Insecticidal activity and changes in midgut histology of the generalist herbivore, Spodoptera litura F. (Lepidoptera: Noctuidae) in response to seed extract of Annona squamosa Linn.
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Abstract
The tobacco caterpillar, Spodoptera litura F., is one of the most devastating, cosmopolitan polyphagous pests affecting major crops that significantly impact agricultural productivity. The present study aimed to evaluate the toxicological effect of seed extract of the medicinal plant, Annona squamosa L. and the histological effect on the midgut of Spodoptera litura F., under laboratory conditions. The crude methanolic extract of A. squamosa seed was tested against the third instar larvae of S. litura at five different concentrations viz., 0.5%, 1.0%, 1.5%, 2.0% and 2.5 % by leaf dip bioassay method. The seed extract exhibited larval mortality of 96.67%, 83.37 %,70%, 53.33% and 40 % at the concentrations 2.5 %, 2.0%, 1.5%, 1.0% and 0.5%, respectively.The results indicated that the response of larval mortality to the seed extract was dose-dependent. The dose of 0.5% showed the lowest mortality (40.00%), while the dose of 2.5 % showed maximum larval mortality (96.67%). Hence they were subjected to histological analysis. The anatomical sectioning of S. litura larval midgut treated with 0.5% concentration showed disruption in the peritrophic membrane and striated border of epithelial cells. The midgut of larvae treated with 2.5 % concentration showed an irregular epithelium and high vacuolization in the cytoplasmic cells. The results indicated that methanol extract of A. squamosa seed extract has the ability to cause changes in the midgut region, thereby affecting the digestion and nutrient absorption of S. litura larvae, which will lead to a debilitating effect on the development of larvae. Based on the present study A. squamosa seed extract will be a potential biopesticide for managing S. litura.
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Keywords
Annona squamosa seeds, Histology, Methanolic extract, Midgut, Spodoptera litura
References
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Anita, S., Sujatha, P.&Prabhudas, P. (2012). Efficacy of pulverised leaves of Annonasquamosa (L.), Moringa oleifera (Lam.) and Eucalyptus globulus (Labill.) against the stored grain pest, Triboliumcastaneum (Herbst.). Recent Res.Sci.Technol., 4(2), 19-23.
Armes, N. J., Wightman, J. A., Jadhav, D. R. & Ranga Rao, G. V. (1997). Status of insecticide resistance in Spodoptera litura in Andhra Pradesh, India. Pestic. Sci., 50(3), 240-248.
Azwanida, N. N. (2015). A review on the extraction methods use in medicinal plants, principle, strength and limitation. Med.Aromat. Plants, 4(196), 2167-2182.
Bancroft, J. D. & Gamble, M. (Eds.). (2008). Theory and practice of histological techniques. Elsevier health sciences.
Caccia, S., Casartelli, M. &Tettamanti, G. (2019). The amazing complexity of insect midgut cells: types, peculiarities, and functions. Cell Tissue Res., 377(3), 505-525.
Chauhan, D. & Mishra, V. K. (2016). Effect of medicinal plant extracts on growth and development of tobacco caterpillar, Spodoptera litura (Fabricius). Int. J. Agric. Environ. Biotechnol., 9(3), 435.
Devanand, P.& Rani, P. U. (2008). Biological potency of certain plant extracts in management of two lepidopteran pests of Ricinus communis L. J. Biopestic., 1(2), 170-176.
Deshmukhe, P. V., Hooli, A. A. & Holihosur, S. N. (2010). Bioefficacy of cold ethyl alcohol extract of Annona squamosa against Spodoptera lituraFabricius. J. Biopestic., 3(1), 271-283.
Farder-Gomes, C. F., Saravanan, M., Martinez, L. C., Plata-Rueda, A., Zanuncio, J. C. & Serrao, J. E. (2022). Azadirachtin-based biopesticide affects the respiration and digestion in Anticarsiagemmatalis caterpillars. Toxin Rev., 41(2), 466-475.
Fiaz, M., Martínez, L. C., da Silva Costa, M., Cossolin, J. F. S., Plata-Rueda, A., Gonçalves, W. G., ... & Serrão, J. E. (2018). Squamocininduce histological and ultrastructural changes in the midgut cells of Anticarsiagemmatalis (Lepidoptera: Noctuidae). Ecotoxicol. Environ. Saf., 156, 1-8.
