Skip to main content
Log in

Fortuitous parasitoids of the invasive tomato leafminer Tuta absoluta in Tunisia

  • Published:
Phytoparasitica Aims and scope Submit manuscript

Abstract

The South American tomato leafminer, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae), is a major threat to tomato (Solanum lycopersicum L.) crops. After its first detection in Spain in 2006, it spread rapidly through the Western Palaearctic region, arriving in Tunisia 2 years later. The aim of this research was to assess whether generalist indigenous parasitoids are adapting to this exotic host in Tunisian tomato crops. For this, we conducted a survey in four Tunisian tomato-growing areas by sampling infested leaves of tomato and solanaceous weeds and exposing artificially infested sentinel plants. Two ectoparasitoid species were found attacking and developing on T. absoluta: Bracon sp. (Hymenoptera: Braconidae) and Necremnus sp. nr artynes (Hymenoptera: Eulophidae), whereas no egg or pupal parasitoids were found. The eulophid wasp was the most abundant with a peak of apparent parasitism rate of 25.5%. It emerged from parasitized T. absoluta young larvae in exposed sentinel plants and in sampled infested tomato leaves, both in greenhouse and open field cultivations. Bracon sp. showed a gregarious development on T. absoluta mature larvae and it was collected only on sentinel plants exposed in the Ragueda (Kiarouan) site, with 10.23% of estimated parasitism. Although further research is still needed to assess properly the ecological role of these parasitoids in the biological control of T. absoluta, this study represents the first step toward establishing the scientific basis for including these parasitoids in the Tunisian IPM and biological programs against this pest.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Abbes, K., & Chermiti, B. (2012). Failure of the biological control of Tuta absoluta using the predator Nesidiocoris tenuis in a protected tomato crop: analysis of factors. IOBC/WPRS Bulletin, 80, 231–236.

    Google Scholar 

  • Ali, A., Ahmad, F., Biondi, A., Wang, Y., & Desneux, N. (2012). Potential for using Datura alba leaf extracts against two major stored grain pests, the khapra beetle Trogoderma granarium and the rice weevil Sitophilus oryzae. Journal of Pest Science, 85, 359–366.

    Article  Google Scholar 

  • Biondi, A., Chailleux, A., Lambion, J., Han, P., Zappalà, L., & Desneux, N. (2013a). Indigenous natural enemies attacking Tuta absoluta (Lepidoptera: Gelechiidae) in Southern France. Egyptian Journal of Biological Pest Control, 23, 117–121.

    Google Scholar 

  • Biondi, A., Desneux, N., Amiens-Desneux, E., Siscaro, G., & Zappalà, L. (2013b). Biology and developmental strategies of the Palaearctic parasitoid Bracon nigricans on the Neotropical moth Tuta absoluta. Journal of Economic Entomology, 106, 1638–1647.

    Google Scholar 

  • Biondi, A., Desneux, N., Siscaro, G., & Zappalà, L. (2012a). Using organic-certified rather than synthetic pesticides may not be safer for biological control agents: selectivity and side effects of 14 pesticides on the predator Orius laevigatus. Chemosphere, 87, 803–812.

    Article  CAS  PubMed  Google Scholar 

  • Biondi, A., Mommaerts, V., Smagghe, G., Vinuela, E., Zappalà, L., & Desneux, N. (2012b). The non-target impact of spinosyns on beneficial arthropods. Pest Management Science, 68, 1523–1536.

    Article  CAS  PubMed  Google Scholar 

  • Bompard, A., Jaworski, C. C., & Desneux, N. (2013). Sharing a predator: can an invasive species affect the predation pressure on a local pest? Population Ecology, 55, 433–440.

    Article  Google Scholar 

  • Boualem, M., Allaoui, H., Hamadi, R., & Medjahed, M. (2012). Biologie et complexe des ennemis naturels de Tuta absoluta à Mostaganem (Algérie). EPPO Bulletin, 42, 268–274.

    Article  Google Scholar 

  • Boucěk, Z. (1958). A study of central European Eulophidae, I: Eulophinae (Hymenoptera). Sborník Entomologického Oddeleni Národního Muzea Praze, 33, 117–170.

    Google Scholar 

  • Burks, R. A. (2003). Key to the Nearctic genera of Eulophidae, subfamilies: Entedoninae, Euderinae, and Eulophinae (Hymenoptera Chalcidoidea). http://cache.ucr.edu/%7Eheraty/Eulophidae/. Accessed 27 August 2012.

  • Cagnotti, C. L., Viscarret, M. M., Riquelme, M. B., Botto, E. N., Carabajal, L. Z., Segura, D. F., et al. (2012). Effects of X-rays on Tuta absoluta for use in inherited sterility programmes. Journal of Pest Science, 85, 413–421.

    Article  Google Scholar 

  • Caparros Megido, R., Haubruge, E., & Verheggen, F. J. (2012). First evidence of deuterotokous parthenogenesis in the tomato leafminer, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). Journal of Pest Science, 85, 409–412.

