.1

6.6###77.7[?] 19.3 bB###83.8[?] 14.0 bAB###90.5[?] 8.0 bA###89.9[?] 7.6 bA###15.4

33###90.5[?] 7.0 aAB###85.1[?] 11.3 bB###91.2[?] 7.4 bAB###95.9[?] 5.1 aA###8.8

66###95.3[?] 5.2 aAB###92.6[?] 5.9 aB###98.0[?] 4.1 aA###97.3[?] 4.6 aA###5.2

99###95.9[?] 5.1 aA###94.6[?] 5.2 aA###98.6[?] 3.5 aA###98.0[?] 4.1 aA###4.7

%CV###15.5###13.1###9.8###7.7

to 16% and 45%. The results of this study have indicated that these three plant essential oils and the essential oil formulations showed potential to be used as a botanical acaricide against the mushroom mite, L. perniciosus. However, studies on application under rearing conditions are still needed.

ACKNOWLEDGEMENTS

This work was supported by Thailand Research Fund under Grant # RTA 4880006. We would like to thank Dr. Tewin Kulpiyawat of Department of Agriculture, Ministry of Agriculture. and Co-operatives for providing mite colonies throughout this study.

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* Corresponding author: agramc@ku.ac.th 0030-9923/2010/0003-0247 $ 8.00/0 Copyright 2010 Zoological Society of Pakistan.

Means in row followed by the same capital letters are not significantly different and means in column followed by the same common letters are not significantly different at the 5% level as determined by LSD (a=0.05)

Means in row with the same contact time followed by the same capital letters are not significantly different and means in column followed by the same common letters are not significantly different at the 5% level as determined by LSD (a=0.05)

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