Advertisement

Neotropical Entomology

, Volume 48, Issue 2, pp 246–259 | Cite as

Olive Leaf Extracts Toxicity to the Migratory Locust, Locusta migratoria: Histopathological Effects on the Alimentary Canal and Acetylcholinesterase and Glutathione S-Transferases Activity

  • K AbdellaouiEmail author
  • O Boussadia
  • M Miladi
  • I Boughattas
  • G Omri
  • M Mhafdhi
  • M Hazzoug
  • F Acheuk
  • M Brahem
Systematics, Morphology and Physiology
  • 61 Downloads

Abstract

The migratory locust, Locusta migratoria (Linnaeus), is the most widespread locust species. Frequent applications of insecticides have inevitably resulted in environmental pollution and development of resistance in some natural populations of the locust. To find a new and safe alternative to conventional insecticides, experiments were conducted to assess the effect of olive leaf extracts on L. migratoria fifth instar larvae. The methanolic extracts were prepared from the leaves sampled during four phenological growth stages of olive tree which are as follows: Cluster formation (Cf), Swelling inflorescence buds (Sib), Full flowering (Ff), and Endocarp hardening (Eh). The most relevant result was noted with the extract prepared from the leaves collected at the Sib-stage. Results showed that treatment of newly emerged larvae resulted in a significant mortality with a dose-response relationship. The olive leaf extracts toxicity was also demonstrated by histopathological changes in the alimentary canal resulting in a considerable disorganization and serious damage of the midgut, ceca, and proventriculus structure. Epithelial cells alterations, less dense and degraded striated border, disintegrated regeneration crypts, vacuolarized cells, extrusion of cytoplasmic contents, and rupture of muscular layer were evident in the midgut and ceca of treated larvae. Data of biochemical analyzes showed that olive leaf extracts induced a significant decrease of the hemolymph metabolites (proteins, carbohydrates, and lipids). In a second series of experiments, we showed that the olive leaf extracts reduced the activity of acetylcholinesterase and induced the glutathione S-transferases with a dose-response relationship.

Keywords

Apolysis enzymes histology metabolites midgut olive tree phenological growth stages 

Notes

Acknowledgments

The authors acknowledge Dr. Nizar Chaira, Aridlands and Oases Cropping Laboratory, Institute of the Arid Areas of Medenine, Tunisia, for the help in metabolites quantification. The authors would like to express their gratitude to Mariem Hafi of the Laboratory of Olive Tree Ecophysiology and Mineral Analysis of Olive Tree Institute (IO) for providing the olive tree leaves samples and technical assistance.