    Article  Google Scholar 

  • Chailleux, A., Desneux, N., Seguret, J., Do Thi Khanh, H., Maignet, P., & Tabone, E. (2012). Assessing European egg parasitoids as a means of controlling the invasive South American tomato pinworm Tuta absoluta. PLoS ONE, 7, e48068. doi:10.1371/journal.pone.0048068.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chailleux, A., Bearez, P., Pizzol, J., Amiens-Desneux, E., Ramirez-Romero, R., & Desneux, N. (2013). Potential for combined use of parasitoids and generalist predators for biological control of the key invasive tomato pest Tuta absoluta. Journal of Pest Science, 86, 533–541.

    Google Scholar 

  • Chermiti, B., Abbes, K., Aoun, M., Ben Othmen, S., Ouhibi, M., et al. (2009). First estimate of the damage of T. absoluta (Povolny) (Lepidoptera: Gelechiidae) and evaluation of the efficiency of sex pheromone traps in greenhouses of tomato crops in the Bekalta region, Tunisia. African Journal of Plant Science and Biotechnology, 3, 49–52.

    Google Scholar 

  • Cocco, A., Deliperi, S., & Delrio, G. (2012). Control of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) in greenhouse tomato crops using the mating disruption technique. Journal of Applied Entomology, 137, 16–28.

    Article  Google Scholar 

  • Cornell, H. V., & Hawkins, B. A. (1993). Accumulation of native parasitoid species on introduced herbivores: a comparison of hosts as natives and hosts as invaders. American Naturalist, 141, 847–865.

    Article  CAS  PubMed  Google Scholar 

  • Desneux, N., Barta, R. J., Hoelmer, K. A., Hopper, K. R., & Heimpel, G. E. (2009). Multifaceted determinants of host specificity in an aphid parasitoid. Oecologia, 160, 387–398.

    Article  PubMed  Google Scholar 

  • Desneux, N., Blahnik, R., Delebecque, C. J., & Heimpel, G. E. (2012). Host phylogeny and specialisation in parasitoids. Ecology Letters, 15, 453–460.

    Article  PubMed  Google Scholar 

  • Desneux, N., Decourtye, A., & Delpuech, J. M. (2007). The sublethal effects of pesticides on beneficial arthropods. Annual Review of Entomology, 52, 81–106.

    Article  CAS  PubMed  Google Scholar 

  • Desneux, N., Luna, M. G., 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. Journal of Pest Science, 84, 403–408.

    Article  Google Scholar 

  • Desneux, N., Wajnberg, E., Wyckhuys, K. A. G., Burgio, G., Arpaia, S., et al. (2010). Biological invasion of European tomato crops by Tuta absoluta: ecology, geographic expansion and prospects for biological control. Journal of Pest Science, 83, 197–215.

    Article  Google Scholar 

  • El Arnaouty, A., & Kortam, M. N. (2012). First record of the mirid predatory species, Nesidiocoris tenuis Reuter (Heteroptera: Miridae) on the tomato leafminer, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) in Egypt. Egyptian Journal of Biological Pest Control, 22, 223–224.

    Google Scholar 

  • EPPO (2009). First record of Tuta absoluta in Tunisia. EPPO reporting service 3(042), 2, 2009.

  • Ferracini, C., Ingegno, B. L., Navone, P., Ferrari, E., Mosti, M., et al. (2012). Adaptation of indigenous larval parasitoids to Tuta absoluta (Lepidoptera: Gelechiidae) in Italy. Journal of Economic Entomology, 105, 1311–1319.

    Article  PubMed  Google Scholar 

  • Gontijo, P. C., Picanço, M. C., Pereira, E. J. G., Martins, J. C., Chediak, M., & Guedes, R. N. C. (2013). Spatial and temporal variation in the control failure likelihood of the tomato leaf miner, Tuta absoluta. Annals of Applied Biology, 162, 50–59.

    Article  Google Scholar 

  • Guedes, R. N. C., & Picanço, M. C. (2012). The tomato borer Tuta absoluta in South America: pest status, management and insecticide resistance. EPPO Bulletin, 42, 211–216.

    Article  Google Scholar 

  • Lietti, M. M. M., Bott, E., & Alzogara, R. (2005). Insecticide resistance in Argentine populations of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). Neotropical Entomology, 34, 113–119.

    Article  Google Scholar 

  • Loni, A., Rossi, E., & van Achterberg, K. (2011). First report of Agathis fuscipennis in Europe as parasitoid of the tomato leafminer Tuta absoluta. Bulletin of Insectology, 64, 115–117.

    Google Scholar 

  • Luna, M. G., Sánchez, N. E., Pereyra, P. C., Nieves, E., Savino, V., Luft, E., et al. (2012). Biological control of Tuta absoluta in Argentina and Italy: evaluation of indigenous insects as natural enemies. EPPO Bulletin, 42, 260–267.