Franzetti, E., Casartelli, M., D'Antona, P., Montali, A., Romanelli, D., Cappellozza, S., ... &Tettamanti, G. (2016). Midgut epithelium in molting silkworm: a fine balance among cell growth, differentiation, and survival. Arthropod Struct.Dev ., 45(4), 368-379.
Hidalgo, J. R., Parellada, E. A., Bardón, A., Vera, N. &Neske, A. (2018). Insecticidal activity of Annonaceousacetogenins and their derivatives on Spodoptera frugiperda Smith (Lepidoptera: Noctuidae). J. Agric. Food Chem., 7(03), 105.
Jackson, A. D. & McLaughlin, J. (2009). Digestion and absorption. Surgery (oxford), 27(6), 231-236.
Jose,V., Raphel, L., Aiswariya, K. S. & Mathew, P. (2021). Green synthesis of silver nanoparticles using Annona squamosa L. seed extract: characterization, photocatalytic and biological activity assay. Bioprocess Biosyst. Eng., 44, 1819-1829.
Kamaraj, C., Bagavan, A., Elango, G., Zahir, A. A., Rajakumar, G., Marimuthu, S., ... &Rahuman, A. A. (2011). Larvicidal activity of medicinal plant extracts against Anopheles subpictus&Culextritaeniorhynchus. Indian J. Med. Res., 134(1), 101.
Khalil, H., Moussa, S., Zein, H. S., Ahmed, D. S., Shaurub, E. S. H. &Elarabi, N. I. (2021). Alterations in the expression of certain midgut genes of Spodoptera littoralis (Boisd.)(Lepidoptera: Noctuidae) larvae and midgut histopathology in response to Bacillus thuringiensis Cry1C toxin. Egypt J. Biol. Pest Control., 31(1), 1-9.
Leatemia, J. A.&Isman, M. B. (2004). Toxicity and antifeedant activity of crude seed extracts of Annona squamosa (Annonaceae) against lepidopteran pests and natural enemies. Int. J. Trop. Insect Sci., 24(2), 150-158.
Leatemia, J. A.&Isman, M. B. (2004). Insecticidal activity of crude seed extracts of Annona spp., Lansiumdomesticum andSandoricumkoetjape against lepidopteran larvae. Phytoparasitica, 32(1), 30-37.
Lin, C. Y., Wu, D. C., Yu, J. Z., Chen, B. H., Wang, C. L. & Ko, W. H. (2009). Control of silverleaf whitefly, cotton aphid and kanzawa spider mite with oil and extracts from seeds of sugar apple. Neotrop. Entomol., 38, 531-536.
Ling, R., Yang, R., Li, P., Zhang, X., Shen, T., Li, X., ... & Yan, J. (2019). Asatone and isoasatone A against Spodoptera litura fab. by acting on cytochrome P450 monoxygenases and glutathione transferases. Mol., 24(21), 39-40.
Mahmoud, M. A. & Hassan, A. N. T. (2022). Insecticidal Activity of seed extracts of Annona squamosa L., against the cotton leafworm Spodoptera littoralis (Boisd.). Egypt. J. Chem., 65(6), 1-2.
Mishra, M., Gupta, K. K., & Kumar, S. (2015). Impact of the stem extract of Thevetia neriifolia on the feeding potential and histological architecture of the midgut epithelial tissue of early fourth instars of HelicoverpaarmigeraHübner. Int. J. Insect Sci., 7, IJIS-S29127.
Mondal, P., Biswas, S., Pal, K. & Ray, D. P. (2018). Annona squamosa as a potential botanical insecticide for agricultural domains: a review. IJBS, 5(1), 81-89.
Nenotek, P. S., Londingkene, J. A., Ludji, R., Harini, T. S., Kapa, M. J., Nguru, E. S., ... &Konanin, M. (2022). The toxicity of Annona squamosa seeds and Anacardium occidentale seed shells from East Nusa Tenggara, Indonesia, against cabbage caterpillar (Crocidolomia pavonana). Intl. J. Trop. Drylands, 6(1).39-44.
Patil, J. R. (2009). Studies on isolation and characterization of bioactive compounds in lime [Citrus aurantifolia (Christm) swingle], their antioxidant and anticancer properties. J. Biochem. Res., 18, 1-10.
Pinto, L. M. N., DrebesDörr, N. C.&Fiuza, L. M. (2011). The toxicity and histopathology of Bacillus thuringiensis Cry1Ba toxin to Spodoptera frugiperda (Lepidoptera, Noctuidae). In Microorganisms In Industry And Environment: From Scientific and Industrial Research to Consumer Products, 137-140.
