Potential of Two Trichogrammatidae species for Helicoverpa armigera control

  • F P PereiraEmail author
  • C Reigada
  • A J F Diniz
  • J R P Parra
Biological Control


Helicoverpa armigera (Hübner) has attacked several economically important crops since it was first reported in Brazil in 2013. Because insecticides have been used intensively to control H. armigera, resistant populations have been detected more frequently. One alternative to insecticides is the use of biological control with egg parasitoids from the family Trichogrammatidae (Hymenoptera). The present study evaluated the use of different species and strains of these parasitoids to control H. armigera in soybean. Five strains of Trichogramma pretiosum (Riley): RV (Rio Verde, Goiás, Brazil), SO (Sorriso, Mato Grosso, Brazil), 47A (Irvine, CA, USA), PR (Colombo, Paraná, Brazil), and AN (Anhumas, São Paulo, Brazil), and Trichogrammatoidea annulata (De Santis) denominated TR, from Anhumas, were used. The following parasitoid biological parameters were evaluated: parasitism rates (%), offspring viability (%) number of parasitoids emerged per egg, egg-adult duration (days), female longevity, and offspring sex ratio. Strain RV of T. pretiosum from central Brazil performed best.


Integrated pest management natural enemies lepidoptera 



We thank Janet W. Reid, JWR Associates, for the English revision. FPP held a fellowship awarded by CAPES during the project execution.

Author Contribution

FPP and JRPP planned and designed the study. FPP and AJFD executed experimental work. FPP wrote the manuscript. CR conducted the data analysis. JRPP supervised the project.

Funding Information

This study received financial support from the National Institute of Semiochemicals in Agriculture (INCT: Process No. 573761/2008-6).


