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Functional response of indigenous Trichogramma spp. to invasive tomato leafminer, Tuta absoluta (Meyrick) under laboratory conditions

  • T. N. Manohar
  • P. L. SharmaEmail author
  • S. C. Verma
  • K. C. Sharma
  • R. S. Chandel
Original Research Article
  • 13 Downloads

Abstract

Functional response is one of the most informative ways to study the density responsiveness of a natural enemy to the target pest. Tuta absoluta (Meyrick), one of the most destructive pests of tomato, has recently invaded India. In the present study, we investigated the functional response of Trichogramma achaeae Nagaraja and Nagarkatti, Trichogramma pretiosum Riley, Trichogramma chilonis (Ishii) and Trichogramma pieridis Nagaraja and Prashanth to the pest. All the parasitoids exhibited type II functional response to T. absoluta eggs. The handling time was minimum for T. achaeae (1.6 h) followed by T. pretiosum (1.86 h) T. chilonis (2.16 h) and T. pieridis (2.65 h). Theoretical maximum number of host eggs that could be parasitized in 24 h by each female of these parasitoids was estimated to be 16.23, 13.24, 11.05 and 8.97, respectively. Functional response parameters indicate that T. achaeae and T. pretiosum were more efficient parasitoids than the other two species against T. absoluta. It is, therefore, important to consider these tested egg parasitoids for biological control based integrated pest management programmes for this invasive pest.

