Fumigant and contact toxicity of Ruta chalepensis l. (Rutaceae) essential oil against five coleopteran stored product pests and its effects on cholinesterases

Year 2023, , 52 - 65, 31.12.2023

Yasemin Yücel Yücel , Ömer Cem Karakoç , Hüseyin Servi , Salih Gücel , Ayşe Nalbantsoy , Kaan Polatoğlu

https://doi.org/10.16955/bitkorb.1374633

Abstract

The essential oil composition of aerial parts of Ruta chalepensis L. was analyzed with GC-MS. Seventy-nine compounds were detected representing 85.93 ± 1.08% (n = 3) of the essential oil. The major components of the essential oil were 2-undecanone 21.52 ± 0.21%, 2-nonanone 18.31 ± 0.27%, and 2-nonyl acetate 13.22%. The highest insecticidal contact toxicity of the oil was observed against Rhyzopertha dominica F. with 0.018 μl/insect LD50 and 0.039 μl/insect LD90 after 24h. Essential oil also produced considerably low 0.50 and 0.59 μl/insect LD50 values after 24h against Sitophilus oryzae L. and Sitophilus granarius L. respectively. The lowest contact toxicity was observed against Tribolium castaneum Herbst. and Tribolium confusum Jacquelin du Val. 0.138 and 0.078 μl/insect LD50 after 24h respectively. The highest fumigant toxicity was observed against S. granarius for the application concentration of 10 μl, 10% oil/acetone (v:v) in a 10 ml chamber which afforded 100.00 ± 0.00% mortality after 48h. The essential oil also produced high fumigant toxicity against S. oryzae, T. castaneum and R. dominica which were 95.47 ± 3.41%, 93.30 ± 5.54%, and 85.47 ± 3.41% mortality at 20 μl application concentration of the oil solution after 48h. The R. chalepensis essential oil produced low acetylcholinesterase enzyme 5.29 ± 1.20% (n=3) inhibition and mediocre butyrylcholinesterase enzyme inhibition 42.6 ± 0.71% (n=3). According to the insecticidal activity assays performed, the essential oil R. chalepensis seems to be a promising source that could yield natural compounds that could be employed in stored product pest management.

Keywords

Ruta chalepensis, essential oil composition, stored product pests, acetylcholinesterase, butyrylcholinesterase, enzyme inhibition

Ethical Statement

The authors declare that the ethics committee approval is not required for this study.

Supporting Institution

The results presented in this poster were obtained using the infrastructure provided by the Republic of Turkey Ministry of Food, Agriculture and Livestock, General Directorate of Agricultural Research and Policies

Project Number

Project No: TAGEM/16 ARGE/07

Ruta chalepensis L. (Rutaceae) uçucu yağının beş coleopteran depo ürün zararlısına karşı fumigant ve kontak toksisitesi ile kolinesterazlar üzerine etkileri

Abstract

Ruta chalepensis L.'nin toprak üstü aksamından elde edilen uçucu yağ kompozisyonu GC-MS ile analiz edildi. Uçucu yağın %85.93 ± 1.08 (n = 3)’i temsil eden yetmiş dokuz bileşik tespit edildi. Uçucu yağın ana bileşenleri olarak %21.52 ± 0.21 oranında 2-undekanon, %18.31 ± 0.27 oranında 2-nonanon ve %13.22 oranında da 2-nonil asetat belirlendi. Uçucu yağı en yüksek insektisidal kontak toksisitesi 24 saat sonra 0.018 μl/böcek LD50 ve 0.039 μl/böcek LD90 değerleri ile Rhyzopertha dominica F. üzerinde gözlemlenmiştir. Uçucu yağ, ayrıca Sitophilus oryzae L. ve Sitophillus granarius L. karşısında 24 saat sonra sırasıyla 0.50 ve 0.59 μl/ böcek değerleriyle oldukça düşük denebilecek LD50 değerlerini gösterdi. En düşük kontak toksisite 24 saat sonra Tribolium castaneum Herbst. ve Triboliom confusum Jacquelin du Val.’e karşı sırasıyla 0.138 ve 0.078 μl/böcek LD50 değerleri şeklinde gözlemlendi. S. granarius'a karşı en yüksek fumigant toksisite 48 saat sonra %100 ölüm oranını sağlayan ve 10 ml‘lik haznede uygulanan 10 μl, %10 yağ/aseton (v:v) konsantrasyonunda görüldü. Uçucu yağ ayrıca S. oryzae, T. castaneum ve R. dominica'ya karşı yüksek fumigant toksisiteyi de ortaya çıkardı. 48 saat sonra 20 μl yağ çözeltisi uygulama konsantrasyonunda ölüm oranı sırasıyla %95.47 ± 3.41, %93.30 ± 5.54 ve %85.47 ± 3.41 idi. R. chalepensis uçucu yağı ile %5.29 ± 1.20’lik düşük bir asetilkolinesteraz enzim inhibisyonu ile %42.6 ± 0.71’lik orta derecede bir bütirilkolinesteraz enzim inhibisyonu elde edildi. Yapılan insektisidal aktivite denemelerine göre, R. chalepensis uçucu yağının, depo ürün zararlılarına karşı mücadelede kullanılabilecek doğal bileşiklerin elde edilmesi adına umut verici bir kaynak olduğu düşünülmektedir.

