Insecticidal effects of Moroccan plant extracts on development, energy reserves and enzymatic activities of Plodia interpunctella

  • N. Bouayad PER – Centre des Études Environnementales Méditerranéennes, Laboratoire de Biologie Appliquée & Sciences de l’Environnement, Université Abdelmalek Essaadi, Faculté des Sciences et Techniques, B.P. 416, Tanger
  • K. Rharrabe Département des Ressources Naturelles, Faculté Polydisciplinaire-Larache, Université Abdelmalek Essaadi, B.P. 745, Larache
  • N. N. Ghailani PER – Centre des Études Environnementales Méditerranéennes, Laboratoire de Biologie Appliquée & Sciences de l’Environnement, Université Abdelmalek Essaadi, Faculté des Sciences et Techniques, B.P. 416, Tanger
  • R. Jbilou PER – Centre des Études Environnementales Méditerranéennes, Laboratoire de Biologie Appliquée & Sciences de l’Environnement, Université Abdelmalek Essaadi, Faculté des Sciences et Techniques, B.P. 416, Tanger
  • P. Castañera Centro de Investigaciones Biológicas, CSIC, Ramiro de Maeztu 9, 28040 Madrid
  • F. Ortego Centro de Investigaciones Biológicas, CSIC, Ramiro de Maeztu 9, 28040 Madrid
Keywords: bioinsecticides, detoxification enzymes, digestive enzymes, reserve substances


The aim of this work was to study the effects of methanol extracts of ten plant species used in traditional medicine in Morocco (Peganum harmala, Ajuga iva, Rosmarinus officinalis, Lavandula stoechas, Lavandula dentata, Cistus ladanifer, Cistus salviaefolius, Cistus monspeliensis, Centaurium erythraea and Launaea arborescens) on Plodia interpunctella Hübner (Lepidoptera: Pyralidae) larvae. Firstly, we studied the effects of the ingestion of these extracts at 500 ppm on post-embryonic development parameters. Most plant extracts provoked a notable decrease of larval weight 8 days after treatment (up to 33% weight loss with C. erythraea) and caused significant alterations on pupation (ranging from 5% to 85%) and adult emergence (below 2.5% with R. officinalis, C. erythraea and A. iva). The plant extracts that showed strongest effects on post-embryonic development were selected to test their effects on the following physiological parameters: larval reserve substances (at 500 ppm); and midgut activities of hydrolytic and detoxification enzymes (at 500, 750 and 1000 ppm). All treatments provoked a significant reduction of protein and carbon hydrate larval contents, the inhibition of proteases and α-amylase activities in a dose depended manner, and the induction of glutathione S-transferase and esterase (using MtB as substrate) activities, whereas the activity of cytochrome P450 monooxygenases and esterases (using 1-NA as substrate) increase or decrease depending on the extract concentration and the plant analyzed.


Download data is not yet available.


Abbassi K, Kadiri AZ, Ghaout S, 2003a. Biological effects of alkaloids extracted from three plants of Moroccan arid areas on the desert locust. Physiol Entomol 28: 232-236. 

Abbassi K, Mergaoui L, Kadiri AZ, Stambouli A, Ghaout S, 2003b. Effets des extraits de Peganum harmala (Zygophyllaceae) sur le criquet pèlerin (Schistocerca gregaria Forskål, 1775). Zool Baet 13/14: 203-217. 

Ahmad S, Brattsten LB, Mullin CA, Yu SJ, 1986. Enzymes involved in the metabolism of plant allelochemicals. In: Molecular aspects of insect-plant associations (Brattsten LB, Ahmad S, eds). Plenum Press, NY, pp: 73-151. 

Arrese El, Soulages JL, 2010. Insect fat body: energy, metabolism, and regulation. Annu Rev Entomol 55: 207-25.
PMid:19725772 PMCid:3075550 

Arrese EL, Canavoso LE, Jouni ZE, Pennington JE, Tsuchida K, Wells MA, 2001. Lipid storage and mobilization in insects: current status and future directions. Insect Biochem Mol Biol 31: 7-17. 

Azelmat K, Sayah F, Mouhib M, Ghailani N, El Garrouj D, 2005. Effects of gamma irradiation on fourth-instar Plodia interpunctella (Hübner) (Lepidoptera: Pyralidae). J Stored Prod Res 41: 423-431. 

