Responses of Spodoptera frugiperda and Trichogramma pretiosum to Rice Plants Exposed to Herbivory and Phytohormones

  • F B LopesEmail author
  • J Sant’Ana
Ecology, Behavior and Bionomics


Damage caused by herbivorous insects and application of phytohormones can activate signaling pathways, which result in greater production of secondary metabolites, increasing plant defenses. This study aimed to evaluate the induced direct resistance (local and systemic) of rice plants caused by herbivorous insects and exogenous application of methyl jasmonate (MJ) and salicylic acid (SA) in the development of fall armyworm, Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae). Moreover, indirect defenses through chemotactic responses of Trichogramma pretiosum (Riley) (Hymenoptera: Trichogrammatidae) submitted to the same treatments were investigated. Direct defense was evaluated by measuring weight gain of fall armyworm larvae fed with leaves of plants previously exposed to herbivores or treated with MJ (2 and 5 mM), SA (8 and 16 mM), or control. Indirect defense was verified by chemotactic behavior of wasps in two-choice olfactometer tests to plants exposed to herbivores and evaluated after 24, 48, and 72 h in comparison with undamaged ones, as well as plants treated with the same phytohormones contrasted with the control. The gain of weight was reduced in immature developmental stage of S. frugiperda fed in leaves previously damaged by fall armyworm and in newly formed leaves after damage to the plants, comparing with control. Leaves treated with MJ (2 mM and 5 mM) and SA (8 mM) were less eaten than those not treated. Parasitoids triggered a positive chemotactic behavior in rice plants that had been sprayed with same concentrations. This study showed that rice plants can activate direct and indirect defenses through an exogenous application of phytohormones.


Methyl jasmonate, salicylic acid, fall armyworm, herbivore-induced volatile, parasitoid 



We would like thank the Coordinating Committee on the Improvement of Higher Education Personnel (CAPES) of Brazil for providing the scholarship to the first author and the National Council for Scientific and Technological Development for the fellowships awarded to the second author (CNPq 306474/2015-8).

Author Contribution Statement

FBL and JS conceived and designed the study; FBL performed the experiments and analyzed the data; FBL and JS wrote the manuscript.


