Open access journal: http://periodicos.uefs.br/ojs/index.php/sociobiology ISSN: 0361-6525 Sociobiology 60(1):35-40 (2013) Fumigant Activity of Eight Plant Essential Oils Against Workers of Red Imported Fire Ant, Solenopsis invicta L Tang, YY Sun, QP Zhang, Y Zhou, N Zhang, ZX Zhang Introduction The red imported fire ant, Solenopsis invcita Bu- ren, which causes severe damage to humans, animals, and the environment, is an important medical and agricultural pest in southern United States, as well as Australia, the Phil- ippines, Taiwan, and Mainland China (Zhang et al., 2007). The ant stings humans, pets, farm animals, and wildlife, as well as damaging farm, electrical equipments and irrigation systems. Moreover, besides destroying crops and fruits di- rectly or indirectly, they negatively affect the local biodiver- sity and cause nearly $5 billion losses in urban and agricul- tural areas yearly in the USA (Cheng et al., 2008). Common methods for managing the red imported fire ant are through insecticides or baits that are also a threat to human health and the environment because of their high toxicity of chemicals (Vogt et al., 2002). Reducing the use of Abstract Plant essential oils from eight plant species were tested for their insecticidal activities against the red imported fire ant, Solenopsis invcita, by using a fumigation bioassay. This study reveals that the mortalities after treatment of the workers of red imported fire ants varied according to the classification of workers, oil type, dosage, and exposure time. Among the essential oils tested, strong insecticidal activity was observed with the essential oils of camphor (Cinnamomum camphora (L.) J. Presl), artemisia annua (Artemisia annua L.), eucalyptus (Eucalyptus globulus Labill.), mugwort (Artemisia argyi H. Lév. & Vaniot), and wintergreen (Ilex chinensis Sims). Ant mortalities from chrysan- themum oil (Dendranthema indicum (L.) Des Moul.), turpentine oil (Pinus massoniana Lamb.), and forsythia oil (Forsythia suspense (Thunb.) Vahl) treatments were significant- ly lower than those from the previously mentioned five essential oil treatments. This study showed that camphor, artemisia annua, eucalyptus, mugwort, and wintergreen oils may have potential to be used as substitutes for chemical insecticides. Sociobiology An international journal on social insects South China Agricultural University, Wushan, Guangzhou, People’s Republic of China. RESEARCH ARTICLE - ANTS Article History Edited by: Gilberto M. M. Santos, UEFS, Brazil Received 06 December 2012 Initial acceptance 16 February 2013 Final acceptance 05 March 2013 Keywords Invasive ant, Solenopsis invicta, Control, Plant essential oil, Fumigation toxicity Corresponding author Zhi-Xiang Zhang Key Laboratory of Natural Pesticide and Chemical Biology, Ministry of Edu- cation, South China Agricultural Uni- versity, Wushan, Guangzhou 510642 People’s Republic of China E-Mail: zdsys@scau.educn synthetic contact insecticides has gained increasing interest in the research and development of alternative control tac- tics, such as fire ant fumigants (Zhou et al., 2012). Fumigation has a major function in insect pest elimi- nation in stored products and in quarantine containers. Stud- ies on the toxicity of botanical essential oils on red imported fire ant have shown that various essential oils are repellent and/or toxic to the ant. Citrus peels showed contact toxic- ity against red imported fire ants (Sheppard, 1984). Aro- matic cedar mulch also showed repellent activity against red imported fire ants (Thorvilson & Rudd, 2001). Vogt et al. (2002) tested mound drench formulations containing raw citrus peel extract (orange oil) on fire ants and found that cold-press citrus peel extract (‘orange oil’) can be effective- ly used as an organic alternative to conventional insecticides for drenching colonies. Mint oil granules were proven to be toxic