Baker JE, 1986. Amylase/proteinase ratios in larval midguts of ten stored-product insects. Ent Exp Appl 40: 41-46. 

Baker JE, Woo SM, Byrd RV, 1984. Ultrastructural features of the gut of Sitophilus granarius (L.) (Coleoptera: Curculionidae) with notes on distribution of proteinases and amylases in crop and midgut. Can J Zoolog 62: 1251-1259. 

Bellakhdar J, 1997. La pharmacopée marocaine traditionnelle-Médecine arabe et savoirs populaires. Ibis Press, Paris.

Berenbaum MR, Neal JJ, 1985. Synergism between myristicin and xanthotoxin, a naturally occurring plant toxicant. J Chem Ecol 11: 1349-1358. 

Bouayad N, Rharrabe K, Ghailani N, Sayah F, 2008. Effects of different food commodities on development of Plodia interpunctella (Hübner) (Lepidoptera: Pyralidae). J Stored Prod Res 44: 373-378. 

Bouayad N, Rharrabe K, Lamhamdi M, Ghailani NN, Sayah F, 2012. Dietary effects of harmine, a β-carboline alkaloid, on development, energy reserves and α-amylase activity of Plodia interpunctella Hübner (Lepidoptera, Pyralidae). Saudi J Biol Sci 19: 73-80. 

Bradford MM, 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle protein-dye binding. Anal Biochem 72: 248-254. 

Brattsten LB, 1987. Inductibility of metabolic insecticide defences in boll budworm caterpillars. Pestic Bioch Physiol 27: 13-23. 

Caballero C, López-Olguín JL, Ruiz M, Ortego F, Castañera P, 2008. Antifeedant activity and effects of terpenoids on detoxication enzymes of the beet armyworm, Spodoptera exigua (Hübner). Span J Agric Res 6: 177-184. 

Canavoso LE, Jouni ZE, Karnas KJ, Pennington JE, Wells MA, 2001. Fat metabolism in insects. Annu Rev Nutrition 21: 23-46.

Duffey SS, Stout MJ, 1996. Antinutritive and toxic components of plant defense against insects. Arch Insect Biochem Physiol 32: 3-37.<3::AID-ARCH2>3.0.CO;2-1 

Ellman GL, 1959. Tissue sulfhydryl groups. Arch Biochem Biophys 82: 70-77. 

Franco LO, Rigden DJ, Melo RF, Grossi-De-Sá FM, 2002. Plant α-amylase inhibitors and their interaction with insect α-amylases. Structure, function and potential for crop protection. Eur J Biochem 269: 397-412.

Gomori G, 1953. Human esterases. J Lab Clin Med 42: 445-453.

Habig WH, Pabst MJ, Jakoby WB, 1974. Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem 249: 7130-7139.

Hill SR, Orchard I, 2005. In vitro analysis of the digestive enzymes amylase and α-glucosidase in the midguts of Locusta migratoria L. in response to the myosuppressin, SchistoFLRFamide. J Insect Physiol. 51: 1-9.

Huang Z, Shi P, Dai J, Du J, 2004. Protein metabolism in Spodoptera litura (F.) is influenced by the botanical insecticide azadirachtin. Pest Biochem Physiol 80: 85-93. 

Isman MB, 2002. Insect antifeedants. Pestic Outlook 13: 152-157. 

Jbilou R, Sayah F, 2008. Effects of Peganum harmala (Zygophyllaceae) seed extracts on the development of Tribolium castaneum (Coleoptera: Tenebrionidae). Int J Trop Insect Sci 27: 199-209. 

Jbilou R, Amri H, Bouayad N, Ghailani N, Ennabili A, Sayah F, 2008. Insecticidal effects of extracts of seven plant species on larval development, α-amylase activity and offspring production of Tribolium castaneum (Herbst) (Insecta: Coleoptera: Tenebrionidae). Bioresour Technol 99: 959-964.

Jing L, Fang Y, Ying X, Wenxing H, Meng X, Syed M, Syed N, Fang C, 2005. Toxic impact of ingested Jatropherol-I on selected enzymatic activities and the ultrastructure of midgut cells in silkworm, Bombyx mori L. J App Entomol 129: 98-104.


Kao CH, Sun CN, 1991. In vitro degradation of some organophosphorus insecticides by sucseptible and resistant diamondback moth. Pestic Bioch Physiol 41: 132-141. 

