Skip to main content
Log in

Pest and natural enemy: how the fat bodies of both the southern armyworm Spodoptera eridania and the predator Ceraeochrysa claveri react to azadirachtin exposure

  • Original Article
  • Published:
Protoplasma Aims and scope Submit manuscript

Abstract

The effects of biopesticides on insects can be demonstrated by morphological and ultrastructural tools in ecotoxicological analysis. Azadirachtin-based products are widely used as biopesticides, affecting numerous insect populations. Through morphological biomarkers, this study aimed to characterize the fat bodies of both the southern armyworm Spodoptera eridania and the predator Ceraeochrysa claveri after chronic exposure to azadirachtin. Larvae of S. eridania and C. claveri were fed with fresh purple lettuce leaves (Lactuca sativa) and egg clusters of Diatraea saccharalis treated with azadirachtin solution of 6 mg active ingredient (a.i.)/L and 18 mg a.i./L for 7 days, respectively. The biological data showed a significant reduction in survival and body mass in S. eridania and cytotoxic effects in the parietal and perivisceral fat bodies in both species. Ultrastructural cell damage was observed in the trophocytes of both species such as dilated cisternae of the rough endoplasmic reticulum and swollen mitochondria. Trophocytes of S. eridania and C. claveri of the parietal and perivisceral layers responded to those injuries by different cytoprotective and detoxification means such as an increase in the amount of cytoplasmic granules containing calcium, expression of heat shock protein (HSP)70/HSP90, and development of the smooth endoplasmic reticulum. Despite all the different means of cytoprotection and detoxification, they were not sufficient to recover from all the cellular damages. Azadirachtin exhibited an excellent performance for the control of S. eridania and a moderate selectivity for the predator C. claveri, which presents better biological and cytoprotective responses to chronic exposure to azadirachtin.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Adamski Z (2007) Exposure to cabaryl leads to ultrastructural changes and alters activity of antioxidant enzymes in Spodoptera exigua (Lepidoptera: Noctuidae). Invert Biol 126(2):191–201

    Article  Google Scholar 

  • Adamski Z, Banaszkiewicz M, Ziemnicki K (2005) Ultrastructural alterations induced by fenitrothion on fat body cells and midgut cells of Tenebrio molitor L. (Insecta, Coleoptera) larvae. J Biol Res 3:15–22

    CAS  Google Scholar 

  • Adamski A, Radtke K, Kopiczko A, Chowanski S, Marciniak P, Szymczak M, Spochacz M, Falabella P, Lelario F, Scrano L, Bufo SA (2016) Ultrastructural and developmental toxicity of potato and tomato leaf extracts to beet armyworm, Spodoptera exigua (Lepidoptera: Noctuidae). Microsc Res Tech 79:948–958. https://doi.org/10.1002/jemt.22726

    Article  PubMed  Google Scholar 

  • Aggarwal N, Brar DS (2006) Effects of different neem preparations in comparison to synthetic insecticides on the whitefly parasitoid Encarsia sophia (Hymenoptera: Aphelinidae) and the predator Chrysoperla carnea (Neuroptera: Chrysopidae) on cotton under laboratory conditions. J Pest Sci 79:201–207. https://doi.org/10.1007/s10340-006-0134-9

    Article  Google Scholar 

  • Ahmad M, Oβiewatsch HR, Basedow T (2003) Effects of neem-treated aphids as food/hosts on their predators and parasitoids. J Appl Entomol 127:458–464

    Article  CAS  Google Scholar 

  • Alves SN, Serrão JE, Melo AL (2010) Alterations in the fat body and midgut of Culex quinquefasciatus following exposure to different insecticides. Micron 41:592–597. https://doi.org/10.1016/j.micron.2010.04.004

    Article  CAS  PubMed  Google Scholar 

  • Amirmohammadi F, Sendi JJ, Zibaee A (2012) Toxicity and physiological effect of essential oil of Artemisia annua (Labiatae) on Agriolimax agrestis L. (Stylommatophora: Limacidae). J Plant Prot Res 52(2):185–189