Prijono, D., Gani, M. S.&Syahputra, E. (1997). Insecticidal activity of annonaceous seed extracts against Crocidolomiabinotalis Zeller (Lepidoptera: Pyralidae).Bulletin of Plant Pests and Diseases, 9, 1-6.
Rajguru, M.& Sharma, A. N. (2012). Comparative efficacy of plant extracts alone and in combination with Bacillus thuringiensis sub sp. kurstaki against Spodoptera litura Fab. larvae. J. Biopestic., 5(1), 81.
Sahu, B., Pachori, R., Navya, R. N. & Patidar, S. (2020). Extent of damage by Spodoptera litura on cabbage.J. Entomol. Zool. Stud., 8, 1153-1156.
Senthil-Nathan, S., Choi, M. Y., Paik, C. H.&Kalaivani, K. (2008). The toxicity and physiological effect of goniothalamin, a styryl-pyrone, on the generalist herbivore, Spodoptera exiguaHübner. Chemosphere, 72(9), 1393-1400.
Sheehan, D.C. & Hrapchak, B.B. 1980. Theory and Practice of Histotechnology. 2nd ed. Mosby, St. Louis, MO. pp. 40-44.
Souto, A. L.,Sylvestre, M., Tölke, E. D., Tavares, J. F., Barbosa-Filho, J. M. & Cebrián-Torrejón, G. (2021). Plant-derived pesticides as an alternative to pest management and sustainable agricultural production: Prospects, applications and challenges. Mol., 26(16), 4835.
Sreeletha, C. & Geetha, P. R. (2012). Pesticidal effects of Annona squamosa L. on male Oryctesrhinoceros Linn.(Coleoptera: Scarabaeidae) in relation to reproduction. Curr. Biotic., 6, 8-21.
Suryani, A. I., Hariani, N., Majid, A. F. & Amalia, D. N. (2020). Histological changes in the midgut of Spodoptera litura larvae exposured by the extract of Mirabilis jalapa leaves, In IOP Conference Series: Earth and Environmental Science, 484: 1-9. IOP Publishing.
Takeda, M. 2012. Structures and functions of insect midgut: The regulatory mechanisms by peptides, proteins and related compounds, Hemolymph Proteins and Functional Peptides: Recent Advances in Insects and Other Arthropods, 1,94-110.
Urs, K. C. D. & B. V. Subramanya. (1974). A simplified semi-synthetic diet for rearing Spodopteralitura (Fab.) in the laboratory,Curr. Res.3,40-41.
Vetal, D. S. & Pardeshi, A. B. (2019). Insecticidal potential of ethanol and hexane solvent seed extract of Annona squamosa against Spodoptera litura Fab.,J. Pharmacogn. Phytochem., 8(3), 842-845.
Ahmad, M., Sayyed, A. H., Saleem, M. A. & Ahmad, M. (2008). Evidence for field evolved resistance to newer insecticides in Spodoptera litura (Lepidoptera: Noctuidae) from Pakistan. Crop Prot., 27(10), 1367-1372.
Anita, S., Sujatha, P.&Prabhudas, P. (2012). Efficacy of pulverised leaves of Annonasquamosa (L.), Moringa oleifera (Lam.) and Eucalyptus globulus (Labill.) against the stored grain pest, Triboliumcastaneum (Herbst.). Recent Res.Sci.Technol., 4(2), 19-23.
Armes, N. J., Wightman, J. A., Jadhav, D. R. & Ranga Rao, G. V. (1997). Status of insecticide resistance in Spodoptera litura in Andhra Pradesh, India. Pestic. Sci., 50(3), 240-248.
Azwanida, N. N. (2015). A review on the extraction methods use in medicinal plants, principle, strength and limitation. Med.Aromat. Plants, 4(196), 2167-2182.
Bancroft, J. D. & Gamble, M. (Eds.). (2008). Theory and practice of histological techniques. Elsevier health sciences.
Caccia, S., Casartelli, M. &Tettamanti, G. (2019). The amazing complexity of insect midgut cells: types, peculiarities, and functions. Cell Tissue Res., 377(3), 505-525.
Chauhan, D. & Mishra, V. K. (2016). Effect of medicinal plant extracts on growth and development of tobacco caterpillar, Spodoptera litura (Fabricius). Int. J. Agric. Environ. Biotechnol., 9(3), 435.