  1. Agrofit/Mapa Sistema de agrotóxicos fitossanitários (2019) Coordenação Geral de Agrotóxicos e Afins, Accessed March 20, 2019
  2. Bai B, Luck RF, Foster L, Stephens B, Janssem JAM (1992) The effect of host size on quality attributes of the egg parasitoid, Trichogramma pretiosum. Entomol Exp Appl 64:37–48CrossRefGoogle Scholar
  3. Ballal CR, Singh SP (2003) The effectiveness of Trichogramma chilonis, Trichogramma pretiosum and Trichogramma brasiliense (Hymenoptera: Trichogrammatidae) as parasitoids of Helicoverpa armigera (Lepidoptera: Noctuidae) on sunflower (Helianthus annuus) and redgram (Cajanus cajan). Biocontrol Sci Tech 13:231–240. CrossRefGoogle Scholar
  4. Beserra E, Dias C, Parra JRP (2003) Características biológicas de linhagens de Trichogramma pretiosum desenvolvidas em ovos de Spodoptera frugiperda. Acta Sci Agron 25:479–483CrossRefGoogle Scholar
  5. Beserra EB, Parra JRP (2004) Biologia e parasitismo de Trichogramma atopovirilia Oatman & Platner e Trichogramma pretiosum Riley (Hymenoptera, Trichogrammatidae) em ovos de Spodoptera frugiperda (J.E. Smith). Rev Bras Entomol 48:119–126. CrossRefGoogle Scholar
  6. Bigler F (1989) Quality assessment and control in entomophagous insects used for biological control. J Appl Entomol 108:390–400CrossRefGoogle Scholar
  7. Bowen W, Stern V (1966) Effect of temperature on the production of males and sexual in a uniparental race of Trichogramma semifumatum (Hymenoptera: Trichogrammatidae). Ann Entomol Soc Am 59:823–834CrossRefGoogle Scholar
  8. Browning H, Melton C (1987) Indigenous and exotic Trichogrammatidae (Hymenoptera: Trichogrammatidae) evaluated for biological control of Eoreuma loftini and Diatraea saccharalis (Lepidoptera: Pyralidae) borers on sugarcane. Environ Entomol 16:360–364CrossRefGoogle Scholar
  9. Bueno RCOF, Parra JRP, Bueno AF, Haddad ML (2009) Desempenho de tricogramatídeos como potenciais agentes de controle de Pseudoplusia includens Walker (Lepidoptera: Noctuidae). Neotrop Entomol 38:389–394. CrossRefPubMedGoogle Scholar
  10. Clarke G, Mckenzie L (1992) Fluctuating asymmetry as a quality control indicator for insect mass rearing processes. J Econ Entomol 85:2045–2050CrossRefGoogle Scholar
  11. Cunningham JP, Zalucki MP (2014) Understanding heliothine (Lepidoptera: Heliothinae) pests: what is a host plant? J Econ Entomol 107:881–896. CrossRefPubMedGoogle Scholar
  12. Czepak C, Albernaz K, Vivan LM, Guimarães HO, Carvalhais T (2013) Primeiro registro de ocorrência de Helicoverpa armigera (Hubner)(Lepidoptera: Noctuidae) no Brasil. Pesqui Agropecu Trop 43:110–113. CrossRefGoogle Scholar
  13. Dahlan A, Gordh G (1996) Development of Trichogramma australicum Girault (Hymenoptera: Trichogrammatidae) on Helicoverpa armigera (Hübner) eggs (Lepidoptera: Noctuidae). Aust J Entomol 35:337–344CrossRefGoogle Scholar
  14. Dhandapani N, Kalyanasundaram M, Swamiappan M, Sundara Babu PC, Jayaraj S (1992) Experiments on management of major pests of cotton with biocontrol agents in India. J Appl Entomol 114:52–56CrossRefGoogle Scholar
  15. Dias NS, Parra JRP, Costa Lima TG (2008) Seleção de hospedeiro alternativo para três espécies de tricogramatídeos neotropicais. Pesq Agropec Bras 43:1467–1473CrossRefGoogle Scholar
  16. Durigan MR, Corrêa AS, Pereira RM, Leite NA, Amado D, Souza DR, Omoto C (2017) High frequency of CYP337B3 gene associated with control failures of Helicoverpa armigera with pyrethroid insecticides in Brazil. Pestic Biochem Physiol 143:73–80. CrossRefPubMedGoogle Scholar
  17. El-Wakeil N (2007) Evaluation of efficiency of Trichogramma evanescens reared on different factitious hosts to control Helicoverpa armigera. J Pest Sci 80:29–34. CrossRefGoogle Scholar