    Article  Google Scholar 

  • Arrese EL, Soulages JL (2010) Insect fat body: energy, metabolism, and regulation. Annu Rev Entomol 55:207–225. https://doi.org/10.1146/annurev-ento-112408-085356

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bierkens JGEA (2000) Applications and pitfalls of stress-proteins in biomonitoring. Toxicology 153:61–72

    Article  CAS  PubMed  Google Scholar 

  • Buckner JS, Henderson TA, Ehresmann DD, Graf G (1990) Structure and composition of urate storage granules from the fat body of Manduca sexta. Insect Biochem 20(2):203–214

    Article  CAS  Google Scholar 

  • Büyükgüzel E, Büyükgüzel K, Snela M, Erdem M, Radtke K, Ziemnicki K, Adamski Z (2013) Effect of boric acid on antioxidant enzyme activity, lipid peroxidation, and ultrastructure of midgut and fat body of Galleria mellonela. Cell Biol Toxicol 29:117–129. https://doi.org/10.1007/s10565-013-9240-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Campos EVR, Oliveira JL, Pascoli M, Lima R, Fraceto LF (2016) Neem oil and crop protection: from now to the future. Front Plant Sci 7:1494. https://doi.org/10.3389/fpls.2016.01494

    Article  PubMed  PubMed Central  Google Scholar 

  • Carvalho RBR, Andrade FG, Levy SM, Moscardi F, Falleiros AMF (2013) Histology and ultrastructure of the fat body of Anticarsia gemmatalis (Hübner, 1818) (Lepidoptera: Noctuidae). Braz Arch Biol Technol 56(2):303–310

    Article  Google Scholar 

  • Catae AF, Roat TC, Oliveira RA, Nocelli RCF, Malaspina O (2014) Cytotoxic effects of thiamethoxan in the midgut and malpighian tubules of africanized Apis mellifera (Hymenoptera: Apidae). Microsc Res Tech 77:274–281. https://doi.org/10.1002/jemt.22339

    Article  CAS  PubMed  Google Scholar 

  • Cerella C, Diederich M, Ghibelli L (2010) The dual role of calcium as messenger and stressor in cell damage, death, and survival. Int J Cell Biol 2010:546163–546114. https://doi.org/10.1155/2010/546163

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheville NF (1994) Ultrastructural pathology: an introduction to interpretation. Iowa State University Press

  • Cheville NF (2009) Ultrastructural pathology: the comparative cellular basis of disease. Wiley-Blackwell

  • Chowanski S, Lubawy J, Paluch-Lubawa E, Spochacz M, Rosinski G, Stocinska M (2017) The physiological role of fat body and muscle tissues in response to cold stress in the tropical cockroach Gromphadorhina coquereliana. PloSOne 12(3):e0173100. https://doi.org/10.1371/journal.pone.0173100

    Article  CAS  Google Scholar 

  • Cloyd RA (2012) Indirect effects of pesticides on natural enemies. In: Soundararajan RP (ed) Pesticides-advances in chemical and botanical pesticides. Intech, Rijeka, pp 127–150. https://doi.org/10.5772/47244

    Chapter  Google Scholar 

  • Cordeiro EMG, Corrêa AS, Venzon M, Guedes RNC (2010) Insecticide survival and behavioral avoidance in the lacewings Chrysoperla externa and Ceraeochrysa cubana. Chemosphere 81:1352–1357. https://doi.org/10.1016/j.chemosphere.2010.08.021

    Article  CAS  PubMed  Google Scholar 

  • Cunha FM, Wanderley-Teixeira V, Teixeira AAC, Alves LC (2016) Ultrastructure and histochemistry of the fat body of Anthonomus grandis (Coleoptera: Curculionidae). Invert Reprod Devel. https://doi.org/10.1080/07924259.2016.1162855