Devanand, P.& Rani, P. U. (2008). Biological potency of certain plant extracts in management of two lepidopteran pests of Ricinus communis L. J. Biopestic., 1(2), 170-176.
Deshmukhe, P. V., Hooli, A. A. & Holihosur, S. N. (2010). Bioefficacy of cold ethyl alcohol extract of Annona squamosa against Spodoptera lituraFabricius. J. Biopestic., 3(1), 271-283.
Farder-Gomes, C. F., Saravanan, M., Martinez, L. C., Plata-Rueda, A., Zanuncio, J. C. & Serrao, J. E. (2022). Azadirachtin-based biopesticide affects the respiration and digestion in Anticarsiagemmatalis caterpillars. Toxin Rev., 41(2), 466-475.
Fiaz, M., Martínez, L. C., da Silva Costa, M., Cossolin, J. F. S., Plata-Rueda, A., Gonçalves, W. G., ... & Serrão, J. E. (2018). Squamocininduce histological and ultrastructural changes in the midgut cells of Anticarsiagemmatalis (Lepidoptera: Noctuidae). Ecotoxicol. Environ. Saf., 156, 1-8.
Franzetti, E., Casartelli, M., D'Antona, P., Montali, A., Romanelli, D., Cappellozza, S., ... &Tettamanti, G. (2016). Midgut epithelium in molting silkworm: a fine balance among cell growth, differentiation, and survival. Arthropod Struct.Dev ., 45(4), 368-379.
Hidalgo, J. R., Parellada, E. A., Bardón, A., Vera, N. &Neske, A. (2018). Insecticidal activity of Annonaceousacetogenins and their derivatives on Spodoptera frugiperda Smith (Lepidoptera: Noctuidae). J. Agric. Food Chem., 7(03), 105.
Jackson, A. D. & McLaughlin, J. (2009). Digestion and absorption. Surgery (oxford), 27(6), 231-236.
Jose,V., Raphel, L., Aiswariya, K. S. & Mathew, P. (2021). Green synthesis of silver nanoparticles using Annona squamosa L. seed extract: characterization, photocatalytic and biological activity assay. Bioprocess Biosyst. Eng., 44, 1819-1829.
Kamaraj, C., Bagavan, A., Elango, G., Zahir, A. A., Rajakumar, G., Marimuthu, S., ... &Rahuman, A. A. (2011). Larvicidal activity of medicinal plant extracts against Anopheles subpictus&Culextritaeniorhynchus. Indian J. Med. Res., 134(1), 101.
Khalil, H., Moussa, S., Zein, H. S., Ahmed, D. S., Shaurub, E. S. H. &Elarabi, N. I. (2021). Alterations in the expression of certain midgut genes of Spodoptera littoralis (Boisd.)(Lepidoptera: Noctuidae) larvae and midgut histopathology in response to Bacillus thuringiensis Cry1C toxin. Egypt J. Biol. Pest Control., 31(1), 1-9.
Leatemia, J. A.&Isman, M. B. (2004). Toxicity and antifeedant activity of crude seed extracts of Annona squamosa (Annonaceae) against lepidopteran pests and natural enemies. Int. J. Trop. Insect Sci., 24(2), 150-158.
Leatemia, J. A.&Isman, M. B. (2004). Insecticidal activity of crude seed extracts of Annona spp., Lansiumdomesticum andSandoricumkoetjape against lepidopteran larvae. Phytoparasitica, 32(1), 30-37.
Lin, C. Y., Wu, D. C., Yu, J. Z., Chen, B. H., Wang, C. L. & Ko, W. H. (2009). Control of silverleaf whitefly, cotton aphid and kanzawa spider mite with oil and extracts from seeds of sugar apple. Neotrop. Entomol., 38, 531-536.
Ling, R., Yang, R., Li, P., Zhang, X., Shen, T., Li, X., ... & Yan, J. (2019). Asatone and isoasatone A against Spodoptera litura fab. by acting on cytochrome P450 monoxygenases and glutathione transferases. Mol., 24(21), 39-40.
Mahmoud, M. A. & Hassan, A. N. T. (2022). Insecticidal Activity of seed extracts of Annona squamosa L., against the cotton leafworm Spodoptera littoralis (Boisd.). Egypt. J. Chem., 65(6), 1-2.