  18. Fathipour Y, Sederatian A (2013) Integrated management of Helicoverpa armigera in soybean cropping systems. In: El-Shemy HA (ed) Soybean: Pest Resistance. Cairo, Intech, pp 231–280 288pGoogle Scholar
  19. Fitt G (1989) The ecology of Heliothis species in relation to agroecosystems. Annu Rev Entomol 34:17–52CrossRefGoogle Scholar
  20. Greenberg SM, Nordlund D, Wu Z (1998) Influence of rearing host on adult size and oviposition behavior of mass produced female Trichogramma minutum Riley and Trichogramma pretiosum Riley (Hymenoptera: Trichogrammatidae). Biol Control 11:43–48CrossRefGoogle Scholar
  21. Hassan SA (1989) Selection of suitable Trichogramma strains to control the codling moth Cydia pomonella and the summer fruit tortrix moth Adoxophyes orana, Pandemis heparana (Lep., Tortricidae). Entomophaga 34:19–27CrossRefGoogle Scholar
  22. Hassan SA (1993) The mass rearing and utilization of Trichogramma to control lepidopterous pests: achievements and outlook. Pestic Sci 37:387–391CrossRefGoogle Scholar
  23. Hassan SA (1994) Strategies to select Trichogramma species for use in biological control. In: Wajnberg E, Hassan SA (eds) Biological Control with Egg Parasitoids. CAB international, Oxon, pp 55–68 286pGoogle Scholar
  24. Hassan SA (1997) Seleção de espécies de Trichogramma para o uso em programas de controle biológico. In: Parra JRP, Zucchi RA (eds) Trichogramma e o controle biológico aplicado. FEALQ, Piracicaba, pp 183–206 324pGoogle Scholar
  25. Hussain D, Saleem M, Ghouse G, Abbas M (2015) Insecticide resistance in field populations of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae). J Entomol Sci 50:119–128CrossRefGoogle Scholar
  26. Jarjees EA, Merritt DJ (2002) Development of Trichogramma australicum Girault (Hymenoptera: Trichogrammatidae) in Helicoverpa armigera (Lepidoptera: Noctuidae) host eggs. Aust J Entomol 41:310–315. CrossRefGoogle Scholar
  27. Keller M, Lewis WJ, Stinner RE (1985) Biological and practical significance of movement by Trichogramma species: a review. Southwest Entomol 8:138–155Google Scholar
  28. Kriticos D, Ota N, Hutchinson WD, Beddow J, Walsh T, Tay WK, Borchert DM, Paula-Moreas SV, Czepak C, Zalucki P (2015) The potential distribution of invading Helicoverpa armigera in North America: it is just a matter of time? PLoS One 10(7):e0119618 PubMedPubMedCentralCrossRefGoogle Scholar
  29. Kukanur VS, Singh TVK, Kranthi KR, Andow DA (2018) Cry1Ac resistance allele frequency in field populations of Helicoverpa armigera (Hübner) collected in Telangana and Andhra Pradesh, India. Crop Prot 107:34–40. CrossRefGoogle Scholar
  30. Lammers J, Macleod A (2007) Report of a pest risk analysis: Helicoverpa armigera (Hubner, 1808). = 3879
  31. Li Li-Ying (1994) Wordwide use of Trichogramma for biological control on differents crops: a survey. In Wajnberg E, Hassan SA eds Biological control with egg parasitoids. Wallingford, CAB International, pp 37-53Google Scholar
  32. Liu Z, Li D, Gong P, Wu K (2004) Life table studies of the cotton bollworm, Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae), on different host plants. Environ Entomol 33:1570–1576. CrossRefGoogle Scholar
  33. Lu Z, Xu Y (1998) The consideration with the incessant outbreak of cotton bollworm Helicoverpa armigera (Hubner). Entomol Knowl 35:132–136Google Scholar
  34. Mantel N (1966) Evaluation of survival data and two new rank order statistics arising in its consideration. Cancer Chemother Rep 50(3):163–170PubMedGoogle Scholar
  35. Martin P, Lingren P, Greene G, Gressel E (1981) The parasitoid complex of three noctuids (Lep.) in a northern Florida cropping system: seasonal occurrence, parasitization, alternate hosts, and influence of host-habitat. Entomophaga 26:401–419CrossRefGoogle Scholar