  • De Freitas S, Penny ND (2001) The green lacewings (Neuroptera: Chrysopidae) of Brazilian agro-ecossystems. Proc Calif Acad Sci 52(19):245–395

    Google Scholar 

  • Domingues CEC, Abdalla FC, Balsamo PJ, Pereira BVR, Hausen MA, Costa MJ, Silva-Zacarin ECM (2017) Thiamethoxam and picoxystrobin reduce the survival and overload the hepato-nephrocitic system of the Africanized honeybee. Chemosphere 186:994–1005. https://doi.org/10.1016/j.chemosphere.2017.07.133

    Article  CAS  PubMed  Google Scholar 

  • Feder ME, Hofmann GE (1999) Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol 61:243–282

    Article  CAS  Google Scholar 

  • Ferreira RAC, Silva Zacarin ECM, Malaspina O, Bueno OC, Tomotake MEM, Pereira AM (2013) Cellular responses in the Malpighian tubules of Scaptotrigona postica (Latreille, 1807) exposed to low doses of fipronil and boric acid. Micron 46:57–65. https://doi.org/10.1016/j.micron.2012.12.008

    Article  CAS  PubMed  Google Scholar 

  • Fontanetti CS, Nogarol LR, Souza RB, Perez DG, Mazivieiro GT (2011) Bioindicators and biomarkers in the assessment of soil toxicity. In: Pascucci S (ed) Soil contamination. Intech, pp 143–168. https://doi.org/10.5772/25042

  • Garcia ASG, Scudeler EL, Pinheiro PFF, Santos DC (2018) Can exposure to neem oil affect the spermatogenesis of predator Ceraeochrysa claveri? Protoplasma. https://doi.org/10.1007/s00709-018-1329-7

  • Goodman LA (1964) Simultaneous confidence intervals for contrasts among multinomial populations. Ann Math Stat 35(2):716–725

    Article  Google Scholar 

  • Goodman LA (1965) On simultaneous confidence intervals for multinomial proportions. Technometrics 7(2):247–254

    Article  Google Scholar 

  • Haunerland NH, Shirk PD (1995) Regional and functional differentiation in the insect fat body. Annu Rev Entomol 40:121–145

    Article  CAS  Google Scholar 

  • Hoyer-Hansen M, Bastholm L, Szyniarowski P, Campanella M, Szabadkai G, Farkas T, Bianchi K, Fehrenbacher N, Elling F, Rizzuto R, Mathiasen IS, Jäättelä M (2007) Control of macroautophagy by calcium, calmodulin-dependent kinase kinase-β, and Bcl-2. Mol Cell 25:193–205. https://doi.org/10.1016/j.molcel.2006.12.009

    Article  CAS  PubMed  Google Scholar 

  • Johnson RA, Wichern DW (2007) Applied multivariate statistical analysis. Prentice Hall, Upper Saddle River

    Google Scholar 

  • Junqueira LCU, Junqueira LMMS (1983) Técnicas básicas de citologia e histologia. Livraria Editora Santos, São Paulo

    Google Scholar 

  • Lanneau D, Brunet M, Frisan E, Solary E, Fontenay M, Garrido C (2008) Heat shock proteins: essential proteins for apoptosis regulation. J Cell Mol Med 12(3):743–761

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lima de Souza JR, Remedio RN, Arnosti A, Abreu RMM, Camargo-Mathias MI (2017) The effects of neem oil (Azadirachta indica A. JUSS) enriched with different concentrations of azadirachtin on the integument of semi-engorged Rhipicephalus sanguineus sensu lato (Acari: Ixodidae) females. Microsc Res Tech 80:838–844. https://doi.org/10.1002/jemt.22871

    Article  CAS  PubMed  Google Scholar 

  • Lin T, Liu Q, Chen J (2016) Identification of differentially expressed genes in Monochamus alternatus digested with azadirachtin. Sci Rep 6:33484. https://doi.org/10.1038/srep33484

