Azadirachtin-induced effects on various life history traits and cellular immune reactions of <i>Galleria mellonella</i> (Lepidoptera: Pyralidae)

Authors

  • Aylin Er Balikesir University, Faculty of Science and Literature
  • Deniz Taşkıran Balikesir University, Faculty of Science and Literature
  • Olga Sak Balikesir University, Faculty of Science and Literature

Keywords:

Galleria mellonella, azadirachtin, fecundity, hemocyte count, nodule

Abstract

The effects of the botanical insecticide azadirachtin were examined on the life history traits, fecundity and immune parameters of Galleria mellonella L. (Lepidoptera: Pyralidae). We determined that for the topical application of azadirachtin, the LC50 was 16.564 ppm; at 100 ppm the adult emergence time was prolonged, however the longevity of adults remained unchanged above sublethal concentrations. The mean number of healthy eggs and the fecundity of adults decreased, whereas the number of defective eggs increased with azadirachtin treatment. At concentrations >50 ppm female G. mellonella adults laid no eggs. Azadirachtin reduced total hemocyte counts at 24 and 48 h posttreatment, however the alterations in differential hemocyte counts were only significant at 100 ppm. Laminarin-induced nodulation response and the spreading ability of hemocytes were also suppressed with azadirachtin treatment. Our results suggest that azadirachtin, as a good candidate for integrated pest control, has the capability to affect the biological parameters and cellular immunity of the model insect G. mellonella.

https://doi.org/10.2298/ABS160421108E

Received: April 21, 2016; Revised: May 27, 2016; Accepted: June 22, 2016; Published online: November 3, 2016

How to cite this article: Er A, Taşkıran D, Sak O. Azadirachtin-induced effects on various life history traits and cellular immune reactions of Galleria mellonella (Lepidoptera: Pyralidae). Arch Biol Sci. 2017;69(2):335-44.

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Author Biographies

Aylin Er, Balikesir University, Faculty of Science and Literature

Department of Biology

Deniz Taşkıran, Balikesir University, Faculty of Science and Literature

Department of Biology

Olga Sak, Balikesir University, Faculty of Science and Literature

Department of Biology

References

Mordue (Luntz) AJ, Blackwell A. Azadirachtin: an update. J Insect Physiol. 1993;39:903-24.

Rong XD, Xu HH, Chiu SF. Progressing on botanical insecticide-neem research. Chin J Pestic Sci. 2000;2:9-14.

Reed E, Majumdar SK. Differential cytotoxic effects of azadirachtin on Spodoptera frugiperda and mouse cultured cells. Entomol Exp Appl. 1998;89:215-21.

Salehzadeh A, Jabbar A, Jennens L, Ley SV, Annadurai RS, Adams R, Strang RHC. The effects of phytochemical pesticides on the growth of cultured invertebrate and vertebrate cells. Pest Manag Sci. 2002;58:268-76.

Huang XY, Li OW, Xu HH. Induction of programmed death and cytoskeletal damage on Trichoplusia ni BTI-Tn-5B1-4 cells by azadirachtin. Pestic Biochem Phys. 2010;98:289-95.

Tanzubil PB, McCaffery AR. Effects of azadirachtin and aqueous neem seed extracts on survival, growth and development of the African armyworm, Spodoptera exempta. Crop Prot. 1990;9:383-6.

Liang GM, Chen W, Liu TX. Effects of three neem-based insecticides on diamondback moth (Lepidoptera: Plutellidae). Crop Prot. 2003;22:333-40.

Singh S. Effects of aqueous extract of neem seed kernel and azadirachtin on the fecundity, fertility and post-embryonic development of the melonfly, Bactrocera cucurbitae and the oriental fruit fly, Bactrocera dorsalis (Diptera: Tephritidae). J Appl Entomol. 2003;127:540-7.

Bruce YA, Gounou S, Olaye AC, Smith H, Schulthess F. The effects of neem (Azadirachta indica A. Juss) oil on oviposition, development and reproductive potentials of Sesamia calamistis Hampson (Lepidoptera: Noctuidae) and Eldana saccharina Walker (Lepidoptera: Pyralidae). Agr Forest Entomol. 2004;6:223-32.

Mordue (Luntz) AJ, Morgan ED, Nisbet AJ. Azadirachtin, a natural product in insect control. In: Gilbert LI, Gill SS, editors. Insect Control. London: Academic Press; 2010. p. 185-203.

Lynn OM, Kim JE, Lee KY. Effects of azadirachtin on the development and gene expression of fifth instar larvae of Indian meal moth, Plodia interpunctella. J Asia Pac Entomol. 2012;15:101-5.