Keywords

Ruta chalepensis, uçucu yağ analizi, depo ürün zararlıları, asetlkolinesteraz, bütirilkolinesteraz, enzim inhibisyonu

Project Number

Project No: TAGEM/16 ARGE/07

References

• Abbad A., Kasrati A., Jamali C.A., Zeroual S., Ba M'hamed T., Spooner-Hart R., Leach D., 2014. Insecticidal properties and chemical composition of essential oils of some aromatic herbs from Morocco. Natural Product Research, 28 (24), 2338-2341.
• Abdellaoui K., Bahloul N., Milad M., Marzouk I.B., Chaiier N., Halima-Kamel M.B., 2014. The bioactivity of Ruta chalepensis and Peganum harmala extracts on the migratory locust Locusta migratoria (Orthoptera: Acrididae). Journal of Natural Product and Plant Resources, 4 (2), 62-68.
• Adsersen A., Gauguin B., Gudiksen L., Jäger A.K., 2006. Screening of plants used in Danish folk medicine to treat memory dysfunction for acetylcholinesterase inhibitory activity. Journal of Ethnopharmacology 104 (3), 418-422.
• Akkari H., Ezzine O., Dhahri S., B’chir F., Rekik M., Hajaji S., Darghouth M.A., Jamâa M.L.B., Gharbi M., 2015. Chemical composition, insecticidal and in vitro anthelmintic activities of Ruta chalepensis (Rutaceae) essential oil. Industrial Crops and Products, 74, 745-751.
• Ali A., Demirci B., Kiyan H.T., Bernier U.R., Tsikolia M., Wedge D.E., Khan I.A., Başer H.C.B., Tabanca N., 2013. Biting deterrence, repellency, and larvicidal activity of Ruta chalepensis (Sapindales: Rutaceae) essential oil and its major individual constituents against mosquitoes. Journal of Medical Entomology, 50 (6), 1267-1274.
• Alkan M., Atay T., 2023. Insecticidal effects of Thymus citriodorus L. (Lamiaceae) essential oil on two important stored product pests. 3nd International Congress of the Turkish Journal of Agriculture-Food Science and Technology, Turjaf 2023, 13-16 September 2023, p 401.
• Alkan M., Kaplan Evlice A., Evlice E., 2023. Chemical composition and potential insecticidal activity of essential oil of Anthemis tinctoria (Asteraceae) and Anthemis austiaca (Asteraceae). Sivas II. International Conference on Scientific and Innovation Research, 15-17 September-Sivas,Türkiye, 1327-1336.
• Atay T., Alkan M., 2023. Biological activity of the Schinus molle L. (Anacardiaceae) essential oil on granary weevil, Sitophilus granarius (Linnaeus) (Coleoptera: Dryophthoridae). 3nd International Congress of the Turkish Journal of Agriculture-Food Science and Technology, Turjaf 2023, 13-16 September 2023, p. 402.
• Atay T., Alkan M., Ertürk S., Toprak U., 2023. Individual and combined effects of α-Pinene and a native diatomaceous earth product on control of stored product beetle pests. Journal of Asia-Pacific Entomology, 26 (4), 102149.
• Alshehry A.Z., Zaitoun A.A., Abo-Hassan R.A., 2014. Insecticidal activities of some plant extracts against subterranean termites, Psammotermes hybostoma (Desneux) (Isoptera: Rhinotermitidae). International Journal of Agricultural Sciences, 4 (9), 257-260.
• Al-mazra’awi S.M., Ateyyat M., 2009. Insecticidal and repellent activities of medicinal plant extracts against the sweet potato whitefly, Bemisia tabaci (Hom.: Aleyrodidae) and its parasitoid Eretmocerus mundus (Hym.: Aphelinidae). Journal of Pest Science, 82 (2), 149-154.
• Başer K.H.C., Özek T., Demirci B., Duman H., 2000a. Composition of the essential oil of Glaucosciadium cordifolium (Boiss.) Burtt et Davis from Turkey. Flavour and Fragrance Journal, 15 (1), 45-46.
• Başer K.H.C., Özek T., Demirci B., Duman H., 2000b. Composition of the essential oil of Prangos heyniae H. Duman et MF Watson, a new endemic from Turkey. Flavour and Fragrance Journal, 15 (1), 47-49.