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lycett GJ, McLaughlin LA, Ranson H, Hemingway J, Kafatos FC, Loukeris TG, Paine MJI (2006) Anopheles gambiae P450 reductase is highly expressed in oenocytes and in vivo knockdown increases permethrin susceptibility. Insect Mol Biol 15(3):321–327

    Article  CAS  PubMed  Google Scholar 

  • Malaspina O, Silva-Zacarin ECM (2006) Cell markers for ecotoxicological studies in target organs of bees. Braz J Morphol Sci 23:303–309

    Google Scholar 

  • MAPA (Ministério da Agricultura, Pecuária e Abastecimento) (2018) Agrofit. Coordenação Geral de Agrotóxicos e Afins/DFIA/DAS, Brasília, DF, Brazil. http://extranet.agricultura.gov.br/agrofit_cons/principal_agrofit_cons. Accessed 2 July 2018

  • Martins GF, Ramalho-Ortigão JM (2012) Oenocytes in insects. Invert Surv J 9:139–152

    Google Scholar 

  • Martins GF, Serrão JE, Ramalho-Ortigão JM, Pimenta PFP (2011) Histochemical and ultrastructural studies of the mosquito Aedes aegypti fat body: effects of aging and diet type. Microsc Res Tech 74:1032–1039. https://doi.org/10.1002/jemt.20990

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Medina P, Smagghe G, Budia F, Tirry L, Viñuela E (2003) Toxicity and absorption of azadirachtin, diflubenzuron, pyriproxyfen, and tebufenozide after topical application in predatory larvae of Chrysoperla carnea (Neuroptera: Chrysopidae). Environ Entomol 32:196–203

    Article  CAS  Google Scholar 

  • Montezano DG, Specht A, Sosa-Gómez DR, Roque-Specht VF, Barros NM (2014) Immature stages of Spodoptera eridania (Lepidoptera: Nocutidae): developmental parameters and host plants. J Insect Sci 14(238). https://doi.org/10.1093/jisesa/ieu100

  • Mordue (Luntz) AJ, Nisbet AJ (2000) Azadirachtin from the neem tree Azadirachta indica: its action against insects. An Soc Entomol Bras 29:615–632

    Article  Google Scholar 

  • Mordue (Luntz) AJ, MSJ S, Ley SV, Blaney WM, Mordue W, Nasiruddin M, Nisbet AJ (1998) Actions of azadirachtin, a plant allelochemical, against insects. Pestic Sci 54:277–284

    Article  Google Scholar 

  • Morgan ED (2009) Azadirachtin, a scientific gold mine. Bioorg Med Chem 17:4096–4105. https://doi.org/10.1016/j.bmc.2008.11.081

    Article  CAS  PubMed  Google Scholar 

  • Nasiruddin M, Mordue (Luntz) AJ (1993) The effect of azadirachtin on the midgut histology of the locusts Schistocerca gregaria and Locusta migratoria. Tissue Cell 25(6):875–884

    Article  CAS  PubMed  Google Scholar 

  • Nogarol LR, Fontanetti CS (2010) Acute and subchronic exposure of diplopods to substrate containing sewage mud: tissular responses of the midgut. Micron 41:239–246. https://doi.org/10.1016/j.micron.2009.10.009

    Article  CAS  PubMed  Google Scholar 

  • Paes de Oliveira VT, Cruz-Landim C (2003) Morphology and function of insect fat body cells: a review. Biociências 11(2):195–205

    Google Scholar 

  • Pappas ML, Broufas GD, Koveos DS (2011) Chrysopid predators and their role in biological control. J Entomol 8(3):301–326

    Article  Google Scholar 

  • Park MS, Park P, Takeda M (2013) Roles of fat body trophocytes, mycetocytes and urocytes in the American cockroach, Periplaneta Americana under starvation conditions: an ultrastructural study. Arthropod Struct Dev 42:287–295. https://doi.org/10.1016/j.asd.2013.03.004