Mishra, M., Gupta, K. K., & Kumar, S. (2015). Impact of the stem extract of Thevetia neriifolia on the feeding potential and histological architecture of the midgut epithelial tissue of early fourth instars of HelicoverpaarmigeraHübner. Int. J. Insect Sci., 7, IJIS-S29127.
Mondal, P., Biswas, S., Pal, K. & Ray, D. P. (2018). Annona squamosa as a potential botanical insecticide for agricultural domains: a review. IJBS, 5(1), 81-89.
Nenotek, P. S., Londingkene, J. A., Ludji, R., Harini, T. S., Kapa, M. J., Nguru, E. S., ... &Konanin, M. (2022). The toxicity of Annona squamosa seeds and Anacardium occidentale seed shells from East Nusa Tenggara, Indonesia, against cabbage caterpillar (Crocidolomia pavonana). Intl. J. Trop. Drylands, 6(1).39-44.
Patil, J. R. (2009). Studies on isolation and characterization of bioactive compounds in lime [Citrus aurantifolia (Christm) swingle], their antioxidant and anticancer properties. J. Biochem. Res., 18, 1-10.
Pinto, L. M. N., DrebesDörr, N. C.&Fiuza, L. M. (2011). The toxicity and histopathology of Bacillus thuringiensis Cry1Ba toxin to Spodoptera frugiperda (Lepidoptera, Noctuidae). In Microorganisms In Industry And Environment: From Scientific and Industrial Research to Consumer Products, 137-140.
Prijono, D., Gani, M. S.&Syahputra, E. (1997). Insecticidal activity of annonaceous seed extracts against Crocidolomiabinotalis Zeller (Lepidoptera: Pyralidae).Bulletin of Plant Pests and Diseases, 9, 1-6.
Rajguru, M.& Sharma, A. N. (2012). Comparative efficacy of plant extracts alone and in combination with Bacillus thuringiensis sub sp. kurstaki against Spodoptera litura Fab. larvae. J. Biopestic., 5(1), 81.
Sahu, B., Pachori, R., Navya, R. N. & Patidar, S. (2020). Extent of damage by Spodoptera litura on cabbage.J. Entomol. Zool. Stud., 8, 1153-1156.
Senthil-Nathan, S., Choi, M. Y., Paik, C. H.&Kalaivani, K. (2008). The toxicity and physiological effect of goniothalamin, a styryl-pyrone, on the generalist herbivore, Spodoptera exiguaHübner. Chemosphere, 72(9), 1393-1400.
Sheehan, D.C. & Hrapchak, B.B. 1980. Theory and Practice of Histotechnology. 2nd ed. Mosby, St. Louis, MO. pp. 40-44.
Souto, A. L.,Sylvestre, M., Tölke, E. D., Tavares, J. F., Barbosa-Filho, J. M. & Cebrián-Torrejón, G. (2021). Plant-derived pesticides as an alternative to pest management and sustainable agricultural production: Prospects, applications and challenges. Mol., 26(16), 4835.
Sreeletha, C. & Geetha, P. R. (2012). Pesticidal effects of Annona squamosa L. on male Oryctesrhinoceros Linn.(Coleoptera: Scarabaeidae) in relation to reproduction. Curr. Biotic., 6, 8-21.
Suryani, A. I., Hariani, N., Majid, A. F. & Amalia, D. N. (2020). Histological changes in the midgut of Spodoptera litura larvae exposured by the extract of Mirabilis jalapa leaves, In IOP Conference Series: Earth and Environmental Science, 484: 1-9. IOP Publishing.
Takeda, M. 2012. Structures and functions of insect midgut: The regulatory mechanisms by peptides, proteins and related compounds, Hemolymph Proteins and Functional Peptides: Recent Advances in Insects and Other Arthropods, 1,94-110.
Urs, K. C. D. & B. V. Subramanya. (1974). A simplified semi-synthetic diet for rearing Spodopteralitura (Fab.) in the laboratory,Curr. Res.3,40-41.
Vetal, D. S. & Pardeshi, A. B. (2019). Insecticidal potential of ethanol and hexane solvent seed extract of Annona squamosa against Spodoptera litura Fab.,J. Pharmacogn. Phytochem., 8(3), 842-845.
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Insecticidal activity and changes in midgut histology of the generalist herbivore, Spodoptera litura F. (Lepidoptera: Noctuidae) in response to seed extract of Annona squamosa Linn. (2023). Journal of Applied and Natural Science, 15(1), 401-407. https://doi.org/10.31018/jans.v15i1.4371