Keywords

Attack rate Egg parasitoid Handling time Tomato pinworm Trichogrammatidae 

Notes

Acknowledgments

The authors are thankful to the Indian Council of Agricultural Research, New Delhi, India for providing financial support to the study through All India Coordinated Research Project on Biological Control of Crop Pests and Weeds.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Arturo C, Salvatore D, Gavino D (2012) Integrated control in protected crops. MeditClim Int Org Biol Integ ContWest Palaearc Reg Sec Bull 80:319–324Google Scholar
  2. Ballal CR, Gupta A, Mohan M, Lalitha Y, Verghese A (2016) The new invasive pest Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) in India and its natural enemies along with evaluation of Trichogrammatids for its biological control. Curr Sci 110:2155–2159CrossRefGoogle Scholar
  3. Bielza P (2010) La resistencia a insecticidas en Tuta absoluta. Phytoma 217:103–106Google Scholar
  4. Biondi A, Guedes RNC, Wan FH, Desneux N (2018) Ecology, Worldwide Spread, and Management of the Invasive South American Tomato Pinworm, Tuta absoluta: Past, Present, and Future. Annu Rev Entomol 63:239–258PubMedCrossRefPubMedCentralGoogle Scholar
  5. Bueno RCOF, Parra JRP, Bueno AF, Haddad ML (2009) Desempenho de tricogramatídeos comopotenciais agentes de controle de Pseudoplusia includens Walker (Lepidoptera: Noctuidae). Neotrop Entomol 38:389–394PubMedCrossRefPubMedCentralGoogle Scholar
  6. Cabello T, Gallego JR, Fernandez-Maldonado FJ, Soler A, Beltran D, Parra A, Vila E (2009) The damsel bug Nabis pseudoferus (hem.: Nabidae) as a new biological control agent of the south American tomato pinworm, Tuta absoluta (Lep.: Gelechiidae), in tomato crops of Spain. Int Org Biol Integ Cont Bull 49:219–223Google Scholar
  7. Campos MR, Biondi A, Adiga A, Guedes RNC, Desneux N (2017) From the western palaearctic region to beyond: Tuta absoluta, 10 years after invading Europe. J Pest Sci 90:787–796CrossRefGoogle Scholar
  8. Chailleux A, Desneux N, Seguret J, Do Thi Khanh H, Maignet P, Tabone E (2012) Assessing European egg parasitoids as a mean of controlling the invasive south American tomato pinworm Tuta absoluta. PLoS One 7(10):e48068PubMedPubMedCentralCrossRefGoogle Scholar
  9. Chailleux A, Beaarez P, Pizzol J, Dessneux EA, Romero RR, Desneux N (2013a) Potential for combined use of parasitoids and generalist predators for biological control of the key invasive tomato pest, Tuta absoluta. J Pest Sci 86:533–543CrossRefGoogle Scholar
  10. Chailleux A, Biondi A, Han P, Tabone E, Desneux N (2013b) Suitability of the pest-plant system Tuta absoluta (Lepidoptera: Gelechiidae)-tomato for Trichogramma (Hymenoptera: Trichogrammatidae) parasitoids and insights for biological control. J Econ Entomol 106:2310–2321PubMedCrossRefPubMedCentralGoogle Scholar
  11. Desneux N, Wajnberg E, Kris A, Wyckhuys G, Burgio G, Arpaia S, Narvaez-Vasquez CA, Gonzalez-Cabrera J, Catalan-Ruescas D, Tabone E, Frandon J, Pizzol J, Poncet C, Cabello T, Urbaneja A (2010) Biological invasion of European tomato crops by Tuta absoluta: ecology, geographic expansion and prospects for biological control. J Pest Sci 83:197–215CrossRefGoogle Scholar
  12. Desneux N, Luna MG, Guillemaud T, Urbaneja A (2011) The invasive south American tomato pinworm, Tuta absoluta, continues to spread in afro-Eurasia and beyond: the new threat to tomato world production. J Pest Sci 84:403–408CrossRefGoogle Scholar
  13. Ebrahimifar J, Jamshidnia A, Allahyari H (2017) Functional response of Eretmocerus delhiensis (Hymenoptera: Aphelinidae) on Trialeurodes vaporariorum (Hemiptera: Aleyrodidae) by parasitism and host feeding. J Insect Sci 56:1–5Google Scholar
  14. El-Arnaouty SA, Pizzol J, Galal HH, Kortam MN, Afifi AI, Beyssat V, Desneux N, Biondi A, Heikal IH (2014) Assessment of two Trichogramma species for the control of Tuta absoluta in north African tomato greenhouses. Afr Entomol 22(4):801–809CrossRefGoogle Scholar
  15. Faria CA, Angela JBT, Farias MI (2000) Functional response of Trichogramma pretiosum Riley (Hymenoptera: Trichogrammatidae) to Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) eggs: effect of host age. Neotrop Entomol 29:85–93Google Scholar
  16. Faria CA, Torres JB, Fernandes AMV, Farias AMI (2008) Parasitism of Tuta absoluta in tomato plants by Trichogramma pretiosum Riley in response to host density and plant structures. Ciencia Rural 38:1504–1509CrossRefGoogle Scholar