    Article  Google Scholar 

  • Maciel, G. M., Maluf, W. R., Silva, V. d. F., Goncalves Neto, A. C., & Augusto Gomes, L. A. (2011). Pre-commercial hybrids obtained from an acylsugar-rich tomato inbred line, resistant to Tuta absoluta. Horticultura Brasileira, 29, 151–156.

    Article  Google Scholar 

  • Miranda, M. M. M., Picanco, M., Zanuncio, J. C., & Guedes, R. N. C. (1998). Ecological life table of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). Biocontrol Science and Technology, 8, 597–606.

    Article  Google Scholar 

  • Mollá, O., González-Cabrera, J., & Urbaneja, A. (2011). The combined use of Bacillus thuringiensis and Nesidiocoris tenuis against the tomato borer Tuta absoluta. Biocontrol, 56, 883–891.

  • Silva, G. A., Picanco, M. C., Bacci, L., Crespo, A. L., Rosado, J. F., & Guedes, R. N. C. (2011). Control failure likelihood and spatial dependence of insecticide resistance in the tomato pinworm, Tuta absoluta. Pest Management Science, 67, 91–920.

    Article  Google Scholar 

  • Stansly, P. A., Schuster, D. J., & Liu, T.-X. (1997). Apparent parasitism of Bemisia argentifolii (Homoptera: Aleyrodidae) by Aphelinidae (Hymenoptera) on vegetable crops and associated weeds in South Florida. Biological Control, 9, 49–57.

    Article  Google Scholar 

  • Tomé, H. V. V., Cordeiro, E. M. G., Rosado, J. F., & Guedes, R. N. C. (2012). Egg exposure to pyriproxyfen in the tomato leaf miner Tuta absoluta: ovicidal activity or behavioural-modulated hatching mortality? Annals of Applied Biology, 160, 35–42.

    Article  Google Scholar 

  • Tropea Garzia, G., Siscaro, G., Biondi, A., & Zappalà, L. (2012). Tuta absoluta, an exotic invasive pest from South America now in the EPPO region: biology, distribution and damage. EPPO Bulletin, 42, 205–210.

    Article  Google Scholar 

  • Urbaneja, A., González-Cabrera, J., Arnó, J., & Gabarra, R. (2012). Prospects for the biological control of Tuta absoluta in tomatoes of the Mediterranean basin. Pest Management Science, 68, 1215–1222.

    Article  CAS  PubMed  Google Scholar 

  • Urbaneja, A., Vercher, R., Navarro, V., Porcuna, J. L., & Garcia-Marí, F. (2007). La polilla del tomate, Tuta absoluta. Phytoma España, 194, 16–24.

    Google Scholar 

  • Weisenburger, D. D. (1993). Human health-effects of agrichemical use. Human Pathology, 24, 571–576.

    Article  CAS  PubMed  Google Scholar 

  • Wharton, R. A. (1993). Bionomics of the Braconidae. Annual Review of Entomology, 38, 121–143.

    Article  Google Scholar 

  • Yu, D. S. K., & van Achterberg, K. (2010). Taxapad Ichneumonoidea (May 2009 version). In: Species 2000 & IT IS catalogue of life: 2010 annual checklist - DVD, Species 2000, Reading, UK.

  • Zappalà, L., Bernardo, U., Biondi, A., Cocco, A., Deliperi, S., et al. (2012a). Recruitment of native parasitoids by the exotic pest Tuta absoluta (Meyrick) in southern Italy. Bulletin of Insectology, 65, 51–61.

    Google Scholar 

  • Zappalà, L., Campolo, O., Grande, S., Saraceno, F., Biondi, A., Siscaro, G., et al. (2012b). Dispersal of Aphytis melinus (Hymenoptera: Aphelinidae) after augmentative releases in citrus orchards. European Journal of Entomology, 109, 561–568.

    Article  Google Scholar 

  • Zappalà, L., Siscaro, G., Biondi, A., Mollà, O., Gonzàlez-Cabrera, J., & Urbaneja, A. (2012c). Efficacy of sulphur on Tuta absoluta and its side effects on the predator Nesidiocoris tenuis. Journal of Applied Entomology, 136, 401–409.

    Article  Google Scholar 

Download references

Acknowledgments

The authors wish to thank Dr. U. Bernardo (CNR – IPP, Naples, Italy) for confirming the identification of Necremnus sp. nr artynes; the Tunisian Ministry of Agriculture and the Tunisian Ministry of High Education and Scientific Research for funding AK and BC, and the University of Catania for funding AB (Ph.D. grant).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Brahim Chermiti.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Abbes, K., Biondi, A., Zappalà, L. et al. Fortuitous parasitoids of the invasive tomato leafminer Tuta absoluta in Tunisia. Phytoparasitica 42, 85–92 (2014). https://doi.org/10.1007/s12600-013-0341-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12600-013-0341-x

Keywords

Navigation