• Başer K.C., Özek T., Demirci B., Kürkçüoǧlu M., Aytac Z., Duman H., 2000c. Composition of the essential oils of Zosima absinthifolia (Vent.) Link and Ferula elaeochytris Korovin from Turkey. Flavour and Fragrance Journal, 15 (6), 371-372.
• Başer K. H. C., Demirci B., Tabanca N., Özek T., Gören N., 2001. Composition of the essential oils of Tanacetum armenum (DC.) Schultz Bip., T. balsamita L., T. chiliophyllum (Fisch. & Mey.) Schultz Bip. var. chiliophyllum and T. haradjani (Rech. fil.) Grierson and the enantiomeric distribution of camphor and carvone. Flavour and Fragrance Journal, 16 (3), 195-200.
• Başer K.H.C., Demirci B., Özek T., Akalin E., Özhatay N., 2002a. Micro-distilled volatile compounds from Ferulago species growing in western Turkey. Pharmaceutical Biology, 40 (6), 466-471.
• Başer K.H.C., Demirci B., Kirimer N.E., Satil F., Tümen G., 2002b. The essential oils of Thymus migricus and T. fedtschenkoi var. handelii from Turkey. Flavour And Fragrance Journal, 17 (1), 41-45.
• Başer K.H.C., Özek T., Kırımer N., Deliorman D., Ergun F., 2004. Composition of the essential oils of Galium aparine L. and Galium odoratum (L.) Scop. from Turkey. Journal of Essential Oil Research, 16 (4), 305-307.
• Başer K.H.C., Özek G., Özek T., Duran A., Duman H., 2006. Composition of the essential oils of Rhabdosciadium oligocarpum (Post ex Boiss.) Hedge et Lamond and Rhabdosciadium microcalycinum Hand.‐Mazz. Flavour and Fragrance Journal, 21 (4), 650-655.
• Bendimerad N., Taleb Bendiab S. A., Benabadji A.B., Fernandez X., Valette L., Lizzani-Cuvelier L., 2005. Composition and antibacterial activity of Pseudocytisus integrifolius (Salisb.) essential oil from Algeria. Journal of Agricultural and Food Chemistry, 53 (8), 2947-2952.
• Bouabidi W., Hanana M., Gargouri S., Amri I., Fezzani T., Ksontini M., Hamrouni L., 2015. Chemical composition, phytotoxic and antifungal properties of Ruta chalepensis L. essential oils. Natural Product Research, 29 (9), 864-868.
• Bouajaj S., Romane A., Benyamna A., Amri I., Hanana M., Hamrouni L., Romdhane M., 2014. Essential oil composition, phytotoxic and antifungal activities of Ruta chalepensis L. leaves from High Atlas Mountains (Morocco). Natural Product Research, 28 (21), 1910-1914.
• Campbell A., Sinha R.N., 1976. Damage of wheat by feeding of some stored product beetles. Journal of Economic Entomology, 69 (1), 11-13.
• Chebli B., Hmamouchi M., Achouri M., Hassani L.I., 2004. Composition and in vitro fungitoxic activity of 19 essential oils against two post-harvest pathogens. Journal of Essential Oil Research, 16 (5), 507-511.
• Chen C.C., Huang Y.L., Huang F.I., Wang C.W., Ou J.C., 2001. Water-soluble glycosides from Ruta graveolens. Journal of Natural Products, 64 (7), 990-992.
• Çam H., Karakoç Ö.C., Gökçe A., Telci İ., Demirtaş İ., 2012. Farklı nane türlerine ait klonların uçucu yağlarının buğday biti [Sitophilus granarius L. (Coleoptera: Curculionidae)]’ne fumigant etkisi. Türkiye Entomoloji Dergisi, 36 (2), 255-263.
• Conti B., Leonardi M., Pistelli L., Profeti R., Ouerghemmi I., Benelli G., 2013. Larvicidal and repellent activity of essential oils from wild and cultivated Ruta chalepensis L. (Rutaceae) against Aedes albopictus Skuse (Diptera: Culicidae), an arbovirus vector. Parasitology Research, 112 (3), 991-999.
• Das A.K., Suresh Kumar J., Swamy P.S., 2015. Larvicidal activity and leaf essential oil composition of three species of genus Atalantia from south India. International Journal of Mosquito Research, 2 (3), 25-29.
• De Feo V., De Simone F., Senatore F., 2002. Potential allelochemicals from the essential oil of Ruta graveolens. Phytochemistry, 61 (5), 573-578.