    Article  CAS  PubMed  Google Scholar 

  • Pearse AGE (1972) Histochemistry: theoretical and applied. Churchill Livingtsone, Edinburgh

    Google Scholar 

  • Pino RM, Pino LC, Bankston PW (1981) The relationships between the Golgi apparatus, GERL, and lysosomes of fetal rat liver kupffer cells examined by ultrastructural phosphatase cytochemistry. J Histochem Cytochem 29:1061–1070

    Article  CAS  Google Scholar 

  • Poiani SB, Cruz-Landim C (2012) Storaged products and presence of acid phosphatase in fat body cells at pre-pupal worker stage of Apis mellifera Linnaeus, 1758 (Hymenoptera, Apidae). Micron 43:475–478. https://doi.org/10.1016/j.micron.2011.11.006

    Article  CAS  PubMed  Google Scholar 

  • Reinecke M, Walther C (1978) Aspects of turnover and biogenesis of synaptic vesicles at locust neuromuscular junctions as revealed by zinc iodide-osmium tetroxide (ZIO) reacting with intravesicular SH-groups. J Cell Biol 78:839–855

    Article  CAS  PubMed  Google Scholar 

  • Remedio RN, Nunes PH, Anholeto LA, Oliveira PR, Sá ICG, Camargo-Mathias MI (2016) Morphological alterations in salivary glands of Rhipicephalus sanguineus ticks (Acari: Ixodidae) exposed to neem oil with known azadirachtin concentration. Micron 83:19–31. https://doi.org/10.1016/j.micron.2016.01.004

    Article  CAS  PubMed  Google Scholar 

  • Roel AR, Dourado DM, Matias R, Porto KRA, Bednaski AV, Costa RB (2010) The effect of sub-lethal doses of Azadirachta indica (Meliaceae) oil on the midgut of Spodoptera frugiperda (Lepidoptera: Noctuidae). Rev Bras Entomol 54:505–510

    Article  Google Scholar 

  • Roma GC, Bueno OC, Camargo-Mathias MI (2010) Morpho-physiological analysis of insect fat body: a review. Micron 41:395–401

    Article  CAS  PubMed  Google Scholar 

  • Santos KB, Meneguim AM, Neves PMOJ (2005) Biologia de Spodoptera eridania (Cramer) (Lepidoptera: Noctuidae) em diferentes hospedeiros. Neotrop Entomol 34(6):903–910

    Article  Google Scholar 

  • Schmutterer H (1990) Properties and potential of natural pesticides from the neem tree, Azadirachta indica. Annu Rev Entomol 35:271–297

    Article  CAS  PubMed  Google Scholar 

  • Scudeler EL, Santos DC (2013) Effects of neem oil (Azadirachta indica A. Juss) on midgut cells of predatory larvae Ceraeochrysa claveri (Navás, 1911) (Neuroptera: Chrysopidae). Micron 44:125–132. https://doi.org/10.1016/j.micron.2012.05.009

    Article  CAS  PubMed  Google Scholar 

  • Scudeler EL, Garcia ASG, Padovani CR, Santos DC (2013) Action of neem oil (Azadirachta indica A. Juss) on cocoon spinning in Ceraeochrysa claveri (Neuroptera: Chrysopidae). Ecotoxicol Environ Saf 97:176–182. https://doi.org/10.1016/j.ecoenv.2013.08.008

    Article  CAS  PubMed  Google Scholar 

  • Scudeler EL, Padovani CR, Santos DC (2014) Effects of neem oil (Azadirachta indica A. Juss) on the replacement of the midgut epithelium in the lacewing Ceraeochrysa claveri during larval-pupal metamorphosis. Acta Histochem 116:771–780. https://doi.org/10.1016/j.acthis.2014.01.008