Salehzadeh A, Akhkha A, Cushley W, Adams RL, Kusel JR, Strang RH. The antimitotic effect of the neem terpenoid azadirachtin on cultured insect cells. Insect Biochem Molec. 2003;33:681-9.

Huang JF, Shui KJ, Li HY, Hu MY, Zhong GH. Antiproliferative effect of azadirachtin A on Spodoptera litura Sl-1 cell line through cell cycle arrest and apoptosis induced by up-regulation of p53. Pestic Biochem Phys. 2011;99:16-24.

Shu B, Wang W, Hu Q, Huang J, Hu M, Zhong G. A comprehensive study on apoptosis induction by azadirachtin in Spodoptera frugiperda cultured cell line Sf9. Arch Insect Biochem. 2015;89:153-68.

Lavine MD, Strand MR. Insect hemocytes and their role in immunity. Insect Biochem Molec. 2002;32:1295-309.

Zibaee A, Bandani AR, Malagoli D. Methoxyfenozide and pyriproxifen alter the cellular immune reactions of Eurygaster integriceps Puton (Hemiptera: Scutelleridae) against Beauveria bassiana. Pestic Biochem Phys. 2012;102:30-7.

Zibaee A, Bandani AR. Effects of Artemisia annua L. (Asteracea) on the digestive enzymatic profiles and the cellular immune reactions of the Sunn pest, Eurygaster integriceps (Heteroptera: Scutellaridae), against Beauveria bassiana. Bull Entomol Res. 2010;100:185-96.

James RR, Xub J. Mechanisms by which pesticides affect insect immunity. J Invertebr Pathol. 2012;109:175-82.

Koodalingam A, Mullainadhan P, Arumugam M. Immuno-suppressive effects of aqueous extract of soapnut Sapindus emarginatus on the larvae and pupae of vector mosquito, Aedes aegypti. Acta Trop. 2013;126:249-55.

Azambuja P, Garcia ES, Ratcliffe NA, Warthen JD Jr. Immune-depression in Rhodnius prolixus induced by the growth inhibitor, azadirachtin. J Insect Physiol. 1991;37:771-7.

Figueiredo MB, Castro DP, Nogueira NFS, Garcia ES, Azambuja P. Cellular immune response in Rhodnius prolixus: Role of ecdysone in hemocyte phagocytosis. J Insect Physiol. 2006;52:711-6.

Sharma PR, Sharma OP, Saxena BP. Effect of Neem gold on hemocytes of the tobacco armyworm, Spodoptera litura (Fabricius) (Lepidoptera|: Noctuidae). Curr Sci India. 2003;84:690-5.

Shaurub EH, Abd El-Meguid A, Abd El-Aziz, NM. Quantitative and ultrastructural changes in the haemocytes of Spodoptera littoralis (Boisd.) treated individually or in combination with Spodoptera littoralis multicapsid nucleopolyhedrovirus (SpliMNPV) and azadirachtin. Micron. 2014;65:62-8.

Büyükgüzel E, Büyükgüzel K, Erdem M. The influence of dietary solanine on the wax moth Galleria mellonella L. Arch Insect Biochem Physiol. 2013;83:15-24.

Dere B, Altuntaş H, Nurullahoğlu, ZU. Insecticidal and oxidative effects of azadirahtin on the model organism Galleria mellonella L. (Lepidoptera: Pyralidae). Arch Insect Biochem. 2015;89:138-52.

Er A, Keskin M. Influence of abscisic acid on the biology and hemocytes of the model insect Galleria mellonella (Lepidoptera: Pyralidae). Ann Entomol Soc Am. 2016;109:244-51.

Finney DJ. Probit analysis. New York: Cambridge University Press; 1971. 333 p.

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

Malczewska M, Gelman DB, Cymborowski B. Effect of azadirachtin on development, juvenile hormone and ecdysteroid titres in chilled Galleria mellonella larvae. J Insect Physiol. 1988;34:725-32.

Gelbič I, Němec V. Developmental changes caused by metyrapone and azadirachtin in Spodoptera littoralis (Boisd.) (Lep., Noctuidae) and Galleria mellonella (L.) (Lep., Pyralidae). J Appl Entomol. 2001;125:417-22.

Charbonneau C, Côté R, Charpentier G. Effects of azadirachtin and of simpler epoxy-alcohols on survival and behaviour of Galleria mellonella (Lepidoptera). J Appl Entomol. 2007;131:447-52.

Izhar-ul-Haq M, Saleem M, Ahmed S. Effect of neem (Azadirachta indica A. Juss) seed extracts against greater wax moth (Galleria mellonella L.) larvae. Pak Entomol. 2008;30:137-40.

Jagannadh V, Nair VSK. Azadirachtin-induced effects on larval-pupal transformation of Spodoptera mauritra. Physiol Entomol. 1992;17:56-61.