• Demirci B., Baser K.H.C., Dadandi M.Y., 2006. Composition of the essential oils of Phlomis rigida Labill. and P. samia L. Journal of Essential Oil Research, 18 (3), 328-331.
• Eisen R.J., Enscore R.E., Atiku L.A., Zielinski-Gutierrez E., Mpanga J.T., Kajik E., Andamab V., Mungujakisab C., Tibob E., MacMillana K., Borcherta J.N., Gage K.L., 2013. Evidence that rodent control strategies ought to be improved to enhance food security and reduce the risk of rodent-borne illnesses within subsistence farming villages in the plague-endemic West Nile region, Uganda. International Journal of Pest Management, 59 (4), 259-270.
• Elamrani A., Benaissa M., 2010. Chemical composition and antibacterial activity of the essential oil of Ononis natrix from Morocco. Journal of Essential Oil Bearing Plants, 13 (4), 477-488.
• Ellman G.L., Courtney K.D., Andres Jr, V., Featherstone R.M., 1961. A new and rapid colorimetric determination of acetylcholinesterase activity. Biochemical pharmacology, 7 (2), 88-95.
• Emam A.M., Swelam E.S., Megally N.Y., 2009. Furocoumarin and quinolone alkaloid with larvicidal and antifeedant activities isolated from Ruta chalepensis leaves. Journal of Natural Products, 2, 10-22.
• Evlice E., Alkan M., 2023. Contact insecticidal activity of Artemisia vulgaris (Asteraceae) essential oil against two important stored product pests. Sivas II. International Conference on Scientific and Innovation Research, 15-17 September-Sivas, Türkiye, 1312-1320.
• Gokce A., Stelinski L.L., Whalon M.E., Gut L.J., 2010. Toxicity and antifeedant activity of selected plant extracts against larval obliquebanded leafroller, Choristoneura rosaceana (Harris). The Open Entomology Journal, 4 (1), 30-36.
• Günaydin A.K., Savci B.S., 2005. Phytochemical studies on Ruta chalepensis (LAM.) Lamarck. Natural Product Research, 19 (3), 203-210.
• Haddouchi F., Chaouche T.M., Zaouali Y., Ksouri R., Attou A., Benmansour A., 2013. Chemical composition and antimicrobial activity of the essential oils from four Ruta species growing in Algeria. Food Chemistry, 141 (1), 253-258.
• Hernandez-Lambrano R., Pajaro-Castro N., Caballero-Gallardo K., Stashenko E., Olivero-Verbel J., 2015. Essential oils from plants of the genus Cymbopogon as natural insecticides to control stored product pests. Journal of Stored Products Research, 62, 81-83.
• Hmamouchi M., Lahlou M., Agoumi A., 2000. Molluscicidal activity of some Moroccan medicinal plants. Fitoterapia, 71 (3), 308-314.
• Hnatyszyn O., Arenas P., Moreno A.R., Rondina R., Coussio J.D., 1974. Plantas reguladoras de la fecundidad segun la medicina folklorica. Revista de la Sociedad Científica, 14, 37.
• Iauk L., Mangano K., Rapisarda A., Ragusa S., Maiolino L., Musumeci R., Costanzoa R., Serra A., Speciale A., 2004. Protection against murine endotoxemia by treatment with Ruta chalepensis L., a plant with anti-inflammatory properties. Journal of Ethnopharmacology, 90 (2-3), 267-272.
• Isman M.B., 2006. Botanical insecticides, deterrents, and repellents in modern agriculture and an increasingly regulated world. Annual Review of Entomology, 51, 45-66.
• Isman M.B., 2008. Perspective, botanical insecticides: for richer, for poorer. Pest Management Science: Formerly Pesticide Science, 64 (1), 8-11.
• Jeon J.H., Kim M.G., Lee H.S., 2013. Insecticidal activities of Ruta chalepensis leaves isolated constituent and structure-relationships of its analogues against Sitophilus oryzae. Journal of The Korean Society for Applied Biological Chemistry, 56 (5), 591-596.
• Jeon J.H., Lee S.G., Lee H.S., 2015. Isolation of insecticidal constituent from Ruta graveolens and structure-activity relationship studies against stored-food pests (Coleoptera). Journal of Food Protection, 78 (8), 1536-1540.