  1. Agrawal AA (2005) Future directions in the study of induced plant responses to herbivory. J Chem Ecol 115:97–105Google Scholar
  2. Baker JE, Bowling CC (1967) Rearing of two lepidopterous pests of rice on a common artificial diet. Ann Entomol Soc Am 60:1215–1216CrossRefGoogle Scholar
  3. Bayram A, Tonga A (2018) Cis-Jasmone treatments affect pests and beneficial insects of wheat (Triticum aestivum L.): the influence of doses and plant growth stages. Crop Prot 105:70–79CrossRefGoogle Scholar
  4. Beserra EB, Dias CTDS, Parra JRP (2002) Distribution and natural parasitism of Spodoptera Frugiperda (Lepidoptera: Noctuidae) eggs at different phenological stages of corn. Florida Entomol 85:588–593CrossRefGoogle Scholar
  5. 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
  6. Boughton AJ, Hoover K, Felton GW (2006) Impact of chemical elicitor applications on greenhouse tomato plants and population growth of the green peach aphid, Myzus persicae. Entomol Exp Appl 120:175–188CrossRefGoogle Scholar
  7. Bruinsma M, Posthumus MA, Mumm R, Mueller MJ, Van Loon JJA, Dicke M (2009) Jasmonic acid-induced volatiles of Brassica oleracea attract parasitoids: effects of time and dose, and comparison with induction by herbivores. J Exp Bot 60:2575–2587CrossRefGoogle Scholar
  8. Counce PA, Keisling TC, Mitchell AJ (2000) A uniform, objective, and adaptive system for expressing rice development. Crop Sci 40:436–443CrossRefGoogle Scholar
  9. De Moraes CM, Lewis WJ, Pare PW, Alborne HT, Tumlinson JH (1998) Herbivore-infested plants selectively attract parasitoids. Nature 393:570–573CrossRefGoogle Scholar
  10. De Sá LAN, Parra JRP, De Sá LAN (1994) Natural parasitism of Spodoptera frugiperda and Helicoverpa zea (Lepidoptera: Noctuidae) eggs in corn by Trichogramma pretiosum (Hymenoptera: Trichogrammatidae) in Brazil. Florida Entomol 77:185CrossRefGoogle Scholar
  11. Durrant WE, Dong X (2004) Systemic acquired resistence. Annu Rev Phytopathol 42:185–209CrossRefGoogle Scholar
  12. Fatouros NE, Dicke M, Mumm R, Meiners T, Hilker M (2008) Foraging behavior of egg parasitoids exploiting chemical information. Behav Ecol 19:677–689CrossRefGoogle Scholar
  13. Ferreira E (1999) Pragas e seu controle. In: Santos AB, Stone LF, Vieira NRA (eds) A cultura do arroz no Brasil. Embrapa Arroz e Feijão, Santo Antônio de Goiás, pp 197–261Google Scholar
  14. Figueiredo M, Cruz I, da Silva RB, Foster JE (2015) Biological control with Trichogramma pretiosum increases organic maize productivity by 19.4%. Agron Sustain Dev 35:1175–1183CrossRefGoogle Scholar
  15. Fonseca JR (2006) Recursos genéticos. In: Santos AB, Stone LF, Vieira NRA (eds) A cultura do arroz no Brasil. Embrapa Arroz e Feijão, Santo Antônio de Goiás, pp 257–288Google Scholar
  16. Freitas TFS (2017) Ecologia química de pentatomídeos em Oryza sativa (Poaceae): implicações no manejo com feromônio sexual sintético e nas interações tritróficas mediadas por fitormônios. 2017. 116 f. Tese (Doutorado em Fitotecnia) - Programa de Pós-Graduação em Fitotecnia, Faculdade de Agronomia, Universidade Federal do Rio Grande do Sul, Porto AlegreGoogle Scholar
  17. Freitas TFS, Stout MJ, Sant’Ana J (2018) Effects of exogenous methyl jasmonate and salicylic acid on rice resistance to Oebalus pugnax. Pest Manag Sci.
  18. Girling RD, Stewart-Jones A, Dherbecourt J, Staley JT, Wright DT, Poppy GM (2011) Parasitoids select plants more heavily infested with their caterpillar hosts: a new approach to aid interpretation of plant headspace volatiles. Proc R Soc B Biol Sci 278:2646–2653CrossRefGoogle Scholar
  19. Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227CrossRefGoogle Scholar
  20. Gordy JW, Leonard BR, Blouin D, Davis JA, Stout MJ (2015) Comparative effectiveness of potential elicitors of plant resistance against Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae) in four crop plants. PLoS One 10:1–14CrossRefGoogle Scholar
  21. Guerrieri E, Poppy GM, Powell W, Tremblay E, Pennacchio F (1999) Induction and systemic release of herbivore-induced plant volatiles mediating in-flight orientation of Aphidius ervi. J Chem Ecol 25:1247–1261CrossRefGoogle Scholar
  22. Hamm JC, Stout MJ, Riggio RM (2010) Herbivore- and elicitor-induced resistance in rice to the rice water weevil (Lissorhoptrus oryzophilus Kuschel) in the laboratory and field. J Chem Ecol 36:192–199CrossRefGoogle Scholar
  23. Harborne JB (1999) Classes and functions of secondary products. In: Walton NJ, Brown DE (eds) Chemicals from plants: perspectives on secondary plant products. Imperial College Press, London, pp 1–25Google Scholar
  24. Houseweart MW, Jennings DT, Welty C, Southard SG (1983) Progeny production by Trichogramma minutum (Hymenoptera: Trichogrammatidae) utilizing eggs for Choristoneura fumiferana (Lepidoptera: Tortricidae) and Sitotroga cerealella (Lepidoptera: Gelechiidae). Can Entomol 115:1245–1252CrossRefGoogle Scholar
  25. Kanno H, Satoh M, Kimura T, Fujita Y (2005) Some aspects of induced resistance to rice blast fungus, Magnaporthe grisea, in rice plant infested by white-backed planthopper, Sogatella furcifera. Appl Entomol Zool 40:91–97CrossRefGoogle Scholar
  26. Kanno H, Hasegawa M, Osamu K (2012) Accumulation of salicylic acid, jasmonic acid and phytoalexins in rice, Oryza sativa, infested by the white-backed planthopper, Sogatella furcifera (Hemiptera: Delphacidae). Appl Entomol Zool 47:27–34CrossRefGoogle Scholar