Adel MM, Sehnal F. Azadirachtin potentiates the action of ecdysteroid agonist RH-2485 in Spodoptera littoralis. J Insect Physiol. 2000;46:267-74.

Tunca H, Kılınçer N, Özkan C. Side-effects of some botanical insecticides and extracts on the parasitoid, Venturia canescens (Grav.) (Hymenoptera: Ichneumonidae). Türk Entomol Derg. 2012;36:205-14.

Akthar Y, Isman MB, Niehaus LA, Lee CH, Lee HS. Antifeedant and toxic effects of naturally occurring and synthetic quinones to the cabbage looper, Trichoplusia ni. Crop Prot. 2012;31:8-14.

Kefford BJ, Zalizniak L, Warne MSJ, Nugegoda D. Is the integration of hormesis and essentiality into ecotoxicology now opening Pandora’s box? Environ Pollut. 2008;151:516-23.

Mukherjee SN, Rawal SK, Ghumare SS, Sharma RN. Hormetic concentrations of azadirachtin and isoesterase profiles in Tribolium castaneum (Herbst) (Coleoptera: Tenebrionidae). Experientia. 1993;49:557-60.

Yu Y, Shen G, Zhu H, Lu Y. Imidacloprid induced hormesis on the fecundity and juvenile hormone levels of the green peach aphid Myzus persicae (Sulzer). Pestic Biochem Phys. 2010;98:238-42.

Vilca Malqui KS, Vieira JL, Guedes RNC, Gontijo LM. Azadirachtin-induced hormesis mediating shift in fecundity-longevity trade-off in the Mexican bean weevil (Chrysomelidae: Bruchinae). J Econ Entomol. 2014;107:860-6.

Okumu FO, Knols BGJ, Fillinger U. Larvicidal effects of a neem (Azadirachta indica) oil formulation on the malaria vector Anopheles gambiae. Malar J. 2007;6:63-70.

Silva MA, Bezerra-Silva GCD, Vendramim JD, Mastrangelo T. Sublethal effect of neem extact on mediterranean fruit fly adults. Rev Bras Frutic. 2013;35:93-101.

Gontijo LM, Celestino D, Queiroz OS, Guedes RNC, Picanço M. Impacts of azadirachtin and chlorantraniliprole on the developmental stages of pirate bug predators (Hemiptera: Anthocoridae) of the tomato pinworm Tuta absoluta (Lepidoptera: Gelechiidae). Fla Entomol. 2015;98:59-64.

Feder D, Valle D, Rembold H, Garcia ES. Azadirachtin-induced sterilization in mature females of Rhodnius prolixus. Z Naturforsch C. 1988;43:908-13.

Büyükgüzel K. Malathion-induced oxidative stress in a parasitoid wasp: effect on adult emergence, longevity, fecundity, and oxidative and antioxidative response of Pimpla turionellae (Hymenoptera: Ichneumonidae). J Econ Entomol. 2006;99:1225-34.

Tiwari RK, Pandey JP, Kumar D. Effect of neem based insecticides on metamorphosis, haemocyte count and reproductive behaviour in red cotton bug, Dysdercus koenigii (Heteroptera: Pyrrhocoridae). Entomon. 2006;31:267-75.

Pandey JP, Tiwari RK, Kumar D. Reduction in haemocyte mediated immune response in Danaus chrysippus following treatment with Neem based insecticides. J Entomol Sci. 2008;5:200-6.

Gardiner EMM, Strand MR. Hematopoiesis in larval Pseudoplusia includens and Spodoptera frugiperda. Arch Insect Biochem. 2000;43:147-64.

Er A, Uçkan F, Rivers DB, Ergin E, Sak O. Effects of parasitization and envenomation by the endoparasitic wasp Pimpla turionellae (Hymenoptera: Ichneumonidae) on hemocyte numbers, morphology, and viability of its host Galleria mellonella (Lepidoptera: Pyralidae). Ann Entomol Soc Am. 2010;103:273-82.

Lai D, Jin X, Wang H, Yuan M, Xu H. Gene expression profile change and growth inhibition in Drosophila larvae treated with azadirachtin. J Biotechnol. 2014;185:51-6.

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Published

2017-05-25

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Er A, Taşkıran D, Sak O. Azadirachtin-induced effects on various life history traits and cellular immune reactions of &lt;i&gt;Galleria mellonella&lt;/i&gt; (Lepidoptera: Pyralidae). Arch Biol Sci [Internet]. 2017May25 [cited 2024Apr.24];69(2):335-44. Available from: https://www.serbiosoc.org.rs/arch/index.php/abs/article/view/481

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