References

  1. Abbott WS (1925) A method of computing the effectiveness of an insecticide. J Econ Entomol 18:265–267CrossRefGoogle Scholar
  2. Abdellaoui K, Ben Halima-Kamel M, Ben Hamouda MH (2009) Insecticidal activity of Gibberellic acid against Spodoptera littoralis (Lepidoptera, Noctuidae) and Locusta migratoria migratoria (Orthoptera, Acrididae). Pest Technology 3:28–33Google Scholar
  3. Abdellaoui K, Ben Halima-Kamel M, Acheuk F, Soltani N, Aribi N, Ben Hamouda MH (2013) Biochemical and histological effects of gibberellic acid on Locusta migratoria migratoria fifth instar larvae. Pestic Biochem Physiol 107:32–37CrossRefGoogle Scholar
  4. Abdellaoui K, Ben Halima-Kamel M, Acheuk F, Soltani N, Aribi N, Ben Hamouda MH (2015) Effects of gibberellic acid on ovarian biochemical composition and ecdysteroid amounts in the migratory locust Locusta migratoria (Orthoptera, Acrididae). International Journal Of Pest Management 61:68–72.  https://doi.org/10.1080/09670874.2014.995746
  5. Acheuk F, Cusson M, Doumandji-Mitiche B (2012) Effects of a methanolic extract of the plant Haplophyllum tuberculatum and of teflubenzuron on female reproduction in the migratory locust, Locusta migratoria (Orthoptera: Oedipodinae). J Insect Physiol 58:335–341CrossRefGoogle Scholar
  6. Acheuk F, Belaid M, Lakhdari W, Abdellaoui K, Dehliz A, Mokrane K (2017a) Repellency and toxicity of the crude ethanolic extract of Limoniastrum guyonianum against Tribolium castaneum. Tunis J Plant Prot 12:71–81Google Scholar
  7. Acheuk F, Lakhdari W, Abdellaoui K, Belaid M, Allouane R, Hallouane F (2017b) Phytochemical study and bioinsecticidal effect of the crude ethanolic extract of the algerian plant Artemisia judaica L. (Asteraceae) against the black bean aphid Aphis fabae Scop. Agriculture and Forestry 63:95–104.  https://doi.org/10.17707/AgricultForest.63.1.11
  8. Ammar M, N’cir S (2008) Incorporation of Cestrum parquii (Solanaceae) leaves in an artificial diet affected larval longevity and gut structure of the desert locust Schistocerca gregaria. Tunis J Plant Prot 3:27–34Google Scholar
  9. Ammar M, Barbouche N, Ben Hamouda MH (1995) Action des extraits de composés de feuilles de Cestrum parqii et d’Olea europea sur la longévité et la croissance du criquet pèlerin Schistocerca gregaria. Meded Fac Landbouwwet Univ Gent 60:831–836Google Scholar
  10. Ammar M, Barbouche N, Ben Hamouda MH (1997) Cuticle alteration and death of Schistocerca gregaria by difficulty in moulting under food effect of Cestrum parqui and Olea europea. In: Proceedings of the sixth arab congress of plant protection organized by the Arab Society for Plant Protection, 27–31 October 1997 Beirut, Arab Society for Plant Protection, 110 pGoogle Scholar
  11. Barbouche N, Ammar M, Ben Hamouda MH, Couillaud F, Girardie J (1996) Action d’une alimentation à base de feuilles d’olivier Olea europea sur la biosynthèse In vitro de la JH III par les carpora allata chez Schistocerca gregaria au cours de la vitéllogenèse. Arch Inst Pasteur Tunis 73:9–12Google Scholar
  12. Ben Hamouda A, Mohamed A, Ben Hamouda MH (2011) Effect of Olea europaea and Cestrum parqui leaves on the cuticle and brain of the desert locust Schistocerca gregaria Forsk. (Orthoptera: Acrididae). Pest Technology 5:55–58Google Scholar
  13. Ben Hamouda A, Boussadia O, Bedis K, Laarif A, Braham M (2015) Studies on insecticidal and deterrent effects of olive leaf extracts on Myzus persicae and Phthorimaea operculella. J Entomol Zool Stud 3:294–297Google Scholar
  14. Ben Hamouda A, Boussadia O, Bedis K, Chaieb I, Laarif A, Braham M (2016) Effect of olive leaf extracts on the feeding, growth and metabolism of Spodoptera littoralis. Tunis J Plant Prot 11:63–72Google Scholar
  15. Bhonwong A, Stout MJ, Attajarusit J, Tantasawat P (2009) Defensive role of tomato polyphenol oxidases against cotton bollworm (Helicoverpa armigera) and beet armyworm (Spodoptera exigua). J Chem Ecol 35:28–38CrossRefGoogle Scholar
