Skip to main content
SpringerLink
Log in

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

  • Original Research Article
  • Published:
International Journal of Tropical Insect Science Aims and scope Submit manuscript

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.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Arturo C, Salvatore D, Gavino D (2012) Integrated control in protected crops. MeditClim Int Org Biol Integ ContWest Palaearc Reg Sec Bull 80:319–324

  • 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 110:2155–2159

    Google Scholar 

  • Bielza P (2010) La resistencia a insecticidas en Tuta absoluta. Phytoma 217:103–106

    Google Scholar 

  • 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 63:239–258

    CAS  PubMed  Google Scholar 

  • Bueno RCOF, Parra JRP, Bueno AF, Haddad ML (2009) Desempenho de tricogramatídeos comopotenciais agentes de controle de Pseudoplusia includens Walker (Lepidoptera: Noctuidae). Neotrop Entomol 38:389–394

    PubMed  Google Scholar 

  • 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 49:219–223

    Google Scholar 

  • 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 90:787–796

    Google Scholar 

  • 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):e48068

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 86:533–543

    Google Scholar 

  • 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 106:2310–2321

    PubMed  Google Scholar 

  • 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 83:197–215

    Google Scholar 

  • 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 84:403–408

    Google Scholar 

  • 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 56:1–5

    Google Scholar 

  • 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):801–809

    Google Scholar 

  • 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 29:85–93

    Google Scholar 

  • 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 38:1504–1509

    Google Scholar 

  • 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 10:1–11

    Google Scholar 

  • 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 23:41–45

    Google Scholar 

  • Fernandez-Arhex V, Corley JC (2003) The functional response of parasitoids and its implications for biological control. Biocont Sci Technol 13:403–413

    Google Scholar 

  • Holling CS (1959) Some characteristics of simple types of predation and parasitism. Can Entomol 91:385–398

    Google Scholar 

  • 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 67:246–252

    Google Scholar 

  • 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 118:229–236

    Google Scholar 

  • 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 213–227

    Google Scholar 

  • 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 98:970–971

    Google Scholar 

  • 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 32:164–171

    Google Scholar 

  • Karimian Z (1998) Bioecology of Trichogramma brassicae in paddy fields of Guilan province. M.Sc. Thesis. Faculty of Agriculture. University of Guilan, Iran 99p

  • Lietti MMM, Botto E, Alzogaray RA (2005) Insecticide resistance in argentine populations of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). Neotrop Entomol 34:113–119

    Google Scholar 

  • 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 42:260–267

    Google Scholar 

  • 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 24:247–256

    Google Scholar 

  • 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 27:80–85

    Google Scholar 

  • 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 29:208–216

    Google Scholar 

  • Moezipour M, Kafil M, Allahyari H (2008) Functional response of Trichogramma brassicae at different temperatures and relative humidities. Bull Insectol 61:245–250

    Google Scholar 

  • Parra JRP, Zucchi RA (2004) Trichogramma in Brazil: feasibility of use after 20 years of research. Neotrop Entomol 33:271–281

    Google Scholar 

  • 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):447–452

    Google Scholar 

  • 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 85:489–496

    Google Scholar 

  • 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 57:21–35

    Google Scholar 

  • 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 109:518–525

    Google Scholar 

  • 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 40:715–718

    Google Scholar 

  • 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 5:462–465

    Google Scholar 

  • Roditakis E, Skarmoutsou C, Staurakaki M (2013) Toxicity of insecticides to populations of tomato borer Tuta absoluta (Meyrick) from Greece. Pest Manag Sci 69:834–840

    CAS  PubMed  Google Scholar 

  • 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 88:9–16

    Google Scholar 

  • 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 32:73–77

    Google Scholar 

  • 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 40:217–220

    CAS  Google Scholar 

  • Shashank PR, Chandrashekar K, Meshram NM, Sreedevi K (2015) Occurrence of Tuta absoluta (Gelechiidae: Lepidoptera) an invasive pest from India. Indian J Entomol 77:323–329

  • 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)

  • 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 11:1015–1020

    PubMed  Google Scholar 

  • 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 20:148–154

    Google Scholar 

  • van Lenteren, J (2012a) IOBC internet book of biological control. Version6. http://www.iobcglobal.org/download/IOBC_InternetBookBiCoVersion6Spring2012.pdf. Accessed 20 Jan 2016

  • van Lenteren J (2012b) The state of commercial augmentative biological control: plenty of natural enemies, but a frustrating lack of uptake. BioControl 57:71–84

    Google Scholar 

  • 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 7:34

    PubMed Central  Google Scholar 

  • Wang B, Ferro DN (1998) Functional response of Trichogramma ostriniae (Hymenoptera: Trichogrammatidae) to Ostrinia nubilalis (Lepidoptera: Pyralidae) under laboratory and field conditions. Environ Entomol 27:752–758

    Google Scholar 

  • Xu HY, Yang W, Duan M, Wan FH (2014) Functional response, host stage preference and interference of two whitefly parasitoids. Insect Sci 23:134–144

    Google Scholar 

  • 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 65:51–61

    Google Scholar 

Download references

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.

Author information

Authors and Affiliations

  1. Department of Entomology, University of Horticulture and Forestry, Nauni, Solan, HP, 173 230, India

    T. N. Manohar, P. L. Sharma, S. C. Verma, K. C. Sharma & R. S. Chandel

Authors
  1. T. N. Manohar
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. P. L. Sharma
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. S. C. Verma
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. K. C. Sharma
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. R. S. Chandel
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to P. L. Sharma.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

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

Manohar, T.N., Sharma, P.L., Verma, S.C. et al. Functional response of indigenous Trichogramma spp. to invasive tomato leafminer, Tuta absoluta (Meyrick) under laboratory conditions. Int J Trop Insect Sci 40, 101–107 (2020). https://doi.org/10.1007/s42690-019-00057-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s42690-019-00057-y

Keywords

Search

Navigation