  36. Mastrangelo T, Paulo DF, Bergamo LW, Morais EGF, Silva M, Bezerra-Silva G, Azeredo-Espin AML (2014) Detection and genetic diversity of a heliothine invader (Lepidoptera: Noctuidae) From North and Northeast of Brazil. J Econ Entomol 107:970–980. CrossRefPubMedGoogle Scholar
  37. Messenger PS, van den Bosch R (1971) The adaptability of introduced biological control agents. In: Huffaker CB (ed) Biological control. Plenum, New York, pp 68–92 292pGoogle Scholar
  38. Molina R, Parra JRP (2006) Seleção de Trichogramma (Hymenoptera: Trichogrammatidae) e determinação do número de parasitóides a ser liberado para o controle de Gymnandrosoma aurantianum Lima (Lepidoptera: Tortricidae). Rev Bras Entomol 50:534–539CrossRefGoogle Scholar
  39. Moral R, Hinde J, Demetrio C (2016) Half-normal plots with simulation envelopes. R package version 1.1-2.Google Scholar
  40. Murúa MG, Scalora FS, Navarro FR, Cazado LE, Casmuz A, Villagrán ME, Lobos E, Gastaminza G (2014) First record of Helicoverpa armigera (Lepidoptera: Noctuidae) in Argentina. Florida Entomol 97:854–856CrossRefGoogle Scholar
  41. Nava DE, Takahashi KM, Parra JRP (2007) Linhagens de Trichogramma e Trichogrammatoidea para controle de Stenoma catenifer. Pesq Agropec Bras 42:9–16CrossRefGoogle Scholar
  42. Nordlund D, Chalfant R, Lewis WJ (1984) Arthropod populations, yields and damage in monocultures and polycultures of corn, beans and tomatoes. Agric Ecosyst Environ 12:127–133CrossRefGoogle Scholar
  43. Nordlund DA (1994) Habitat location by Trichogramma, in biological control with egg parasitoids. In: Wajnberg E, Haasan S (eds) Biological control with egg parasitoids. CAB International, Oxon, pp 155–164 286pGoogle Scholar
  44. Pak G (1988) Selection of Trichogramma for inundative biological control. Agricultural University, Wageningen, p 224Google Scholar
  45. Pak G, Berkhout H, Klapwijk J (1991) Do Trichogramma look for hosts? Les Colloq I’INRA 56:77–80Google Scholar
  46. Pak G, van Lenteren J (1988) Criteria and methods for the pre-release evaluation of diferent Trichogramma spp. strains, p.165–172. In: International Symposium, Trichogramma and Other Egg Parasites, 2. Guangzhou, 390p.Google Scholar
  47. Parra JRP, Zucchi RA, Silveira Neto S (1986) Biological control of pests throught egg parasitoids of the genera Trichogramma and/or Trichogrammatoidea. Mem Inst Oswaldo Cruz 82:153–160CrossRefGoogle Scholar
  48. Parra JRP (2014) Biological control in Brazil: an overview. Sci Agric 71:345–355CrossRefGoogle Scholar
  49. Parra JRP, Coelho A Jr, Geremias LD, Bertin A, Ramos CJ (2014) Criação de Anagasta kuehniella em pequena escala, para produção de Trichogramma. Occasio, Piracicaba, p 32Google Scholar
  50. Parra JRP, Zucchi RA, Coelho A Jr, Geremias LD, Cônsoli FL (2015) Trichogramma as a tool for IPM in Brazil. In: Vinson SB, Greenberg SM, Liu TX, Rao A, Volosciuk LF (eds) Biological control of pests using Trichogramma: current status and perspectives. Northwest A&F University Press, Yangling, pp 472–496 496pGoogle Scholar
  51. Pratissoli D, Parra JRP (2001) Seleção de linhagens de Trichogramma pretiosum Riley (Hymenoptera: Trichogrammatidae) para o controle das traças Tuta absoluta (Meyrick) e Phtorimaea operculella (Zeller) (Lepidoptera: Gelechiidae). Neotrop Entomol 30:277–282CrossRefGoogle Scholar
  52. Pratissoli D, Thuler RT, Andrade GS, Zanotti LCM, Silva AF (2005) Estimativa de Trichogramma pretiosum para controle de Tuta absoluta em tomateiro estaqueado. Pesqui Agropecu Bras 40:715–718CrossRefGoogle Scholar
  53. R Development Core Team (2018) R Development Core Team. A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. 3501p.Google Scholar
  54. Reed W (1965) Heliothis armigera (Hb.) (Noctuidae) in western Tanganyika: II. Ecology and natural and chemical control. Bull Entomol Res 56:127–140CrossRefGoogle Scholar