    Article  CAS  PubMed  Google Scholar 

  • Scudeler EL, Garcia ASG, Padovani CR, Pinheiro PFF, Santos DC (2016a) Cytotoxic effects of neem oil in the midgut of the predator Ceraeochrysa claveri. Micron 80:96–111. https://doi.org/10.1016/j.micron.2015.10.005

    Article  CAS  PubMed  Google Scholar 

  • Scudeler EL, Garcia ASG, Padovani CR, Pinheiro PFF, Santos DC (2016b) Are the biopesticide neem oil and the predator Ceraeochrysa claveri (Navás, 1911) compatible? J Entomol Zool Stud 4(2):340–346

    Google Scholar 

  • Shannag HK, Capinera JL, Freihat NM (2015) Effects of neem-based insecticides on consumption and utilization of food in larvae of Spodoptera eridania (Lepidoptera: Noctuidae). J Insect Sci 15(1):152. https://doi.org/10.1093/jisesa/iev134

    Article  CAS  Google Scholar 

  • Shu Y, Du Y, Wang J (2011) Molecular characterization and expression patterns of Spodoptera litura heat shock protein 70/90, and their response to zinc stress. Comp Biochem Physiol 158:102–110. https://doi.org/10.1016/j.cbpa.2010.09.006

    Article  CAS  Google Scholar 

  • Silva-Zacarin ECM, Gregorc A, Moraes RLMS (2006) In situ localization of heat-shock proteins and cell death labelling in the salivary gland of acaricide-treated honeybee larvae. Apidologie 37:507–516. https://doi.org/10.1051/apido:2006030

    Article  CAS  Google Scholar 

  • Souza TS, Fontanetti CS (2011) Morphological biomarkers in the Rhinocricus padbergi midgut exposed to contaminated soil. Ecotoxicol Environ Saf 74:10–18

    Article  CAS  Google Scholar 

  • Specht A, Montezano DG, Sosa-Gómez DR, Paula-Moraes SV, Roque-Specht VF, Barros NM (2016) Reproductive potential of Spodoptera eridania (Stoll) (Lepidoptera: Noctuidae) in the laboratory: effect of multiple couples and the size. Braz J Biol 76(2):526–530. https://doi.org/10.1590/1519-6984.23114

    Article  CAS  PubMed  Google Scholar 

  • Tong Y, Song F (2015) Intracellular calcium signaling regulates autophagy via calcineurin-mediated TFEB dephosphorylation. Autophagy 11(7):1192–1195. https://doi.org/10.1080/15548627.2015.1054594

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Valizadeh B, Sendi JJ, Zibaee A, Oftadeh M (2013) Effect of neem based insecticide Achook® on mortality, biological and biochemical parameters of elm leaf beetle Xanthogaleruca luteola (Col: Chrysomelidae). J Crop Prot 2(3):319–330

    Google Scholar 

  • Wang X, Chen M, Zhou J, Zhang X (2014) HSP27, 70 and 90, anti-apoptotic proteins, in clinical cancer therapy (review). Int J Oncol 45:18–30. https://doi.org/10.3892/ijo.2014.2399

    Article  CAS  PubMed  Google Scholar 

  • Zar JH (2009) Biostatistical analysis. Prentice Hall, Upper Saddle River

    Google Scholar 

Download references

Acknowledgments

We are grateful to the Electron Microscopy Center of the Institute of Biosciences of Botucatu, UNESP.

Funding

This study was supported and funded by the São Paulo Research Foundation (Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP)) (2014/15016-2).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Daniela Carvalho dos Santos.

Ethics declarations

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Handling Editor: Reimer Stick

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Scudeler, E.L., Garcia, A.S.G., Padovani, C.R. et al. Pest and natural enemy: how the fat bodies of both the southern armyworm Spodoptera eridania and the predator Ceraeochrysa claveri react to azadirachtin exposure. Protoplasma 256, 839–856 (2019). https://doi.org/10.1007/s00709-019-01347-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-019-01347-5

Keywords

Navigation