and repel- L Tang, YY Sun, QP Zhang, Y Zhou, N Zhang, ZX Zhang - Fumigant activity of essential oils against workers of fire ant36 lent to red imported fire ants, and all red imported fire ant mounds that were treated with mint oil granules were aban- doned (Appel et al., 2004). Citronella oil was repellent and toxic to both Argentine and red imported fire ants (Wiltz et al., 2007). The essential oil from Cinnamomum osmophloe- um Kaneh. leaves was reported to be toxic to red imported fire ants in open and closed exposure trials (Cheng et al., 2008). Callicarpenal and intermedeol were isolated from the leaves of American beautyberry (Callicarpa americana L.) and Japanese beautyberry (Callicarpa japonica Thunb.), and had repellent effects on red imported fire ants (Chen et al., 2008). The over-the-counter essential oil products from China FYJ were investigated for repellent effects against workers of red imported fire ants, and each of its six major components also showed repellent effects at various concen- trations (Chen, 2009). Without prior exposure to air, vetiver oil showed a significant repellent effect to workers. How- ever, the repellent effect of vetiver oil to previously exposed workers reduced at low concentrations (Li et al., 2009). The repellent effects of five botanical essential oils, namely, Cymbopogon nardus (L.) Rendle, Cinnamomum cassia (L.) C. Presl, Ilex pedunculosa Miq., Salvia sclar- ea L., and Capsicum annuum L. on fire ant workers were evaluated using a Y-tube olfactometer bioassay (Wang et al., 2012). However, few researches existed on fumigant inves- tigations related to plant essential oils against the red im- ported fire ant. Zhou et al. (2012) tested the fumigant activity of methyl bromide and found that all red imported fire ants treated with methyl bromide above 22.52 g/m2 for 8 h died. Plant essential oils of garlic (Allium sativum L.), glove bud (Eugenia caryophyllata Thunb.), ajowan (Trachyspermum ammi (L.) Sprague), allspice (Pimenta dioica (L.) Merrill), caraway (Carum carvi L.), dill (Anethum graveolens L.), geranium (Pelargonium graveolens L’ Hér.), litsea (Litsea cubeba (Lour.) Pers.) showed strong insecticidal activity af- ter testing 59 oils on the Japanese termite, Reticulitermes speratus Kolbe, by using a fumigation bioassay (Park & Shin, 2005; Seo et al., 2009). Formic acid has been tested in the laboratory for contact and fumigation toxicity against workers, alates, and queens of red imported fire ants (Chen, 2012). Because of being highly volatile, constituting a rich source of bioactive chemicals (Chang et al., 2001 ), being safe as they are commonly used as fragrances and flavor- ing agents for foods and beverages (Isman, 2000), plant es- sential oils were used as potential alternatives for chemical insecticides. We evaluated the fumigant activity of eight plant es- sential oils on red imported fire ant workers with a fumiga- tion bioassay to determine the essential oils with efficient fumigant activity to red fire ant. Materials and Methods Plant essential oils Plant essential oils of camphor (Cinnamomum cam- phora), wintergreen (Ilex chinensis), eucalyptus (Eucalyptus globulus), artemisia annua (Artemisia annua), mugwort (Ar- temisia argyi), chrysanthemum (Dendranthema indicum), forsythia (Forsythia suspense), and turpentine (Pinus mas- soniana) were purchased from Kangshen Natural Medicinal Oil Refinery (Jiangxi, China), on January 12, 2012. Insects S. invicta colonies were collected from the suburb of Guangzhou and maintained in the laboratory for bioas- says. The collected ants were fed with a mixture of 10% honey and live insects (Tenebrio molitor L.). A test tube (25 mm×200 mm), which was partially filled with water and plugged with cotton, was used as a water source. The ants were maintained in the laboratory at 25±2 C. Fumigation toxicity bioassay The method of Seo et al. (2009) was