Advertisement

Effect of azadirachtin on mortality and immune response of leaf-cutting ants

  • Karina D. AmaralEmail author
  • Lailla C. Gandra
  • Marco Antonio de Oliveira
  • Danival J. de Souza
  • Terezinha M. C. Della Lucia
Article

Abstract

Leaf-cutting ants are difficult pests to control because they have numerous defense strategies and are highly selective in their plant harvesting choices. The search for effective pest control methods that have minimal negative effects on the environment has been continuous. Azadirachtin, a compound extracted from the neem tree (Azadirachta indica), is a promising alternative for the control of various pests, as it is toxic to some insects but readily degrades in the environment. In this study, we evaluated the effects of azadirachtin on the mortality, through topical exposure to the compound, and immune response, by introducing an artificial antigen into leaf-cutting ants Atta sexdens and Acromyrmex subterraneus subterraneus. Azadirachtin caused death to minor and major workers of both species in a concentration-dependent manner. Topical application of the compound did not diminish the immune response of ants in a microfilament encapsulation assay. Azadirachtin showed no effect on the immune response of workers but increased worker mortality, which indicates its potential as an ant control agent.

Keywords

Immunity Neem Encapsulation Formicidae Attini Hymenoptera 

Notes

Acknowledgements

We would like to thank the Brazilian National Council for Scientific and Technological Development (CNPq) (Research Project no. 140294-2016-3 and 403708-2013-3) and the Minas Gerais Research Foundation (FAPEMIG) for their financial support. This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brasil (CAPES) – Finance code 001. We also thank the Federal University of Tocantins for the research grant provided to DJdS.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Informed consent

Informed consent was obtained from all individual participants included in the study.