Khambay BPS, Beddie DG, Simmonds MSJ, 2002. An insecticidal mixture of tetramethylcyclohexenedione isomers from Kunzea ambigua and Kunzea baxterii. Phytochemistry 59: 69-71. 

Lehane MJ, Müller HM, Crisanti A, 1996. Mechanisms controlling the synthesis and secretion of digestive enzymes in insects. In: Biology of the insect midgut (Lehane MJ, Billingsley PF, eds). Chapman & Hall, London, pp: 195-205. 

Liang GM, Chen W, Liu TX, 2003. Effects of three neem-based insecticides on diamondback moth (Lepidoptera: Plutellidae). Crop Prot 22: 333-340. 

Liu ZL, Ho SH, Goh SH, 2008. Effect of fraxinellone on growth and digestive physiology of Asian corn borer, Ostrinia furnacalis Guenee. Pestic Bioch Physiol 91: 122-127. 

Liu ZL, Ho SH, Goh SH, 2009. Modes of action of fraxinellone against the tobacco budworm, Heliothis virescens. Insect Sci 16: 147-155. 

Masters BSS, Kamin H, Gibson QH, Williams CH, 1965. Studies on the mechanism of microsomal triphosphopyridine nucleotide-cytochrome c reductase. J Biol Chem 240: 921-931.

Mordue AJL, Morgan ED, Nisbet AJ, 2005. Azadirachtin, a natural product in insect control. In: Comprehensive molecular insect science (Gilbert LI, Iatrou K, Gill S, eds), pp: 116-135. 

Nasiruddin M, Mordue (Luntz) AJ, 1993. The effects of azadirachtin on the midgut histology of the locusts Schistocerca gregaria and Locusta migratoria. Tissue Cell 25: 875-884. 

Oppenoorth FJ, Smissaert HR, Welling W, Van Der Pas LJT, Hitman KT, 1977. Insensitive acetylcholinesterase, high glutathione-S-transferase, and hydrolytic activity as resistance factors in a tetrachlorvinphos-resistant strain of house fly. Pestic Bioch Physiol 7: 34-47. 

Oppert B, Kramer KJ, Johnson D, Upton SJ, Mcgaughey WH, 1996. Luminal proteinases from Plodia interpunctella and the hydrolysis of Bacillus thuringiensis Cry1A(c) protoxin. Insect Biochem Mol Biol 26: 571-583. 

Ortego F, Rodríguez B, Castañera P, 1995. Effects of neo-clerodane diterpenes from Teucrium on feeding behavior of Colorado potato beetle larvae. J Chem Ecol 21: 1375-1386. 

Ortego F, Novillo C, Castañera P, 1996. Characterization and distribution of digestive proteases of the stalk corn borer, Sesamia nonagrioides Lef. (Lepidoptera: Noctuidae). Arch Insect Biochem Physiol 33: 163-180.<163::AID-ARCH6>3.0.CO;2-Z 

Ortego F, López-Olguín J, Ruíz M, Castañera P, 1999. Effects of toxic and deterrent terpenoids on digestive protease and detoxication enzyme activities of Colorado potato beetle larvae. Pest Biochem Physiol 63: 76-84. 

Papachristos DP, Stamopoulos DC, 2002. Repellent, toxic and reproduction inhibitory effects of essential oil vapours on Acanthoscelides obtectus (Say) (Coleoptera: Bruchidae). J Stored Prod Res 38: 117-128. 

Patil BS, Vanamal J, Hallman G, 2004. Irradiation and storage influence on bioactive components and quality of early and late season `Rio Red´ grapefruit (Citrus paradisi Macf.). Posthavest Biol Technol 34: 53-64. 

Phillips WT, Throne TE, 2010. Biorational approaches to managing stored-product insects. Annu Rev Entomol 55: 375-397.

Polis GA, 1998. Exploitation competition and the evolution of interference, cannibalism, and intraguild predation in age/size-structured populations. In: Size-structured populations (Ebenman B, Persson L, eds). Springer, Berlin, Heidelberg, pp: 185-202. 

Rharrabe K, Bakrim A, Ghailani N, Sayah F, 2007. Bioinsecticidal effect of harmaline on Plodia interpunctella development (Lepidoptera: Pyralidae). Pest Biochem Physiol 89: 137-145. 