  16. Boss A, Bishop KS, Marlow G, Barnett MPG, Ferguson LR (2016) Evidence to support the anti-cancer effect of olive leaf extract and future directions. Nutrients 8:513.  https://doi.org/10.3390/nu8080513 CrossRefGoogle Scholar
  17. Brader L, Djibo H, Faye FG, Ghaout S, Lazar M, Luzietoso PN, Ould Babah MA (2006) Towards a more effective response to desert locusts and their impacts on food insecurity, livelihoods and poverty. Multilateral evaluation of the 2003–05 desert locust campaign, FAO, Rome, Italy. http://www.fao.org/pbe/pbee/common/ecg/272/en/DesertLocustfinalReport.doc
  18. Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein dye-binding. Anal Biochem 72:248–254CrossRefGoogle Scholar
  19. Buhl J, Sumpter DJT, Couzin ID, Hale JJ, Despland E, Miller ER, Simpson SJ (2006) From disorder to order in marching locusts. Science 312:1402–1406CrossRefGoogle Scholar
  20. Céspedes CL, Torres P, Marin JC, Arciniegas A, Romo de Vivar A, Pérez-Castorena AL, Aranda E (2004) Insect growth inhibitor by tocotrienols and hydroquinones from Roldana barba johannis. Phytochemistry 65:1963–1975CrossRefGoogle Scholar
  21. Chapman RF (2013) The insects: structure and function. Cambridge University Press, United Kingdom, p 929Google Scholar
  22. De Vreyer P, Guilbert N, Mesple-Sompsa S (2014) Impact of natural disasters on education outcomes: evidence from the 1987-89 locust plague in Mali. J Afr Econ 24:57–100CrossRefGoogle Scholar
  23. Duchateau G, Florkin M (1959) Sur la tréhalosémie des insectes et sa signification. Arch Insect Biochem Physiol 67:306–314Google Scholar
  24. Ellman GL, Courtney KD, Andres JV, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95CrossRefGoogle Scholar
  25. Finney DJ (1971) Probit analysis. Cambridge University Press, Cambridge, p 333Google Scholar
  26. Gökçe A, Stelinsky LL, Whalon ME (2005) Behavioral and electrophysiological responses of leaf roller moths to selected plant extracts. Environ Entomol 34:1426–1432CrossRefGoogle Scholar
  27. Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferases, the first enzymatic step in mercapturic acid. J Biol Chem 249:7130–7139Google Scholar
  28. Hakan C, Mehmet K, Muhittin K (2016) Monitoring of mineral and polyphenol content in olive leaves underdrought conditions: application chemometric techniques. Ind Crop Prod 88:78–84CrossRefGoogle Scholar
  29. Hassan Adeyemi MM (2010) The potential of secondary metabolites in plant material as deterrents against insect pests: a review. Afr J Pure Appl Chem 4:243–246Google Scholar
  30. He YP, Ma EB, Zhu KY (2004) Characterizations of general esterases in relation to malathion susceptibility in two field populations of the oriental migratory locust, Locusta migratoria manilensis. Pest Biochem Physiol 78:103–113CrossRefGoogle Scholar
  31. Hoffmann KH, Lorenz MW (1998) Recent advances in hormones in insect pest control. Phytoparasitica 26:1–8CrossRefGoogle Scholar
  32. Ji R, Xie BY, Li DM, Li Z, Zhang X (2004) Use of Modis data to monitor the oriental migratory locust plague. Agric Ecosyst Environ 104:615–620CrossRefGoogle Scholar
  33. Lazar M, Piou C, Doumandji-Mitiche B, Lecoq M (2016) Importance of solitarious desert locust population dynamics: lessons from historical survey data in Algeria. Entomol Exp Appl 161:168–180CrossRefGoogle Scholar
  34. Lo Scalzo R, Scarpati ML, Verzebgnassi B, Vita G (1994) Olea europaea chemical repellent to Dacus oleae females. J Chem Ecol 20:1813–1923CrossRefGoogle Scholar
  35. Martoja M, Martoja R (1967) Initiation aux Techniques de l’Histologie Animale. Masson & Cie, FranceGoogle Scholar
  36. Nasiruddin M, Mordue AJ (1993) The effect of azadirachtin on the midgut histology of the locusts Schistocerca gregaria and Locusta migratoria. Tissue Cell 26:875–884CrossRefGoogle Scholar
  37. Pavela R (2009) Effectiveness of some botanical insecticides against Spodoptera littoralis Boisduvala (Lepidoptera: Noctudiae), Myzus persicae Sulzer (Hemiptera: Aphididae) and Tetranychus urticae Koch (Acari: Tetranychidae). Plant Prot Sci 45:161–167CrossRefGoogle Scholar