  55. Reigada C, de Andrade MR, Demétrio CGB, Parra JRP (2018) Cross-crop effects on larval growth, survivorship and fecundity of Helicoverpa armigera. J Pest Sci 91:121–131. CrossRefGoogle Scholar
  56. Singh S, Ballal C, Poorani J (2002) Old World bollworm Helicoverpa armigera, associated Heliothinae and their natural enemies. Project Directorate of Biological Control, Karmataka, 135pGoogle Scholar
  57. Singh SP (1994) Fifteen years of AICRP on biological control. Tech Bull 8:320Google Scholar
  58. Smith S (1996) Biological control with Trichogramma: advances, successes, and potential of their use. Annu Rev Entomol 41:375–406PubMedCrossRefGoogle Scholar
  59. Sosa-Gómez DR, Specht A, Paula-Moraes SV, Lima-Lopes A, Yano SAC, Micheli A, Morais EGF, Gallo P, Pereira PRVS, Salvadori JR, Botton M, Zenker MM, Azevedo-Filho WS (2015) Timeline and geographical distribution of Helicoverpa armigera (Hübner) (Lepidoptera, Noctuidae: Heliothinae) in Brazil. Rev Bras Entomol 60:101–104. CrossRefGoogle Scholar
  60. Tay WT, Soria MF, Walsh T, Thomazoni D, Silvie P, Behere GT, et al. (2013) A Brave New World for an Old World Pest: Helicoverpa armigera (Lepidoptera: Noctuidae) in Brazil. PLoS ONE 8(11):e80134. Scholar
  61. Thorpe K (1985) Effects of height and habitat type on egg parasitism by Trichogramma minutum and T. pretiosum (Hym.: Trichogrammatidae). Agric Ecosyst Environ 12:117–126CrossRefGoogle Scholar
  62. van Lenteren J (1986) Evalution, mass production, quality control and release of entomophagous insects. In: Franz J (ed) Biological plant and health protection. Fischer, Stuttgart, pp 31–56 280pGoogle Scholar
  63. van Lenteren J (1989) Biological control by augmentation. In: Vedalia symposium on biological control: a century of success. University of California, Riverside, p 33Google Scholar
  64. Vinson S (1997) Comportamento de seleção hospedeira de parasitoides de ovos, com ênfase na familia Trichogrammatidae. In: Parra JRP, Zucchi RA (eds) Trichogramma e o controle biológico aplicado. FEALQ, Piracicaba, pp 67–119 324pGoogle Scholar
  65. Wajnberg E (1994) Intra-population genetic variation in Trichogramma. In: Wajnberg E, Hassan S (eds) Biological control with egg parasitoids. CAB International, Oxon, pp 245–266 286pGoogle Scholar
  66. Yadav D, Patel RC, Patel DS (1985) Impact of inundative release of Trichogramma chilonis Ishii against Heliothis armigera (Hbn.) in Gujarat (India). J Entomol Res 9:153–159Google Scholar
  67. Yang Y, Li Y, Wu Y (2013) Current status of insecticide resistance in Helicoverpa armigera after 15 years of Bt cotton planting in China. J Econ Entomol 106:375–381PubMedCrossRefGoogle Scholar
  68. Zalucki M, Daglish G, Firempong S, Twine P (1986) The biology and ecology of Heliothis armigera (Hubner) and H. punctigera Wallengreen (Lepidoptera: Noctuidae) in Australia: what do we know? Aust J Zool 34:779–814CrossRefGoogle Scholar
  69. Zucchi RA, Querino RB, Monteiro RC (2010) Diversity and hosts of Trichogramma in the new world, with emphasis in South America. In: Cônsoli FL, Parra JRP, Zucchi RA (eds) Egg parasitoids in agroecosystems with emphasis on Trichogramma. Springer, New York, pp 219, 479p–237Google Scholar

Copyright information

© Sociedade Entomológica do Brasil 2019

Authors and Affiliations

  • F P Pereira
    • 1
    Email author
  • C Reigada
    • 2
  • A J F Diniz
    • 1
  • J R P Parra
    • 1
  1. 1.Depto de Entomologia e Acarologia, Escola Superior de Agricultura Luiz de QueirozUniv de São PauloSão PauloBrazil
  2. 2.Depto de Ecologia e Biologia EvolutivaUniv Federal de São CarlosSão PauloBrazil

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