• Joichi A., Yomogida K., Awano K.I., Ueda Y., 2005. Volatile components of tea‐scented modern roses and ancient Chinese roses. Flavour and Fragrance Journal, 20 (2), 152-157.
• Joulain D., Laurent R., Fourniol J.P., Yaacob K.B., 1991. Novel moskachan related compounds in the essential oil of Ruta angustifolia Pers. from Malaysia. Journal of Essential Oil Research, 3 (5), 355-357.
• Jorge T.C., Lenartovicz V., Andrade M.W., Bonafin T., Giordani M.A., Bueno N.B., Schneider D.S.L.G., 2009. Pediculicidal activity of hydroethanolic extracts of Ruta graveolens, Melia azedarach and Sambucus australis. Latin American Journal of Pharmacy, 28 (3), 457-459.
• Kamanula J., Sileshi G.W., Belmain S.R., Sola P., Mvumi B.M., Nyirenda G.K., Stevenson P.C., 2010. Farmers' insect pest management practices and pesticidal plant use in the protection of stored maize and beans in Southern Africa. International Journal of Pest Management, 57 (1), 41-49.
• Kamatou G.P.P., Viljoen A.M., Őzek T., Başer K.H.C., 2008. Head-space volatiles of Gethyllis afra and G. ciliaris fruits (“kukumakranka”). South African Journal of Botany, 74 (4), 768-770.
• Kamariah A.S., Lim L.B., Baser K.H.C., Ozek T., Demirci B., 1999. Composition of the essential oil of Plumeria obtusa L. Flavour and Fragrance Journal, 14 (4), 237-240.
• Karakoç Ö.C., Gökçe A., Telci I., 2006. Fumigant activity of some plant essential oils against Sitophilus oryzae L., Sitophilus granarius L. (Col.: Curculionidae) and Acanthoscelides obtectus Say. (Col.: Bruchidae). Turkish Journal of Entomology, 30 (2), 123-135.
• Kawakami M., Kobayashi A., 1991. Volatile constituents of green mate and roasted mate. Journal of Agricultural and Food Chemistry, 39 (7), 1275-1279.
• Kaya A., Demirci B., Başer K.H.C., 2003. The essential oil of Seseli tortuosum L. growing in Turkey. Flavour and Fragrance Journal, 18 (2), 159-161.
• Kılıç C.S., Coşkun M., Duman H., Demirci B., Başer K.H., 2010. Comparison of the essential oils from fruits and roots of Prangos denticulata Fisch. et Mey. growing in Turkey. Journal of Essential Oil Research, 22 (2), 170-173.
• Kim M.K., Jang Y.S., Ahn Y.J., Lee D.K., Lee H.S., 2002. Larvicidal activity of Australian and Mexican plant extracts against Aedes aegypti and Culex pipiens pallens (Diptera: Culicidae). Journal of Asia-Pacific Entomology, 5 (2), 227-231.
• Kırımer N., Tabanca N., Özek T., Tümen G., Baser K.H.C., 2000. Essential oils of annual Sideritis species growing in Turkey. Pharmaceutical Biology, 38 (2), 106-111.
• Kıvçak B., Akay S., Demirci B., Başer K., 2004. Chemical composition of essential oils from leaves and twigs of Pistacia lentiscus, Pistacia lentiscus var. chia, and Pistacia terebinthus from Turkey. Pharmaceutical Biology, 42 (4-5), 360-366.
• Kollmannsberger H., Nitz S., Drawert F., 1992. Über die Aromastoffzusammensetzung von Hochdruckextrakten. Zeitschrift fur Lebensmittel-Untersuchung und Forschung, 194 (6), 545-551.
• Kumazawa K., Masuda H., 1999. Identification of potent odorants in Japanese green tea (Sen-cha). Journal of Agricultural and Food Chemistry, 47 (12), 5169-5172.
• Lardos A., 2006. The botanical materia medica of the Iatrosophikon—a collection of prescriptions from a monastery in Cyprus. Journal of Ethnopharmacology, 104 (3), 387-406.
• Lin S.Y., Trumble J.T., Kumamoto J., 1987. Activity of volatile compounds in glandular trichomes of Lycopersicon species against two insect herbivores. Journal of Chemical Ecology, 13 (4), 837-850.
• López M.D., Pascual-Villalobos M.J., 2010. Mode of inhibition of acetylcholinesterase by monoterpenoids and implications for pest control. Industrial Crops and Products, 31 (2), 284-288.