  38. Pener MP, Simpson SJ (2009) Locust phase polyphenism: an update. Adv Insect Phys 36:1–272CrossRefGoogle Scholar
  39. Pener MP, Yerushalmi Y (1998) The physiology of locust phase polymorphism: an update. J Insect Physiol 32:853–857CrossRefGoogle Scholar
  40. Qin G, Jia M, Liu T, Xuan T, Zhu KY, Guo Y, Ma E, Zhang J (2011) Identification and characterisation of ten glutathione S-transferase genes from oriental migratory locust, Locusta migratoria manilensis (Meyen). Pest Manag Sci 67:697–704CrossRefGoogle Scholar
  41. Qin G, Jia M, Liu T, Zhang X, Guo Y, Zhu KY, Ma E, Zhang J (2013) Characterization and functional analysis of four glutathione S-Transferases from the migratory locust, Locusta migratoria. PLoS One 8:e58410.  https://doi.org/10.1371/journal.pone.0058410 CrossRefGoogle Scholar
  42. Rattan RS (2010) Mechanism of action of insecticidal secondary metabolites of plant origin. Crop Prot 29:913–920CrossRefGoogle Scholar
  43. Scott IM, Jensen H, Scott JG, Isman MB, Arnason JT, Philogene BJR (2003) Botanical insecticides for controlling agricultural pests: piperamides and the Colorado potato beetle Leptinotarsa decemlineata Say (Coleoptera: Chrysomelidae). Arch Insect Biochem Physiol 54:212–225CrossRefGoogle Scholar
  44. Sharaby A, Montasser SA, Mahmoud YA, Ibrahim SA (2012) Natural plant essential oils for controlling the grasshopper (Heteracris littoralis) and their pathological effects on the alimentary canal. Ecol Balkanica 4:39–52Google Scholar
  45. Steedman A (1988) Locust handbook. Overseas Development Natural Resources Institute, London, p 180Google Scholar
  46. Sword GA, Lecoq M, Simpson SJ (2010) Phase polyphenism and preventative locust management. J Insect Physiol 56:949–957CrossRefGoogle Scholar
  47. Symmons P (1992) Strategies to combat the desert locust. Crop Prot 11:206–212CrossRefGoogle Scholar
  48. Thomas MB, Langewald J, Wood SN (1996) Evaluating the effects of a biopesticide on populations of the variegated grasshopper, Zonocerus Šariegatus. J Appl Ecol 33:1509–1516CrossRefGoogle Scholar
  49. Uvarov BP (1966) Grasshoppers and locusts. Cambridge University Press, p 613Google Scholar
  50. Vanhaelen N, Haubruge E, Lognay G, Francis F (2001) Hoverfly glutathione S-Transferases and effect of Brassicaceae secondary metabolites. Pestic Biochem Physiol 71:170–177CrossRefGoogle Scholar
  51. Wang JJ, Cheng W, Ding W, Zhao ZM (2004) The effect of the insecticide dichlorvous on esterase activity extracted from the psocids, Liposcelis bostrychophila and Liposcelis entomophila. J Insect Sci 4:1–5CrossRefGoogle Scholar
  52. Wei SH, Clark AG, Syvanen M (2001) Identification and cloning of a key insecticide-metabolizing glutathione S-transferase (MdGST-6A) from a hyper insecticide-resistant strain of the house-fly Musca domestica. Insect Biochem Mol Biol 31:1145–1153CrossRefGoogle Scholar
  53. Yang ML, Zhang JZ, Zhu KY, Xuan T, Liu XJ, Guo YP, Ma EB (2009) Mechanisms of organophosphate resistance in a field population of oriental migratory locust, Locusta migratoria manilensis (Meyen). Arch Insect Biochem Physiol 71:3–15CrossRefGoogle Scholar
  54. Yu SJ (1982) Host plant induction of glutathione-S-transferase in the fall armyworm. Pestic Biochem Physiol 18:101–106CrossRefGoogle Scholar
  55. Zhang M, Fang T, Pu G, Sun X, Zhou X, Cai Q (2013) Xenobiotic metabolism of plant secondary compounds in the English grain aphid, Sitobion avanae (F.) (Hemiptera: Aphididae). Pestic Biochem Physiol 107:44–49CrossRefGoogle Scholar

Copyright information

© Sociedade Entomológica do Brasil 2018

Authors and Affiliations

  1. 1.Dept of Biological Sciences and Plant Protection, Higher Agronomic Institute of Chott MariemSousse UnivSousseTunisia
  2. 2.Unit of SousseOlive Tree InstituteSousseTunisia
  3. 3.General Directorate of Plant Health and Agricultural Inputs ControlMinistry of AgricultureTunisTunisia
  4. 4.Lab of Valorization and Conservation of Biological Resources “Valcore,” Dept of Biology, Faculty of SciencesUniv of BoumerdesBoumerdesAlgeria

Personalised recommendations