Rharrabe K, Amri H, Bouayad N, Sayah F, 2008. Effects of azadirachtin on post-embryonic development, energy reserves and α-amylase activity of Plodia interpunctella Hübner (Lepidoptera: Pyralidae). J Stored Prod Res 44: 290-294. 

Rharrabe K, Bouayad N, Sayah F, 2009. Effects of ingested 20-hydroxyecdysone on development and midgut epithelial cells of Plodia interpunctella (Lepidoptera, Pyralidae). Pest Biochem Physiol 93: 112-119. 

Roe JH, 1955. Determination of sugar in blood and spinal fluid with anthrone reagent. J Biol Chem 212: 335-338.

Scott JG, Liu N, Wen ZM, 1998. Insect cytochromes P450: diversity, insecticide resistance and tolerance to plant toxins. Comp Biochem Physiol 121C: 147-155. 

Senthil Nathan S, 2006. Effect of Melia azedarach on nutritional physiology and enzyme activities of the rice leaffolder Cnaphalocrocis melinalis (Guenée) (Lepidoptera: Pyralidae). Pestic Biochem Physiol 84: 98-108. 

Senthil Nathan S, Kalaivani K, Chung PG, 2005a. The effects of azadirachtin and nucleopolyhedrovirus on midgut enzymatic profile of Spodoptera litura Fab. (Lepidoptera: Noctuidae). Pest Biochem Physiol 83: 46-57. 

Senthil Nathan S, Kalaivani K, Murugan K, Chung PG, 2005b. The toxicity and physiological effect of neem limonoids on Cnaphalocrocis medinalis (Guenée) the rice leaffolder. Pest Biochem Physiol 81: 113-122. 

Smirle MJ, Lowery DT, Zurowski CL, 1996. Influence of neem oil on detoxication enzyme activity in the obliquebanded leafroller, Choristoneura rosaceana. Pest Biochem Physiol 56: 220-230. 

Statistica, 1997. Statistica statsoft Inc. release 5.1. Tulsa, OK, USA.


Sun CN, Huang SY, Hu NT, Chung WY, 2001. Glutathione S-transferase and insect resistance to insecticides. In: Biochemical sites of insecticide action and resistance (Ishaaya I, ed). Springer, Berlin, pp: 239-252. 

Terra WR, Ferreira C, 1994. Insect digestive enzymes-properties, compartmentalization and function. Comp Biochem Phys B 109: 1-62. 

Terriere LC, 1984. Induction of detoxication enzymes in insects. Ann Rev Entomol 29: 71-88.

Valencia A, Bustillo AE, Ossa GE, Chrispeels MJ, 2000. Alpha-amylases of the coffee berry borer (Hypothenemus hampei) and their inhibition by two plant amylase inhibitors. Insect Biochem Mol Biol 30: 207-213. 

Van Handel E, 1965. Micro-separation of glycogen, sugars and lipids. Anal Biochem 11: 266-271. 

Via S, 1999. Cannibalism facilitates the use of a novel environment in the flour beetle, Tribolium castaneum. Heredity 82: 267-275.

Weimin Li, Mary AS, May RB, 2003. Diversification of furanocoumarin-metabolizing cytochrome P450 monooxygenases in two papilionids: Specificity and substrate encounter rate. Proc Nat Acad Sci USA 100(Suppl 2): 14593-14598.
PMid:12968082 PMCid:304124 

White NDG, 1995. Insects, mites and insecticides in stored grain ecosystems. In: Stored grain ecosystem (Jayas DS, White ND, Muir WE, eds). Marcel Dekker, NY, pp: 123-168. 

Yu SJ, 1983. Induction of detoxifying enzymes by allelochemicals and host plants in the fall armyworm. Pestic Bioch Physiol 19: 330-336. 

Zöllner N, Krich K, 1962. The quantitative determination of lipids (micromethod) by means of sulphosphovanillin reaction common to many natural lipids (all known plasma lipids). Z Ges Exp Med 135: 54.

How to Cite
BouayadN., RharrabeK., GhailaniN. N., JbilouR., CastañeraP., & OrtegoF. (2012). Insecticidal effects of Moroccan plant extracts on development, energy reserves and enzymatic activities of Plodia interpunctella. Spanish Journal of Agricultural Research, 11(1), 189-198.
Plant protection