• Madkour M.H., Zaitoun A.A., Singer F.A., 2012. Efficacy of three plant species extracts in the control of Trogoderma granarium Everts (Coleoptera: Dermestidae). Journal of Food, Agriculture & Environment, 10 (2 part 3), 1200-1203.
• Majdoub O., Dhen N., Souguir S., Haouas D., Baouandi M., Laarif A., Chaieb I., 2014. Chemical composition of Ruta chalepensis essential oils and their insecticidal activity against Tribolium castaneum. Tunisian Journal of Plant Protection, 9 (1), 83-90.
• Mancebo F., Hilje L., Mora G.A., Castro V.H., Salazar R., 2001. Biological activity of Ruta chalepensis (Rutaceae) and Sechium pittieri (Cucurbitaceae) extracts on Hypsipyla grandella (Lepidoptera: Pyralidae) larvae. Revista de Biología Tropical, 49 (2), 501-508.
• Marcomini A.M., Alves L.F.A., Bonini A.K., Mertz N.R., Santos J.D., 2009. Atividade inseticida de extratos vegetais e do óleo de nim sobre adultos de Alphitobius diaperinus Panzer (Coleoptera, Tenebrionidae). Arquivos do Instituto Biológico, 76 (3), 409-416.
• Martin D.T., Baributsa D., Huesing J.E., Williams S.B., Murdock L.L., 2015. PICS bags protect wheat grain, Triticum aestivum (L.), against rice weevil, Sitophilus oryzae (L.) (Coleoptera: Curculionidae). Journal of Stored Products Research, 63, 22-30.
• Mckenzie J.D., Goldman R., 2005. The Student guide to MINITAB release 14 Manual. Pearson Education, Boston, MA.
• Mejri J., Bouajila J., Ali S.B.S., Abderrabba M., Mejri M., 2012. Ruta chalepensis L. essential oil: chemical composition and phytotoxic activity. Journal of Biologically Active Products from Nature, 2 (6), 341-352.
• Miyazawa M., Watanabe H., Kameoka H., 1997. Inhibition of acetylcholinesterase activity by monoterpenoids with ap-menthane skeleton. Journal of Agricultural and Food Chemistry, 45 (3), 677-679.
• Miyazawa M., Yamafuji C., 2005. Inhibition of acetylcholinesterase activity by bicyclic monoterpenoids. Journal of Agricultural and Food Chemistry, 53 (5), 1765-1768.
• Moawad S.S., Al-Barty A.M., 2011. Evaluation of some medicinal and ornamental plant extracts toward pomegranate aphid, Aphis punicae (Passerini) under laboratory conditions. African Journal of Agricultural Research, 6 (10), 2425-2429.
• Narain N., Galvão M.D.S., Ferreira D.D.S., Navarro D.M., 2007. Flavor biogeneration in Mangaba (Hancornia speciosa Gomes) fruit. Revista Brasileira de Engenharia de Biossistemas, 1 (1), 25-31.
• Ntalli N.G., Manconi F., Leonti M., Maxia A., Caboni P., 2011. Aliphatic ketones from Ruta chalepensis (Rutaceae) induce paralysis on root knot nematodes. Journal of Agricultural and Food Chemistry, 59 (13), 7098-7103.
• Özek G., Demirci F., Özek T., Tabanca N., Wedge D.E., Khan S.I., Başer K.H.C., Duran A., Hamzaoglu E., 2010. Gas chromatographic–mass spectrometric analysis of volatiles obtained by four different techniques from Salvia rosifolia Sm., and evaluation for biological activity. Journal of Chromatography A, 1217 (5), 741-748.
• Prakash A., Rao J., 1996. Botanical pesticides in agriculture. CRC Press, Lewis Publishers, Boca Raton, Florida, 476 pp.
• Pathak M.A., Daniels Jr, F., Fitzpatrick T.B., 1962. The presently known distribution of furocoumarins (psoralens) in plants. Journal of Investigative Dermatology, 39 (3), 225-239.
• Perez López L.A., de la Torre Y.C., Cirio A.T., de Torres N.W., Flores Suárez A.E., Aranda R.S., 2015. Essential oils from Zanthoxylum fagar a wild lime, Ruta chalepensis L. and Thymus vulgaris L.: composition and activity against Aedes aegypti larvae. Pakistan Journal of Pharmaceutical Sciences, 28, 1911-1915.Pimentel M.A.G., Faroni L.R.D.A., Batista M.D., Silva F.H.D., 2008. Resistance of stored-product insects to phosphine. Pesquisa Agropecuária Brasileira, 43, 1671-1676.
