Agricultural crops are the most important food source for millions of people worldwide. However, in most cases, grains are not used immediately after harvesting, but instead are stored for the next season or exported to other countries. The loss of grain yield during storage can be attributed to many factors, and among those, insect pests are the most important cause of loss because they reduce the quality of the stored grain (Jayakumar et al. 2017).
Unchecked growth of human population has led to numerous and very serious problems, including food shortage. Globally, Tribolium castaneum (Herbst) (Coleoptera: Tenebrionidae) and Oryzaephilus surinamensis (L.) (Coleoptera: Silvanidae) are the 2 most important stored–grain pests, damaging 10 to 40% of all stored agricultural crops (Al Qahtani et al. 2012). These beetles feed on grains, dried fruits, flour, sugar, candies, tobacco, and many other plant products intended for human consumption, as well as dried meat (Bilal et al. 2015).
Currently, the intensive use of chemicals for the control of storedproducts pests has resulted in serious problems, including pest resistance to insecticides, environmental contamination, the presence of unacceptable pesticide residues in foods, and lethal effects on nontarget organisms (White & Leesch 1995; Jovanovic et al. 2007; Lu et al. 2011). Botanical insecticides have long been used as alternatives to synthetic insecticides for insect pest management because botanicals pose little threat to the environment or to human health (Isman 2006; Ahmad et al. 2013). Many previous studies have demonstrated the effectiveness of plant oils to control stored–products insects. Magd El–Din (2001) evaluated the efficacy of 3 essential oils to control 3 storedproduct insects, among which caraway seed oil demonstrated high toxicity to both insect eggs and adults. Plant oils comprise complex mixtures of monoterpenes, sesquiterpenes, and aromatic compounds (Nattudri et al. 2017), and may act as contact insecticides, antifeedants, repellents, or fumigants (Jayakumar et al. 2017).
Essential oils are interesting natural plant products thatpossess various biological activities, among other qualities. These materials rapidly degrade under ambient air temperature and moisture, and are readily broken down by detoxification enzymes. These features are important for their use as biopesticides, because a rapid breakdown means less persistence in the environment (i.e., lower residual effects), and reduced risks to non–target organisms. Although natural enemies are sensitive to direct contact with such materials, predators and parasitoids that attack the product 1 to 2 d after treatment application are not affected by the toxins (Isman 2006).
In this study, we evaluated the effectiveness of 5 types of plant oils on T. castaneum and O. surinamensis. These plant oils were selected based on prior knowledge regarding their effective toxicity to control similar pests (Magd–El–Din 2001; Al–Jabr 2006; Lopez et al. 2008; Germinara et al. 2017). These oils also are relatively inexpensive and readily available in most countries.
Materials and Methods
Pure plant oils were obtained from Diar Almadina Company in Jeddah, Saudi Arabia (Table 1). We evaluated 4 concentrations of these oils (1, 2, 3, and 4 µL per mL) diluted in acetone, that was used as a solvent because of its rapid evaporation.
INSECT REARING TECHNIQUE
Tribolium castaneum and O. surinamensis were collected from infested products obtained from a local market in Albaha City, Saudi Arabia, and reared under laboratory conditions at 27 °C, 70 ± 5% relative humidity, and 12:12 h (L:D) photoperiod. Yeast and flour (5:100 g) were used as food for the insects that were maintained in jars covered with muslin cloth fastened with rubber bands. One– to 3–wk–old adults were collected and used for bioassays (Madkour et al. 2013).
CONTACT TOXICITY BIOASSAY
As a bioassay, we used the thin film technique described by Iwuala et al. (1981). One mL of each concentration of the plant oils was evenly spread over the bottom of a Petri dish. Petri dishes used for control treatments were treated with 1 mL of acetone. Mature adults were exposed to a thin film of plant oils for 24 h, when mortality was recorded following adjustment with Abbott's (1925) formula. Four replicates of 10 adults were used for each concentration treatment.
Plant oils used in bioassays and source of essential oil.
The data were analyzed using 1–way analysis of variance (ANOVA), followed by Tukey's honest significant difference (HSD) test. Differences were considered significant at P < 0.05. The LC50 values (oil concentration high enough to kill 50% of the insects) were calculated using Probit analysis (Finney 1964).