  27. Kawazu K, Mochizuki A, Sato Y, Sugeno W, Murata M, Seo S, Mitsuhara I (2012) Different expression profiles of jasmonic acid and salicylic acid inducible genes in the tomato plant against herbivores with various feeding modes. Arthropod Plant Interact 6:221–230CrossRefGoogle Scholar
  28. Ko K, Liu Y, Hou M, Babendreier D, Zhang F, Song K (2014) Evaluation for potential Trichogramma (Hymenoptera: Trichogrammatidae) strains for control of the striped stem borer (Lepidoptera: Crambidae) in the greater mekong subregion. J Econ Entomol 107:955–963CrossRefGoogle Scholar
  29. Lou YG, Ma B, Cheng JA (2005) Attraction of the parasitoid Anagrus nilaparvatae to rice volatiles induced by the rice brown planthopper Nilaparvata lugens. J Chem Ecol 31:2357–2372CrossRefGoogle Scholar
  30. Martinazzo T (2007) Liberação de Trichogramma pretiosum para controle biológico de Spodoptera frugiperda na cultura do milho. Rev Bras Agroecol 2:1657–1660Google Scholar
  31. Moraes MCB, Laumann RA, Pareja M, Sereno FTPS, Michereff MFF, Birkett MA, Pickett JA, Borges M (2009) Attraction of the stink bug egg parasitoid Telenomus podisi to defence signals from soybean activated by treatment with cis-jasmone. Entomol Exp Appl 131:178–188CrossRefGoogle Scholar
  32. Moreira X, Sampedro L, Zas R (2009) Defensive responses of Pinus pinaster seedlings to exogenous application of methyl jasmonate: concentration effect and systemic response. Environ Exp Bot 67:94–100CrossRefGoogle Scholar
  33. Parra JRP (1997) Técnicas de criação de Anagasta kuehniella, hospedeiro alternativo para a produção de Trichogramma. In: Parra JRP, Zucchi RA (eds) Trichogramma e o controle biológico aplicado. Editora FEALQ, Piracicaba, pp 121–150Google Scholar
  34. Poelman EH, Oduor AMO, Broekgaarden C, Hordijk CA, Jansen JJ, Van Loon JJA, Van Dam NM, Vet LEM, Dicke M (2009) Field parasitism rates of caterpillars on Brassica oleracea plants are reliably predicted by differential attraction of Cotesia parasitoids. Funct Ecol 23:951–962CrossRefGoogle Scholar
  35. Rodriguez-Saona CRB, Isaacs R (2012) Manipulation of natural enemies in agroecosystems: habitat and semiochemicals for sustainable insect pest control. In: Larramendy ML, Soloneski S (eds) Integrated pest management and pest control - current and future tactics. InTech, Rijeka, pp 89–126Google Scholar
  36. Sanches PA, Santos F, Peñaflor MFGV, Bento JMS (2017) Direct and indirect resistance of sugarcane to Diatraea saccharalis induced by jasmonic acid. Bull Entomol Res 107:828–838CrossRefGoogle Scholar
  37. Schweiger R, Heise AM, Persicke M, Müller C (2014) Interactions between the jasmonic and salicylic acid pathway modulate the plant metabolome and affect herbivores of different feeding types. Plant Cell Environ 37:1574–1585CrossRefGoogle Scholar
  38. Senthil-Nathan S, Kalaivani K, Choi MY, Paik CH (2009) Effects of jasmonic acid-induced resistance in rice on the plant brownhopper, Nilaparvata lugens Stål (Homoptera: Delphacidae). Pestic Biochem Physiol 95:77–84CrossRefGoogle Scholar
  39. Simpson M, Gurr GM, Simmons AT, Wratten SD, James DG, Leeson G, Nicol HI (2011) Insect attraction to synthetic herbivore-induced plant volatile-treated field crops. Agric For Entomol 13:45–57CrossRefGoogle Scholar
  40. Stout MJ, Riggio MR, Yang Y (2009) Direct induced resistance in Oryza sativa to Spodoptera frugiperda. Environ Entomol 38:1174–1181CrossRefGoogle Scholar
  41. Tamaoki D, Seo S, Yamada S, Kano A, Miyamoto A, Shishido H, Miyoshi S, Taniguchi S, Akimitsu K, Gomi K (2013) Jasmonic acid and salicylic acid activate a common defense system in rice. Plant Signal Behav 8:1–4CrossRefGoogle Scholar
  42. Tamiru A, Khan ZR (2017) Volatile semiochemical mediated plant defense in cereals: a novel strategy for crop protection. Agronomy 7:58CrossRefGoogle Scholar
  43. Tan CW, Lo JC, Yadav J, Ravuiwasa KT, Hwang SY (2011) Methyl jasmonate induced responses in four plant species and its effect on Spodoptera litura Fab. performance. J Asia Pac Entomol 14:263–269CrossRefGoogle Scholar
  44. Thaler JS, Stout MJ, Karban R, Duffey SS (1996) Exogenous jasmonates simulate insect wounding in tomato plants (Lycopersicon esculentum) in the laboratory and field. J Chem Ecol 22:1767–1781CrossRefGoogle Scholar
  45. Tian D, Peiffer M, De Moraes CM, Felton GW (2014) Roles of ethylene and jasmonic acid in systemic induced defense in tomato (Solanum lycopersicum) against Helicoverpa Zea. Planta 239:577–589CrossRefGoogle Scholar
  46. Tremacoldi CR (2009) Proteases e inibidores de proteases na defesa de plantas contra pragas. Embrapa Amazônia Oriental, Belém, p 44Google Scholar
  47. Williams L, Rodriguez-Saona C, Del Conte SCC (2017) Methyl jasmonate induction of cotton: a field test of the “attract and reward” strategy of conservation biological control. AoB Plants 9:1–15CrossRefGoogle Scholar
  48. Ye M, Luo SM, Xie JF, Li YF, Xu T, Liu Y, Song YY, Salzman KZ, Zeng RS (2012) Silencing COI1 in rice increases susceptibility to chewing insects and impairs inducible defense. PLoS One 7:1–11Google Scholar
  49. Yuan JS, Köllner TG, Wiggins G, Grant J, Degenhardt J, Chen F (2008) Molecular and genomic basis of volatile-mediated indirect defense against insects in rice. Plant J 55:491–503CrossRefGoogle Scholar

Copyright information

© Sociedade Entomológica do Brasil 2018

Authors and Affiliations

  1. 1.Ethology and Insect Chemical Ecology Lab, Federal Univ. of Rio Grande do SulPorto AlegreBrasil

Personalised recommendations