  17. Farrokhi S, Ashouri A, Shirazi J, Allahyari H, Huigens ME (2010) A comparative study on the functional response of Wolbachia infected and uninfected forms of the parasitoid wasp Trichogramma brassicae. J Insect Sci 10:1–11CrossRefGoogle Scholar
  18. Fathipour Y, Haghani M, Attaran M, Talebi AA, Moharramipour S (2003) Functional response of Trichogramma embryophagum (Hym.: Trichogrammatidae) on two laboratory hosts. J Entomol Soc Iran 23:41–45Google Scholar
  19. Fernandez-Arhex V, Corley JC (2003) The functional response of parasitoids and its implications for biological control. Biocont Sci Technol 13:403–413CrossRefGoogle Scholar
  20. Holling CS (1959) Some characteristics of simple types of predation and parasitism. Can Entomol 91:385–398CrossRefGoogle Scholar
  21. Ingegno BL, Ferracini CD, Gallinotti A, Alma Tavella L (2013) Evaluation of the effectiveness of Dicyphus errans (Wolff) as predator of Tuta absoluta (Meyrick). BioControl 67:246–252Google Scholar
  22. Jones RF, Rochat J, Goebel FR, Tabone E (2006) Functional response of Trichogramma chilonis to Galleria mellonella and Chilo sacchariphagus eggs. Entomol Exp et Appl 118:229–236CrossRefGoogle Scholar
  23. Juliano SA (2001) Nonlinear curve fitting: predation and functional response curves. In: Scheiner SM, Gureven J (eds) Design and analysis of ecological experiments. Oxford University Press, New York, pp 213–227Google Scholar
  24. Kalleshwaraswamy CM, Murthy S, Viraktamath CA, Krishnakumar NK (2015) Occurrence of Tuta absoluta (Lepidoptera: Gelechiidae) in the Malnad and Hyderabad-Karnataka regions of Karnataka, India. Fla Entomol 98:970–971CrossRefGoogle Scholar
  25. Kalyebi A, Overholtb WA, Schulthessa F, Muekec JM, Hassand SA, Sithananthama (2005) Functional response of six indigenous trichogrammatid egg parasitoids (Hymenoptera: Trichogrammatidae) in Kenya: influence of temperature and relative humidity. Biol Control 32:164–171CrossRefGoogle Scholar
  26. Karimian Z (1998) Bioecology of Trichogramma brassicae in paddy fields of Guilan province. M.Sc. Thesis. Faculty of Agriculture. University of Guilan, Iran 99pGoogle Scholar
  27. Lietti MMM, Botto E, Alzogaray RA (2005) Insecticide resistance in argentine populations of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). Neotrop Entomol 34:113–119CrossRefGoogle Scholar
  28. Luna MG, Sanchez NE, Pereyra PC, Nieves E, Savino V, Luft E, Virla E, Speranza S (2012) Biological control of Tuta absoluta in Argentina and Italy: evaluation of indigenous insects as natural enemies. Eur Medit Pl Prot Org Bull 42:260–267Google Scholar
  29. Luo SP, Li HM, Lu YH, Zhang F, Haye T, Kuhlmann U, Wu K (2014) Functional response and mutual interference of Peristenus spretus (Hymenoptera: Braconidae), a parasitoid of Apolygus lucorum (Heteroptera: Miridae). Biocont Sci Technol 24:247–256CrossRefGoogle Scholar
  30. Medeiros MA, Boas GLV, Vilela NJ, Carrijo OA (2009) A preliminary survey on the biological control of south American tomato pinworm with the parasitoid Trichogramma pretiosum in greenhouse models. Hortic Bras 27:80–85CrossRefGoogle Scholar
  31. Mills NJ, Lacan I (2004) Ratio dependence in the functional response of insect parasitoids: evidence from Trichogramma minutum foraging for eggs in small host patches. Ecol Entomol 29:208–216CrossRefGoogle Scholar
  32. Moezipour M, Kafil M, Allahyari H (2008) Functional response of Trichogramma brassicae at different temperatures and relative humidities. Bull Insectol 61:245–250Google Scholar
  33. Parra JRP, Zucchi RA (2004) Trichogramma in Brazil: feasibility of use after 20 years of research. Neotrop Entomol 33:271–281CrossRefGoogle Scholar
  34. Pizzol J, Pintureau B, Khoualdia O, Desneux N (2010) Temperature-dependent differences in biological traits between two strains of Trichogramma cacoeciae (Hymenoptera: Trichogrammatidae). J Pest Sci 83(4):447–452CrossRefGoogle Scholar
  35. Pizzol J, Desneux N, Wajnberg E, Thiery D (2012) Parasitoid and host egg ages have independent impact on various biological traits in a Trichogramma species. J Pest Sci 85:489–496CrossRefGoogle Scholar