used with slight modifications to determine the effectiveness of controlling the red imported fire ant. A 1.5 mL centrifuge tube treated with the essential oil being tested was placed at the bottom lid of a glass cylinder (5 cm diameter×10 cm) with eight pin holes on the tube to allow the oil to vaporize into the bottle. The lid was then sealed. The vertical wall inside each glass cylinder was coated with a Fluon emulsion and allowed to dry for 24 h to prevent the ants from escaping. We classi- fied the fire ant workers as major workers (4.3 mm to 4.5 mm body-length, 1.0 mm to 1.1 mm head-width) and minor workers (2.8 mm to 3.0 mm body-length, 0.6 mm to 0.7 mm head-width). Fifteen fire ant workers were placed at the bot- tom lid of the glass cylinder. The insects were maintained at 25±1°C and at a relative humidity of 80%. Experiment 1 (Cumulative mortalities were determined 12 and 24 h af- ter testing at the concentration of 0.5, 1, 2, 3, and 5 mg/ centrifuge tube). Experiment 2 (The cumulative mortalities were then determined 5, 8, 11, 13, and 24 h after testing with camphor, wintergreen, eucalyptus, artemisia annua, and mugwort oils at a concentration of 2 mg/centrifuge tube). All treatments were replicated three times. We used the fol- lowing equations: Statistical analysis For effect of oil type, dosage and exposure time on mortalities of the minor and major workers, data were trans- Sociobiology 60(1): 35-40 (2013) 37 formed to arcsine square root values for three-way analy- sis of variance (ANOVA) at P = 0.05 for the significance of main effects and various interactions. Means were compared and separated by using the Duncan-test. Results When eight plant essential oils were bioassayed, the mortalities of minor and major workers varied significantly according to oil type, dosage, and exposure time (ANOVA, P < 0.05). In addition, all of the interactions among the three factors were found to be significant (Tables 1, 3). The re- sults on mortality were shown in Table 2 and Table 4. Sig- nificant differences were found among workers: developing from different oil types, exposed to different time and dif- ferent dosage treatments (df = 28, F =7.623, F = 9.074, P = 0.0001). A 100% mortality was achieved in five out of eight essential oils, namely, camphor, artemisia annua, eucalyptus, mugwort, and turpentine oils, 12 h after treatment at 5 mg/ centrifuge tube to minor workers. Wintergreen, chrysanthe- mum, and forsythia oil showed 100% fumigant activity 24 h after treatment. Moreover, camphor, artemisia annua, eu- calyptus, mugwort, and turpentine oils achieved 100% mor- tality 12 h after treatment at 5 mg/centrifuge tube to major workers. At a concentration of 5 mg/centrifuge tube, winter- green, chrysanthemum, and forsythia oils showed 100% fu- migant activity 24 h after treatment on major workers. Plant essential oils with >80% mortality at 5 mg/filter paper were observed at lower concentrations. Camphor, artemisia annua, and eucalyptus oils caused 100% mortality of minor work- ers at a concentration of 2 mg/centrifuge tube. In addition, wintergreen, mugwort, turpentine, and forsythia oils caused >80% mortality on minor workers at a concentration of 2 mg/centrifuge tube. For major workers, only camphor and eucalyptus oils caused >80% mortality at a concentration of 2 mg/centrifuge tube. After 24 h exposure to essential oils of camphor, artemisia annua, eucalyptus, and wintergreen at 1 mg/centrifuge tube, the insect mortalities were 100%, 100%, 80.00 ±6.67%, and 86.67 ±3.85% for minor workers and 60.00 ±6.67%, 60.00 ±6.67%, 53.33 ±6.67%, and 53.33 Main effects Interactions O D T O×D O×T D×T O×D×T df 7 4 1 28 7 4 28 F 224.339 734.465 628.156 14.829 42.245 13.402 7.623 P 0.0001 0.0001 0.0001 0.0001 0.0001 0.0001 0.0001 0: oil type, D: dosage, T: exposure time (P=0.05; df=239). Table 1. Analysis of variance (three-way ANOVA) for main effects (oil type, dosage and exposure time) on mortality of minor workers, and interactions. Table 2. Mortality of minor workers of red imported fire ants caused by essential oils at different concentrations (mg/centr. tube) in the fumigation bioassay for 12. h and 24 h. * Means sharing the same letters are not significantly different from each other (P>0.05, Duncan test). essential oil mg/centrifuge tube Mortality (%,mean±SEM,N=3)* 12h 24h camphor 5 100.00 a 100.00 a 3 100.00 a 100.00 a 2 100.00 a 100.00 a 1 100.00 a 100.00 a 0.5 51.11±5.88 efghi 86.67±7.70 bc artemisia annua 5 100.00 a 100.00 a 3 100.00 a 100.00 a 2 100.00 a 100.00 a 1 80.00±10.18 cd 100.00 a 0.5 42.22±2.22 ghijkl 55.56±2.22 efgh eucalyptus 5 100.00 a 100.00 a 3 100.00 a 100.00 a 2 100.00 a 100.00 a 1 62.22±5.88 ef 80.00±6.67 cd 0.5 35.56±2.22 ijklm 48.89±2.22 efghijk wintergreen 5 66.67±7.70 de 100.00 a 3 53.33±6.67 efghi 100.00 a 2 33.33±3.85 jklm 100.00 a 1 15.56±4.44 nop 86.67±3.85 c 0.5 0.00 r 26.67±6.67 lmn mugwort 5 100 a 100.00 a 3 84.44±2.22 c 100.00 a 2 66.67±3.85d e 86.67±10.18 bc 1 31.11±2.22 klm 53.33±3.85 efghi 0.5 13.33±3.85 nopq 24.44±2.22 mno chrysanthemum 5 53.33±6.67 efghi 100.00 a 3 33.33±6.67 klm 93.33±6.67 ab 2 26.67±3.85 lmn 66.67±3.85 de 1 6.67±3.85 q 26.67±7.70 lmn 0.5 0.00 r 13.33±3.85 nopq turpentine 5 100 a 100.00 a 3 53.33±7.70 efghi 100.00 a 2 40.00±3.85 hijklm 80.00±7.70 cd 1 6.67±0.00 pq 40.00±3.85 hijklm 0.5 0.00 r 6.67±3.85 q forsythia 5 66.67±6.67 de 100.00 a 3 46.67±7.70 fghijk 100.00 a 2 33.33±3.85 jklm 86.67±3.85 c 1 13.33±6.67 opq 60.00±7.70 efg 0.5 0.00 r 0.00 r ck 0 0.00 o 0.0 o L Tang, YY Sun, QP Zhang, Y Zhou, N Zhang, ZX Zhang - Fumigant activity of essential oils against workers of fire ant38 Main effects Interactions O D T O×D O×T D×T O×D×T df 7 4 1 28 7 4 28 F 298.284 826.704 289.027 29.917 37.522 6.672 9.074 P 0.0001 0.0001 0.0001 0.0001 0.0001 0.0001 0.0001 0: oil type, D: dosage, T: exposure time (P=0.05; df=239). Table 3. Analysis of variance (three-way ANOVA) for main effects (oi l type, dosage and exposure time) on mortality of major workers, and interactions. ±6.67% for major workers, respectively. However, these values decreased to 86.67 ±7.70%, 55.56 ±2.22%, 48.89 ±2.22%, and 26.67 ±6.67% for minor workers and 13.33 ±3.85%, 33.33 ±3.85%, 40.00 ±6.67%, and 20.00 ±6.67% for major workers, respectively, when the dosage decreased to 0.5 mg/centrifuge tube. The toxicities of camphor, artemisia annua, eucalyp- tus, wintergreen, and mugwort oils after treatment on minor and major workers at a concentration of 2 mg/centrifuge tube were able to control the red imported fire ants (Figs. 1 and 2). Fig. 1 showed that camphor, artemisia annua, and eucalyptus oils completely killed the minor workers after 11 h, whereas wintergreen and mugwort oils showed 26.67 ± 3.85% and 46.67 ± 6.67% mortality, respectively. However, when the exposure time increased to 24 h, the wintergreen oil caused 100% mortality to the fire ants. Fig. 2 showed that the mortalities of major workers of red imported fire ant caused by camphor, eucalyptus, mugwort, wintergreen, and artemisia annua oils after 11 h were 73.33 ± 10.18%, 73.33 ± 6.67%, 40.00 ± 6.67%, 20 ± 3.85%, and 20 ± 6.67%, respectively, at a concentration of 2 mg/centrifuge tube. By contrast, at an exposure time of 24 h, the mortalities from the above five essential oils were 100%, 80 ± 7.70%, 46.67 ± 7.70%, 53.33 ± 6.67%, and 60 ± 6.67%, respectively. Discussion This study showed that the mortalities of the workers of red imported fire ant after treatment varied according to the classification of workers, oil type, dosage, and exposure time. Minor workers had a significantly higher mortality than major workers. The essential oils of camphor, artemisia annua, eucalyptus, mugwort, and wintergreen had the strong toxicity against red imported fire ants at a low concentra- tion (P < 0.05). In