References

  1. Baccaro FB, Feitosa RM, Fernandez F et al. (2015) Guia para os gêneros de formigas do Brasil.  https://doi.org/10.5281/zenodo.32912
  2. Bernardi D, Botton M, da Cunha US et al. (2013) Effects of azadirachtin on Tetranychus urticae (Acari: Tetranychidae) and its compatibility with predatory mites (Acari: Phytoseiidae) on strawberry. Pest Manag Sci 69:75–80.  https://doi.org/10.1002/ps.3364 CrossRefGoogle Scholar
  3. Biondi A, Zappalà L, Stark JD, Desneux N (2013) Do biopesticides affect the demographic traits of a parasitoid wasp and its biocontrol services through sublethal effects? PLoS ONE 8.  https://doi.org/10.1371/journal.pone.0076548 CrossRefGoogle Scholar
  4. Blaney WM, Simmonds MSJ, Ley SV et al. (1990) Antifeedant effects of azadirachtin and structurally related compounds on lepidopterous larvae. Entomol Exp Appl 55:149–160.  https://doi.org/10.1007/BF00352576 CrossRefGoogle Scholar
  5. Boeke SJ, Boersma MG, Alink GM et al. (2004) Safety evaluation of neem (Azadirachta indica) derived pesticides. J Ethnopharmacol 94:25–41CrossRefGoogle Scholar
  6. Boff P, Giesel A, Carissimi Boff MI (2016) No-residual baits and farmer perception to manage leaf-cutting ants. Agroecol Sustain Food Syst.  https://doi.org/10.1080/21683565.2016.1139649 CrossRefGoogle Scholar
  7. Box GEP, Cox DR (1964) An analysis of transformations. Source J R Stat Soc Ser B J R Stat Soc Ser B.  https://doi.org/10.2307/2287791 CrossRefGoogle Scholar
  8. Chaudhary S (2017) Progress on Azadirachta indica based biopesticides in replacing synthetic toxic pesticides. Front Plant Sci 8:1–13.  https://doi.org/10.3389/fpls.2017.00610 CrossRefGoogle Scholar
  9. da Silva Camargo R, Puccini C, Forti LC (2017) Allogrooming, self-grooming, and touching behavior: Contamination routes of leaf-cutting ant workers using a fat-soluble tracer dye. Insects 59(8) 1–9.  https://doi.org/10.3390/insects8020059 CrossRefGoogle Scholar
  10. de Azambuja P, Garcia ES, Ratcliffe NA, David Warthen J (1991) Immune-depression in Rhodnius prolixus induced by the growth inhibitor, azadirachtin. J Insect Physiol 37:771–777.  https://doi.org/10.1016/0022-1910(91)90112-D CrossRefGoogle Scholar
  11. de Souza DJ, Bézier A, Depoix D et al. (2009) Blochmannia endosymbionts improve colony growth and immune defence in the ant Camponotus fellah. BMC Microbiol 9:29.  https://doi.org/10.1186/1471-2180-9-29 CrossRefGoogle Scholar
  12. Della Lucia TM, Gandra LC, Guedes RN (2014) Managing leaf-cutting ants: peculiarities, trends and challenges. Pest Manag Sci 70:14–23.  https://doi.org/10.1002/ps.3660 CrossRefGoogle Scholar
  13. Della Lucia TMC (2003) Capitulo 24. Hormigas de importancia económica en la región Neotropical. In: Introduccion a las hormigas de la region Neotropical. pp 337–349.  https://doi.org/10.1108/EUM0000000005647 CrossRefGoogle Scholar
  14. Della Lucia TMC, Moreira DDO (1993) Caracterização de ninhos. In: Della Lucia TMC (ed) As formigas cortadeiras. Folha de Viçosa, Viçosa, MG, Brazil, pp 32–42Google Scholar
  15. Della Lucia TMC, Oliveira MA, Araújo MS, Vilela EF (1995) Avaliação da não preferência da formiga cortadeira Acromyrmex subterraneus subterraneus Forel ao corte de Eucalyptus. Rev Arvore 19(1):92–99Google Scholar
  16. Desneux N, Decourtye A, Delpuech J-M (2007) The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol 52:81–106.  https://doi.org/10.1146/annurev.ento.52.110405.091440 CrossRefGoogle Scholar
  17. Ebrahimi M, Safaralizade MH, Valizadegan O (2013) Contact toxicity of Azadirachta indica (Adr. Juss.), Eucalyptus camaldulensis (Dehn.) and Laurus nobilis (L.) essential oils on mortality cotton aphids, Aphis gossypii Glover (Hem.: Aphididae). Arch Phytopathol Plant Prot 46:2153–2162.  https://doi.org/10.1080/03235408.2013.774526 CrossRefGoogle Scholar
  18. Er A, Taşkıran D, Sak O (2017) Azadirachtin-induced effects on various life history traits and cellular immune reactions of Galleria mellonella (Lepidoptera: Pyralidae). Arch Biol Sci 69:335–344.  https://doi.org/10.2298/ABS160421108E CrossRefGoogle Scholar
  19. Gandra LC, Amaral KD, Couceiro JC et al. (2016) Mechanism of leaf-cutting ant colony suppression by fipronil used in attractive toxic baits. Pest Manag Sci 72:1475–1481.  https://doi.org/10.1002/ps.4239 CrossRefGoogle Scholar
  20. Garcia JF, Grisoto E, Vendramim JD, Botelho PS (2006) Bioactivity of neem, Azadirachta indica, against spittlebug Mahanarva fimbriolata (Hemiptera: Cercopidae) on sugarcane. J Econ Entomol 99:2010–2014CrossRefGoogle Scholar
  21. Gillespie JP, Kanost MR, Trenczek T (1997) Biological mediators of insect immunity. Annu Rev Entomol 42:611–43.  https://doi.org/10.1146/annurev.ento.42.1.611 CrossRefGoogle Scholar
  22. Hölldobler B, Wilson EO (1990) The Ants. Harvard University Press, Cambridge, MassCrossRefGoogle Scholar
  23. Hubbell SP, Wiemer DF (1983) Host plant selection by an attine ant. In: Proceedings of the first international symposium on social insects in the tropics. pp 133–154Google Scholar
  24. Isman MB (2006) Botanical insecticides, deterrents, and repellents in modern agriculture and an increasingly regulated world. Annu Rev Entomol 51:45–66.  https://doi.org/10.1146/annurev.ento.51.110104.151146 CrossRefGoogle Scholar
  25. Martinez SS (2002) O nim - Azadirachta indica - natureza, usos múltiplos, produção. IAPAR, Londrina, PR, BrazilGoogle Scholar
  26. Mordue (Luntz) AJ, Blackwell A (1993) Azadirachtin: an update. J Insect Physiol 39:903–924.  https://doi.org/10.1016/0022-1910(93)90001-8 CrossRefGoogle Scholar
  27. Mordue AJ, Simmonds MSJ, Ley SV et al. (1998) Actions of azadirachtin, a plant allelochemical, against insects. Pestic Sci 54:277–284.  https://doi.org/10.1002/(SICI)1096-9063(1998110)54:33.0.CO;2-I
  28. Oliveira MA, Araújo MS, Marinho CGS et al. (2011) Manejo de formigas-cortadeiras. In: Della Lucia TMC (ed) Formigas-cortadeiras: da bioecologia ao manejo, 1st edn. Editora UFV, Viçosa, MG, Brazil, pp 400–419Google Scholar
  29. Ribeiro MMR, Della Lucia TMC, Bacci L et al. (2008) Effect of plant extracts on survival of leaf-cutting ant workers (Hymenoptera:Formicidae). Sociobiology 52:387–398Google Scholar
  30. Santana DLQ, Couto L (1990) Resistência intra-especifica de eucaliptos a formigas-cortadeiras. Bol Pesq Flores 20:13–21Google Scholar
  31. Santos-Oliveira MFS, Bueno OC, Marini T, et al. (2006) Toxicity of Azadirachta indica to leaf-cutting ant Atta sexdens rubropilosa (Hymenoptera: Formicidae). Sociobiology. www.csuchico.edu/biol/Sociobiology/sociobiologyindex.html
  32. Schmutterer H (1985) Which insect pests can be controlled by application of neem seed kernel extracts under field conditions? Zeitschr f angew Ent 100:468–475.  https://doi.org/10.1111/j.1439-0418.1985.tb02808.x CrossRefGoogle Scholar
  33. Schmutterer H (1990) Properties and potential of natural pesticide from the neem tree, Azadirachta indica. Annu Rev Entomol 35:271–297CrossRefGoogle Scholar
  34. Souza CR, Sarmento RA, Venzon M, et al. (2015) Lethal and sublethal effects of neem on Aphis gossypii and Cycloneda sanguinea in watermelon. Acta Sci Agron 233–239.  https://doi.org/10.4025/actasciagron.v37i2.19517
  35. Tomé HVV, Martins JC, Corrêa AS et al. (2013) Azadirachtin avoidance by larvae and adult females of the tomato leafminer Tuta absoluta. Crop Prot 46:63–69.  https://doi.org/10.1016/j.cropro.2012.12.021 CrossRefGoogle Scholar
  36. Vendramin JD, Silveira Neto S, Cerignoni JA (1995) Não-preferência de Atta sexdens rubropilosa Forel (Hymenoptera: Formicidae) por especies de Eucalyptus. Ecossistema 20:87–92Google Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Departamento de EntomologiaUniversidade Federal de ViçosaViçosaBrazil
  2. 2.Universidade Federal de ViçosaFlorestalBrazil
  3. 3.Universidade Federal do TocantinsGurupiBrazil
  4. 4.Departamento de Biologia AnimalUniversidade Federal de ViçosaViçosaBrazil

Personalised recommendations