The insecticidal activity of lavender, onion, flaxseed, caraway, and saad oils tested on T. castaneum are listed in Table 2 and depicted in Figures 1 to 5, respectively. The data indicated that caraway oil was the most toxic of the oils evaluated, causing a mortality rate of 50% at the lowest concentration (1 µL per mL) and 95% mortality at the highest concentration (4 µL per mL), with LT50 value of 1.2 µL per mL. For insects treated with lavender oil for 24 h, mortality was 30% at a concentration of 1 µL per mL and 70% at 4 µL per mL. Onion oil was less potent than the 2 aforementioned oils, causing only 5% mortality at a concentration of 1 µL per mL and 90% mortality at 4 µL per mL. Flaxseed and saad oils showed similarly low toxic effects, with LT50 values of 4.5 and 4.24 µL per mL, respectively. Results clearly indicated that insect mortality increased with increasing oil concentration. Thus, plant oils can be ranked as follows according to their toxicity to control T. casteneum: caraway > lavender > onion > saad > flaxseed.
Insecticidal activity of the 5 plant oils examined on O. surinamensis are listed in Table 3, and those of lavender, flaxseed, caraway, and saad oils are depicted in Figures 6 to 9, respectively. Onion oil caused 100% insect mortality at all concentrations that were examined. The LT50 value was 0.6 µL per mL for lavender oil, which caused 65% mortality at a concentration of 1 µL per mL and 90% mortality at 4 µL per mL, after a 24 h exposure. Insects treated with saad oil exhibited 60% mortality at a concentration of 1 µL per mL and 90% mortality at 4 µL per mL, with an LT50 value of 0.77 µL per mL. Caraway oil caused 100% insect mortality at the highest concentration, with an LT50 value 0.81 µL per mL. Flaxseed oil caused 55% and 95% mortality in insects treated at 1 and 4 µL per mL, respectively, and produced an LT50 value of 1 µL per mL. Based on these results, plant oils were ranked in the following order according to their toxicity for O. surinamensis: onion > lavender > saad > caraway > flaxseed.
The results of this study demonstrated that the toxicity of the 5 selected plant oils varied depending on the oil concentration and target insect species. Caraway, lavender, and onion oils were most effective in controlling T. castaneum and O. surinamensis. These findings are consistent with the results of previous studies that have investigated the toxic effects of plant oils on these 2 insects (Al–Jabr 2006; Mondal & Khalequzzaman 2006; Ahmed et al. 2009; Lu et al. 2011; Hamed et al. 2012; Madkour et al. 2013; Iieke & Ogungbite 2014; Aref & Farashiani 2015; Khanzada et al. 2015). These studies indicated that edible plant oils affect the developmental stages of T. castaneum, resulting in low adult emergence and pest fecundity in grain treated with plant oils.
Mortality of Tribolium castaneum adults exposed to different concentrations of plant oils.
Talukder et al. (1998) demonstrated that the toxic effects of plant oils are due to the presence of oleic, linoleic, and palmitic acids, and alkalis that may block insect tracheae, thereby inhibiting respiration during contact or fumigation tests. Yoon et al. (2011) showed a repellent effect of lavender oil for the spotted lantern fly, Lycorma delicatula (White) (Hemiptera: Fulgoridae) (also referred to as “spot clothing wax cicada” or “Chinese blistering cicada” in the literature) and established that linalool (a monoterpene) was the most effective constituent present in this oil. Similarly, Lucic et al. (2015) demonstrated the toxic effects of the lavender plant parts and essential oil on 3 stored–wheat pests, including T. castaneum. Other studies have concluded that plant essential oils from the family Linaceae, including lavender oil, may cause feeding inhibition, repellence, and insecticidal action to control various insect pests (Papachristos & Stamopoulus 2004; Gonzalez– Coloma et al. 2006). Furthermore, Magd–El–Din (2001) demonstrated that caraway oil exhibited a high toxicity for Tribolium confusum Jacquelin du Val (Coleoptera: Tenebrionidae) and other pests. Fang et al. (2010) found that the essential oil of C. carvi showed a strong toxicity in controlling Sitophilus zeamais (Motschulsky) (Coleoptera: Curculionidae) and T. castaneum with (R)–carvone and D–limonene being the principal toxic constituents for these 2 insects.
Mortality of Oryzaephilus surinamensis adults exposed to different concentrations of plant oils.
Several studies have demonstrated that plant extracts can be more effective in controlling pest insects than individual active compounds, owing to natural synergism, that also may delay the development of insecticide resistance (Yoon et al. 2011; Bilal et al. 2015). In this study, O. surinamensis was found to be more susceptible to the toxic effects of the oils, whereas T. castaneum was more resistant, as previously reported by Al–Jabr (2006). Interestingly, in the present study we found that A. cepa oil was highly toxic to O. surinamensis; however, other studies that investigated the effect of A. cepa oil on insect pests did not report similar results (Tunaz et al. 2009; Denloye 2010).