• Pino J.A., Márquez E., Castro D., 2009. Volatile and non‐volatile acids of noni (Morinda citrifolia L.) fruit. Journal of the Science of Food and Agriculture, 89 (7), 1247-1249.
• Polatoğlu K., Karakoç Ö.C., 2016. Biologically active essential oils against stored product pests. Essential Oils in Food Preservation, Flavor and Safety, Chapter 5, Elsevier Inc., 39-59. http://dx.doi.org/10.1016/B978-0-12-416641-7.00005-5
• Polatoğlu K., Demirci F., Demirci B., Gören N., Baser K.H.C., 2010. Antimicrobial activity and essential oil composition of a new T. argyrophyllum (C. Koch) Tvzel var. argyrophyllum chemotype. Journal of Oleo Science, 59 (6), 307-313.
• Pollio A., De Natale A., Appetiti E., Aliotta G., Touwaide A., 2008. Continuity and change in the Mediterranean medical tradition: Ruta spp.(Rutaceae) in hippocratic medicine and present practices. Journal of Ethnopharmacology, 116 (3), 469-482.
• Rajendran S., Sriranjini V., 2008. Plant products as fumigants for stored-product insect control. Journal of Stored Products Research, 44 (2), 126-135.
• Rattan R.S., 2010. Mechanism of action of insecticidal secondary metabolites of plant origin. Crop Protection, 29 (9), 913-920.
• Rustaiyan A., Khossravi M., Sultani-Lotfabadi F., Yari M., Masoudi S., Monfared A., 2002. Constituents of the essential oil of Ruta chalepensis L. from Iran. Journal of Essential Oil Research, 14 (5), 378-379.
• Sasanelli N., 1992. Nematicidal activity of aqueous extracts from leaves of Ruta graveolens on Xiphinema index. Nematologia Mediterranea, 20 (1), 53-55.
• Sasanelli N., D'Addabbo T., 1993. Effect of Cineraria maritima, Ruta graveolens and Tagetes erecta leaf and root extracts on Italian populations of Meloidogyne species. Nematologia Mediterranea, 21 (1), 21-25.
• Shah T.B., Saeed M., Khan I., Khan A., Khan G.Z., Farid A., Khan S.M., 2015. Repellency evaluation of selected indigenous medicinal plant materials against Rhyzopertha dominica (Herbst) (Coleoptera: Tenebrionidae). Journal of Entomology and Zoology Studies, 3, 65-68.
• Shaaya E., Kostjukovski M., Eilberg J. E., Sukprakarn C., 1997. Plant oils as fumigants and contact insecticides for the control of stored-product insects. Journal of Stored Products Research, 33 (1), 7-15.
• Soto-Monterrosa F., Hilje-Quirós L., Mora-López G.A., Aguilar-Vega M.E., Carballo-Vargas M., 2007. Systemic activity of plant extracts in Cedrela odorata (Meliaceae) seedlings and their biological activity on Hypsipyla grandella (Lepidoptera: Pyralidae) larvae. Actividad sistémica de extractos vegetales en plántulas de Cedrela odorata (Meliaceae) y su actividad biológica sobre larvas de Hypsipyla grandella (Lepidoptera: Pyralidae). Agricultural and Forest Entomology, 9, 221-226.
• Stashenko E.E., Villa H.S., Combariza M.Y., 1995. Comparative study of Colombian rue oils by high resolution gas chromatography using different detection systems. Journal of Microcolumn Separations, 7 (2), 117-122.
• Stashenko E.E., Acosta R., Martı́nez J.R., 2000. High-resolution gas-chromatographic analysis of the secondary metabolites obtained by subcritical-fluid extraction from Colombian rue (Ruta graveolens L.). Journal of Biochemical and Biophysical Methods, 43 (1), 379-390.
• Tabanca N., Demirci B., Gürbüz İ., Demirci F., Becnel J.J., Wedge D.E., Can Başer K.H., 2011. Essential oil composition of five collections of Achillea biebersteinii from central Turkey and their antifungal and insecticidal activity. Natural Product Communications, 6 (5), 701-706.