  36. Polaszek A, Paul F, Jones R, Stouthamer R, Hernandez-Suarez E, Cabello T, Perez M (2012) Molecular and morphological diagnoses of five species of Trichogramma: biological control agents of Chrysodeixis chalcites (Lepidoptera: Noctuidae) and Tuta absoluta (Lepidoptera: Gelechiidae) in the Canary Islands. BioControl 57:21–35CrossRefGoogle Scholar
  37. Poncio S, Montoya P, Cancino J, Nava DE (2016) Determining the functional response and mutual interference of Utetes anastrephae (Hymenoptera: Braconidae) on Anastrepha oblique (Diptera: Tephritidae) larvae for mass rearing purposes. An Entomol Soc Am 109:518–525CrossRefGoogle Scholar
  38. Pratissoli D, Thuler RT, Andrade GS, Zanotti LCM, da Silva AF (2005) Estimate of Trichogramma pretiosum to control Tuta absoluta in stalked tomato. Pesq Agrop Brasileira 40:715–718CrossRefGoogle Scholar
  39. Puneeth P, Vijayan VA (2014) Parasitization capacity of Trichogramma chilonis Ishii (Hymenoptera: Trichogrammatidae) on the eggs of Helicoverpa armigera (Lepidoptera: Noctuidae) under laboratory conditions. Int J Sci Nat 5:462–465Google Scholar
  40. Roditakis E, Skarmoutsou C, Staurakaki M (2013) Toxicity of insecticides to populations of tomato borer Tuta absoluta (Meyrick) from Greece. Pest Manag Sci 69:834–840PubMedCrossRefPubMedCentralGoogle Scholar
  41. Roditakis E, Vasakis EA, Grispou M, Stavrakaki M, Nauen R, Gravouil M, Bassi A (2015) First report of T. absoluta resistence to diamide insecticides. J Pest Sci 88:9–16CrossRefGoogle Scholar
  42. Shao JB, Liu S, Yu YZ, Liu YQ (2010) Functional response of Eretmocerus hayati to two biotypes of the whitefly, Bemisia tabaci. J Environ Entomol 32:73–77Google Scholar
  43. Sharma PL, Gavkare O (2017) New distributional and record of invasive pest, T. absoluta (Meyrick) in North Western Himalayan region of India. Nat Acad Sci Lett 40:217–220CrossRefGoogle Scholar
  44. Shashank PR, Chandrashekar K, Meshram NM, Sreedevi K (2015) Occurrence of Tuta absoluta (Gelechiidae: Lepidoptera) an invasive pest from India. Indian J Entomol 77:323–329Google Scholar
  45. Sheoran OP, Tonk DS, Kaushik LS, Hasija RC, Pannu RS (1998) Statistical software package for agricultural research workers. Recent advances in information theory, statistics & computer applications by D.S. Hooda & R.C. Hasija Department of Mathematics Statistics, CCS HAU, Hisar (139-143)Google Scholar
  46. Sohani NZ, Shishehbor P, Kocheili F (2008) Functional and numerical responses of Eretmocerus mundus Mercet (Hymenoptera: Aphelinidae) parasitizing cotton whitefly, Bemisia tabaci Gennadius (Homoptera: Aleyrodidae). Pak J Biol Sci 11:1015–1020PubMedCrossRefPubMedCentralGoogle Scholar
  47. Sridhar V, Chakravarthy AK, Asokan R, Vinesh LS, Rebijith KB, Vennila S (2014) New records of invasive south American tomato leaf miner, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) in India. Pest Manag Hort Ecosyst 20:148–154Google Scholar
  48. van Lenteren, J (2012a) IOBC internet book of biological control. Version6. http://www.iobcglobal.org/download/IOBC_InternetBookBiCoVersion6Spring2012.pdf. Accessed 20 Jan 2016
  49. van Lenteren J (2012b) The state of commercial augmentative biological control: plenty of natural enemies, but a frustrating lack of uptake. BioControl 57:71–84CrossRefGoogle Scholar
  50. van Lenteren JC, Hemerik L, Lins JC, Bueno VHP (2016) Functional responses of three neotropical mirids predator to eggs of Tuta absoluta on tomato. Insects 7:34PubMedCentralCrossRefGoogle Scholar
  51. Wang B, Ferro DN (1998) Functional response of Trichogramma ostriniae (Hymenoptera: Trichogrammatidae) to Ostrinia nubilalis (Lepidoptera: Pyralidae) under laboratory and field conditions. Environ Entomol 27:752–758CrossRefGoogle Scholar
  52. Xu HY, Yang W, Duan M, Wan FH (2014) Functional response, host stage preference and interference of two whitefly parasitoids. Insect Sci 23:134–144CrossRefGoogle Scholar
  53. Zappala L, Bernardo U, Biond A, Cocco A, Deliperi S (2012) Recruitment of native parasitoids by the exotic pest Tuta absoluta (Meyrick) in southern Italy. Bull Insectol 65:51–61Google Scholar

Copyright information

© African Association of Insect Scientists 2019

Authors and Affiliations

  • T. N. Manohar
    • 1
  • P. L. Sharma
    • 1
    Email author
  • S. C. Verma
    • 1
  • K. C. Sharma
    • 1
  • R. S. Chandel
    • 1
  1. 1.Department of EntomologyUniversity of Horticulture and ForestrySolanIndia

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