addition, camphor, artemisia annua, and eucalyptus oils had a higher activity than wintergreen and mugwort oils (P < 0.05). However, the active ingredient of the oils necessitates further studies. Essential oils, widely used as fragrances and flavors in the perfume and food industries, have long been reputed to repel, contact, fumigate insects, and control some impor- tant plant pathogens (Koul et al., 2008). But the fumigant Table 4. Mortality of major workers of red imported fire ants caused by essential oils at different concentrations (mg/centr. tube) in the fumigation bioassay for 12 h and 24 h. essential oil mg/centrifuge tube Mortality (%,mean±SEM,N=3)* 12h 24h camphor 5 100.00 a 100.00 a 3 100.00 a 100.00 a 2 73.33±7.70 cd 100.00 a 1 53.33±7.70 efg 60.00±6.67 def 0.5 6.67±3.85 n 13.33±3.85 lmn artemisia annua 5 100.00 a 100.00 a 3 93.33±7.70 b 100.00 a 2 53.33±6.67 efg 73.33±6.67 cd 1 40.00±3.85 ghi 60.00±6.67 def 0.5 13.33±3.85 lmn 33.33±3.85 hijk eucalyp- tus 5 100.00 a 100.00 a 3 100.00 a 100.00 a 2 73.33±6.67 cd 84.44±4.44 c 1 40.00±6.67 ghi 53.33±6.67 efg 0.5 13.33±3.85 lmn 40.00±6.67 ghi winter- green 5 26.67±7.70 ijkl 100.00 a 3 20.00±3.85 jklm 100.00 a 2 13.33±3.85 lmn 66.67±6.67 de 1 6.67±3.85 n 53.33±6.67 efg 0.5 0.00 o 20.00±6.67 jklm mugwort 5 100.00 a 100.00 a 3 66.67±10.18 de 100.00 a 2 40.00±6.67 ghi 46.67±7.70 fgh 1 26.67±7.70 ijkl 35.56±2.22 ghij 0.5 6.67±3085 n 13.33±3.85 lmn chrysan- themum 5 53.33±6.67efg 100.00 a 3 33.33±3.85 hijk 40.00±6.67 ghi 2 13.33±3.85 lmn 20.00±6.67 klm 1 6.67±3.85 n 11.11±2.22 mn 0.5 0.00 o 0.00 o turpen- tine 5 100.00 a 100.00 a 3 0.00 o 6.67±3.85 n 2 0.00 o 0.00 o 1 0.00 o 0.00 o 0.5 0.00 o 0.00 o forsythia 5 26.67±3.85 ijkl 100.00 a 3 6.67±3.85 n 13.33±3.85 lmn 2 0.00 o 0.00 o 1 0.00 o 0.00 o 0.5 0.00 o 0.00 o ck 0 0.00 o 0.0 o * Means sharing the same letters are not significantly different from each other (P > 0.05, Duncan test). Sociobiology 60(1): 35-40 (2013) 39 Figure 2. Mortality of major workers of red imported fire ants treat- ed with essential oils at 2 mg/centrifuge tube . activities of essential oils against red imported fire ant were rarely reported. Zhou et al., (2011) tested the fumigant ac- tivity of methyl bromide and found that all red imported fire ant that were treated with methyl bromide above 22.52 g/m2 for 8 h died. Plant essential oils from 29 plant species and components from garlic and glove bud oils, and plant essen- tial oils from 30 plant species and components from ajowan, allspice, caraway, dill, geranium, and litsea oils were tested for their insecticidal activities against the Japanese termite, R. speratus Kolbe, by using a fumigation bioassay (Park & Shin 2005; Seo et al., 2009). Formic acid has been tested in the laboratory for contact and fumigation toxicity against workers, alates, and queens of red S. invicta (Chen, 2012). The essential oils of camphor, artemisia annua, eu- calyptus, mugwort, turpentine wintergreen, chrysanthemum, and forsythia showed effective toxicity against both minor and major workers of red imported fire ants. More specifi- Figure 1. Mortality of minor workers of red imported fire ants treat- ed with essential oils at 2 mg/centrifuge tube. cally, camphor, artemisia annua, eucalyptus, mugwort, and wintergreen oils showed the strongest toxicity against red imported fire ants (P < 0.05). As a conclusion, this study showed that camphor, ar- temisia annua, eucalyptus, mugwort, and wintergreen oils may have potential as natural fumigants, and can be used as substitutes for chemical insecticides. Moreover, the de- velopment of formulations with improved efficacy, stability and reduced costs necessitates further studies. Acknowledgments This study was supported by the Science and Tech- nology Planning Project of Guangdong Province, China (No.2012B020309004). References Appel, A. G., M. J. 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