• Tabanca N., Demirci B., Baser K.H.C., Mincsovics E., Khan S.I., Jacob M.R., Wedge D.E., 2007. Characterization of volatile constituents of Scaligeria tripartita and studies on the antifungal activity against phytopathogenic fungi. Journal of Chromatography B, 850 (1-2), 221-229.
• Tabanca N., Demirci B., Baser K.H.C., Aytac Z., Ekici M., Khan S.I., Jacob M.R., Wedge D.E., 2006. Chemical composition and antifungal activity of Salvia macrochlamys and Salvia recognita essential oils. Journal of Agricultural and Food Chemistry, 54 (18), 6593-6597.
• Tabanca N., Demirci B., Kirimer N., Baser K.H.C., Bedir E., Khan I.A., Wedge D.E., 2005. Gas chromatographic–mass spectrometric analysis of essential oils from Pimpinella aurea, Pimpinella corymbosa, Pimpinella peregrina and Pimpinella puberula gathered from Eastern and Southern Turkey. Journal of Chromatography A, 1097 (1-2), 192-198.
• Tounsi M.S., Wannes W.A., Ouerghemmi I., Msaada K., Smaoui A., Marzouk B., 2011. Variation in essential oil and fatty acid composition in different organs of cultivated and growing wild Ruta chalepensis L. Industrial Crops And Products, 33 (3), 617-623.
• Tümen G., Başer K.H.C., Demirci B., Ermin N., 1998. The essential oils of Satureja coerulea Janka and Thymus aznavourii Velen. Flavour and Fragrance Journal, 13 (1), 65-67.
• Tzakou O., Couladis M., 2001. Essential oil of Ruta chalepensis L. from Greece. Journal of Essential Oil Research, 13 (4), 258-259.
• Udo I.O., 2005. Evaluation of the potential of some local spices as stored grain protectants against the maize weevil Sitophilus zeamais Mots (Coleoptera: Curculionidae). Journal of Applied Sciences and Environmental Management, 9 (1), 165 – 168.
• Ulubelen A., Terem B., Tuzlaci E., Cheng K.F., Kong Y.C.,1986. Alkaloids and coumarins from Ruta chalepensis. Phytochemistry, 25 (11), 2692-2693.
• Van Vuuren S.F., Viljoen A.M., Őzek T., Demirci B., Başer K.H.C., 2007. Seasonal and geographical variation of Heteropyxis natalensis essential oil and the effect thereof on the antimicrobial activity. South African Journal of Botany, 73 (3), 441-448.
• Van Vuuren S.F., Viljoen A.M., Van Zyl R.L., Van Heerden F.R., Başer K.H.C., 2006. The antimicrobial, antimalarial and toxicity profiles of helihumulone, leaf essential oil and extracts of Helichrysum cymosum (L.) D. Don subsp. cymosum. South African Journal of Botany, 72 (2), 287-290.
• Villaverde J.J., Sevilla‐Morán B., Sandín‐España P., López‐Goti C., Alonso‐Prados J.L., 2014. Biopesticides in the framework of the European Pesticide Regulation (EC) No. 1107/2009. Pest Management Science, 70 (1), 2-5.
• Viney D.E., 1994. An illustrated flora of north Cyprus. Koenigstein, Germany, Koeltz Scientific Books, 697 pp.
• Wen Y.Q., He F., Zhu B.Q., Lan Y.B., Pan Q.H., Li C.Y., Reeves M.J., Wang J., 2014. Free and glycosidically bound aroma compounds in cherry (Prunus avium L.). Food Chemistry, 152, 29-36.
• Wszelaki N., Kuciun A., Kiss A., 2010. Screening of traditional European herbal medicines for acetylcholinesterase and butyrylcholinesterase inhibitory activity. Acta Pharmaceutica, 60 (1), 119.
• Yaacob K.B., Abdullah C.M., Joulain D., 1989. Essential oil of Ruta graveolens L. Journal of Essential Oil Research, 1 (5), 203-207.
• Yazdgerdian A.R., Akhtar Y., Isman M.B., 2015. Insecticidal effects of essential oils against woolly beech aphid, Phyllaphis fagi (Hemiptera: Aphididae) and rice weevil, Sitophilus oryzae (Coleoptera: Curculionidae). Journal of Entomology and Zoology Studies, 3 (3), 265-271.
• Yıldırım E., Ozbek H., Alan I., 2001. Depolanmış ürün zararlıları, Atatürk Üniversitesi Ziraat Fakültesi Yayınları, No: 191, Erzurum, 117.
• Zar J.H., 1996. Biostatistical Analysis. 3rd Edition, Prentice Hall, Upper Saddle River, 662 p.