In conclusion, the results of the present study indicate that onion, lavender, and caraway oils are promising alternatives for the control of T. castaneum and O. surinamensis in stored products. Synthetic insecticides cause adverse effects on the environment, including pest resistance, pollution, and toxicity to non–target organisms. Plant essential oils are less likely to elicit pest resistance and are less toxic to the environment. However, further studies are needed to evaluate the cost of these oils and their effectiveness in controlling a wider range of insect pests.
The authors would like to thank Fatimah Alzahrani for her assistance during the preparation of the manuscript.
- Abbott W. 1925. A method of computing the effectiveness of an insecticide.Journal of Economic Entomology18: 265–267. Google Scholar
- Ahmed S, Zainab A, Nisar S, Rana N. 2009. Effect of new formulations of neem products on biology of Tribolium castaneum (Herbst) (Tenebrionidae: Coleoptera).Pakistan Entomologist31: 133–137. Google Scholar
- Al–Jabr AM. 2006. Toxicity and repellency of seven plant essential oils to Oryzaephilus surinamensis (Coleoptera: Silvanidae) and Tribolium castaneum (Coleoptera: Tenebrionidae).Scientific Journal of King Faisal University7: 49–59. Google Scholar
- Al Qahtani AM, Al–Dahafar ZM, Rady M. 2012. Insecticidal and biochemical effect of some dried plants against Oryzaephilus surinamensis (Coleoptera: Silvanidae).Journal of Basic and Applied Zoology65: 88–93. Google Scholar
- Aref PS, Farashiani EM. 2015. Eucalyptus dundasii Maiden essential oil, chemical composition and insecticidal values against Rhyzopertha dominica (F.) and Oryzaephilplus surinamensis (L.).Journal of Plant Protection Research55: 35–41. Google Scholar
- Bilal H, Akram W, Hassan SA, Zia A, Bhatti AR, Mastoi I, Aslam S. 2015. Insecticidal and repellent potential of citrus essential oils against Tribolium castaneum Herbst (Coleoptera: Tenebrionidae).Pakistan Journal of Zoology47: 997–1002. Google Scholar
- Denloye A. 2010. Bioactivity of powder and extracts from garlic, Allium sativum L. (Alliaceae) and spring onion, Allium fistulosum (Alliaceae) against Callosobruchus macullatus F. (Coleoptera: Bruchidae) on cowpea, Vigna unguiculate (L.) Walp (Leguminosae) seeds.Psyche2010: 1–5. http://dx.doi.org/10.1155/2010/958348 Google Scholar
- Fang R, Jiang CH, Wang XY, Zhang HM, Liu ZL, Zhou L, Du SS, Deng ZW. 2010. Insecticidal activity of essential oil of Carum carvi fruits from China and its main components against two grain storage insects.Molecules15: 9391–9402. Google Scholar
- Finney DJ. 1964. Probit Analysis. 2nd ed.Cambridge University Press, Cambridge, United Kingdom. Google Scholar
- Germinara G, Stefano M, Acutis L, Pati S, Delfine S, Cristofaro A, Rotundo G. 2017. Bioactivities of Lavandula angustifolia essential oil against the stored grain pest Sitophilus granarius.Bulletin of Insectology70: 129–138. Google Scholar
- Gonzalez–Coloma A, Martin–Benito D, Mohamed N, Garcia–Vallejo V, Soria A. 2006. Antifeedant effects and chemical composition of essential oils from different populations of Lavandula luisieri L.Biochemical Systematics and Ecology34: 609–616. Google Scholar
- Hamed KR, Abotaleb MS, Bahria B. 2012. Efficacy of certain plant oils as grain protectants against the rice weevil, Sitophilus oryzae (Coleoptera: Curculionidae) on wheat.Egyptian Academic Journal of Biological Sciences5: 49–53. Google Scholar
- Iieke DK, Ogungbite OC. 2014. Entomocidal activity of powders and extracts of four medicinal plants against Sitophilus oryzae (L), Oryzaephilus surinamensis Mercator (Faur) and Ryzopertha dominica (Fabr).Jordan Journal of Biological Sciences7: 57–62. Google Scholar
- Isman MB. 2006. Botanical insecticides, deterrents, and repellents in modern agriculture and an increasingly regulated world.Annual Review of Entomology51: 45–66. Google Scholar
- Iwuala MOE, Ossiogu IUW, Agbackwuru EOP. 1981. Dennettia oil, a potential insecticide: tested with adults and nymphs of Periplaneta americana and Zonocerus variegatus.Journal of Economic Entomology74: 249–252. Google Scholar
- Jayakumar M, Arivoli S, Raveen R, Tennyson S. 2017. Repellent activity and fumigant toxicity of a few plant oils against the adult rice weevil Sitophilus oryzae Linnaeus 1763 (Coleoptera: Curculionidae).Journal of Entomology and Zoology Studies5: 324–335. Google Scholar
- Jovanovic Z, Kostic M, Popovic Z. 2007. Grain–protective properties of herbal extracts against the bean weevil Acanthoscelides obtectus Say.Industrial Crops and Products26: 100–104. Google Scholar
- Khan FZA, Sagheer M, Hasan M, Saeed S, Ali K, Gul HT, Bukhar SA, Manzoor SA. 2013. Toxicological and repellent potential of some plant extracts against stored product insect pest, Tribolium castaneum (Herbst.) (Coleoptera: Tenebrionidae).International Journal of Biosciences3: 280–286. Google Scholar
- Khanzada H, Sarwar M, Lohar M. 2015. Repellence activity of plant oils against red flour beetle Tribolium castaneum (Herbst) (Coleoptera: Tenebrionidae) in wheat.International Journal of Animal Biology1: 86–92. Google Scholar
- Lopez M, Jordan M, Pascual–Villalobos M. 2008. Toxic compounds in essential oils of coriander, caraway and basil active against stored rice pests.Journal of Stored Products Research44: 273–278. Google Scholar
- Lu J, Wu C, Shi Y. 2011. Toxicity of essential oil from Artemisia argyi against Oryzaephilus surinamensis (Linnaeus) (Coleoptera: Silvanidae).African Journal of Microbiology Research5: 2816–2819. Google Scholar
- Lucic P, Liska A, Rosman V, Balicevic R, Dumlic M. 2015. The potential use of lavender (Lavandula intermedia) in protection of stored wheat against storage insect, pp. 160–165 In Proceedings of the 8th International Scientific/ Professional Conference Agriculture in Nature and Environment Protection.Vukovar, Croatia, 1–3 Jun 2015 . Google Scholar
- Madkour HM, Zaitoun AA, Singer F. 2013. Repellent and toxicity of crude plant extracts on saw–toothed grain beetle (Oryzaephilus surinamensis) (L.).Journal of Food, Agriculture and Environment11: 381–384. Google Scholar
- Magd–El–Din M. 2001. Biological activity of three essential oils against some stored product insects (Coleoptera: Bostrichidae, Curclionidae, and Tenebrionidae).Journal of the Egyptian–German Society of Zoology34(E): 143–155. Google Scholar
- Mondal M, Khalequzzaman M. 2006. Toxicity of essential oils against red flour beetle, Tribolium castaneum (Herbst) (Coleoptera: Tenebrionidae).Journal of Bio–Science14: 43–48. Google Scholar
- Nattudri G, Arulvasu C, Baskar K. 2017. Indigenous knowledge in stored product pest management.Entomology, Ornithology and Herpetology6: 2. DOI: 10.4172/2161–0983.1000e127 Google Scholar
- Papachristos DP, Stamopoulos DC. 2004. Fumigant toxicity of three essential oils on the eggs of Acanthoscelides obtectus (Say) (Coleoptera: Bruchidae).Journal of Stored Products Research40: 517–525. Google Scholar
- Talukder D, Malek MA, Khanam M, Dey KC. 1998. Toxicity of some indigenous plant seed oils against Tribolium confusum Duval adults (Coleoptera: Tenebrionidae).Pakistan Journal of Zoology30: 331–334. Google Scholar
- Tunaz H, Kubilay M, Isikber AA. 2009. Fumigant toxicity of plant essential oils and selected monoterpenoid components against the adult German cockroach, Blattella germanica (L.) (Dictyoptera: Blattellidae).Turkish Journal of Agriculture and Forestry33: 211–217. Google Scholar
- White NDG, Leesch JG. 1995. Chemical control, pp. 287–330 In Subramanyam B, Hagstrum DW [eds.], Integrated Management of Insects in Stored Products.Marcel Dekker, New York, USA. Google Scholar
- Yoon C, Moon SR, Jeong J, Shin Y, Cho S, Ahn K, Yang J, Kim GH. 2011. Repellency of lavender oil and linalool against spot clothing wax cicada, Lycorma delicatula (Hemiptera: Fulgoridae) and their electrophysiological responses.Journal of Asia–Pacific Entomology14: 411–416 Google Scholar