Biological control of Tuta absoluta through releases of Trichogramma cacoeciae parasitoids and Macrolophus pygmaeus predators in northeastern Tunisian greenhouses

References

• Agamy, E. A. (1994). Comparative studies on three species of Trichogramma for controlling the European corn borer, Ostrinia nubilalis Hübner (Lepidoptera: Crambidae) [Ph.D. Thesis]. Cairo University, Faculty of Agriculture.
   Google Scholar
• Arnó, J., & Gabarra, R. (2011). Side effects of selected insecticides on the Tuta absoluta (Lepidoptera: Gelechiidae) predators Macrolophus pygmaeus and Nesidiocoris tenuis (Hemiptera: Miridae). Journal of Pest Science, 84(4), 513–520. https://doi.org/10.1007/s10340-011-0384-z
   Web of Science ®Google Scholar
• Biondi, A., Desneux, N., Siscaro, G., & Zappalà, L. (2012). 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(7), 803–812. https://doi.org/10.1016/j.chemosphere.2011.12.082
   PubMed Web of Science ®Google Scholar
• Biondi, A., Guedes, R. N. C., Wan, F. H., & Desneux, N. (2018). Ecology, worldwide spread and management of the invasive South American tomato pinworm, Tuta absoluta: Past, present and future. Annual Review of Entomology, 63(1), 239–258. https://doi.org/10.1146/annurev-ento-031616-034933
   PubMedGoogle Scholar
• Cabello, T., Gallego, J. R., Vila, E., Soler, A., del Pino, M., Carnero, A., Hernandez- Suarez, E., & Polaszek, A. (2009). Biological control of the South American tomato pinworm, Tuta absoluta (Lep.: Gelechiidae), with releases of Trichogramma achaeae (Hym.: Trichogrammatidae) in tomato greenhouses of Spain. IOBC WPRS Bulletin, 49, 225–230.
   Google Scholar
• Campolo, O., Cherif, A., Ricupero, M., Siscaro, G., Grissa-Lebdi, K., Russo, A., Cucci, L. M., Di Pietro, P., Satriano, C., Desneux, N., & Biondi, A. (2017). Citrus peel essential oil nanoformulations to control the tomato borer, Tuta absoluta: Chemical properties and biological activity. Scientific Reports, 7(1), 13036. https://doi.org/10.1038/s41598-017-13413-0
   PubMedGoogle Scholar
• Campos, M. R., Biondi, A., Adiga, A., Guedes, R. N. C., & Desneux, N. (2017). From the Western Palaearctic region to beyond: Tuta absoluta ten years after invading Europe. Journal of Pest Science, 90(3), 787–796. https://doi.org/10.1007/s10340-017-0867-7
   Web of Science ®Google Scholar
• Chailleux, A., Biondi, A., Han, P., Tabone, E., & Desneux, N. (2013). Suitability of the pest–plant system Tuta absoluta (Lepidoptera: Gelechiidae). tomato for Trichogramma (Hymenoptera: Trichogrammatidae) parasitoids and insights for biological control. Journal of Economic Entomology, 106(6), 2310–2321. https://doi.org/10.1603/EC13092
   PubMed Web of Science ®Google Scholar
• Chailleux, A., Desneux, N., Seguret, J., Khanh, H. D. T., 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. https://doi.org/10.1371/journal.pone.0048068
   PubMed Web of Science ®Google Scholar
• Cherif, A., Mansour, R., Barhoumi-Attia, S., Zappalà, L., & Grissa-Lebdi, K. (2019). Effectiveness of different release rates of Trichogramma cacoeciae (Hymenoptera: Trichogrammatidae) against Tuta absoluta (Lepidoptera: Gelechiidae) in protected and open field tomato crops in Tunisia. Biocontrol Science and Technology, 29(2), 149–161. https://doi.org/10.1080/09583157.2018.1542485
   Web of Science ®Google Scholar
• Cherif, A., Mansour, R., & Grissa-Lebdi, K. (2013). Biological aspects of tomato leafminer Tuta absoluta (Lepidoptera: Gelechiidae) in conditions of Northeastern Tunisia: Possible implications for pest management. Environmental and Experimental Biology, 11, 179–184.
   Google Scholar
• Cherif, A., Mansour, R., & Grissa-Lebdi, K. (2021). The egg parasitoids Trichogramma: From laboratory mass rearing to biological control of lepidopteran pests. Biocontrol Science and Technology, 31(7), 661–693. https://doi.org/10.1080/09583157.2020.1871469
   Web of Science ®Google Scholar
• Cocco, A., Deliperi, S., & Delrio, G. (2013). Control of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) in greenhouse tomato crops using the mating disruption technique. Journal of Applied Entomology, 137(1-2), 16–28. https://doi.org/10.1111/j.1439-0418.2012.01735.x
   Web of Science ®Google Scholar
• Desneux, N., Han, P., Mansour, R., Arnó, J., Brévault, T., Campos, M. R., Chailleux, A., Guedes, R. N., Karimi, J., Konan, K. A. J., & Lavoir, A. V. (2022). Integrated pest management of Tuta absoluta: Practical implementations across different world regions. Journal of Pest Science, 95(1), 17–39. https://doi.org/10.1007/s10340-021-01442-8
   Web of Science ®Google Scholar
• Desneux, N., Wajnberg, E., Wyckhuys, K. A. G., Burgio, G., Arpaia, S., Narvaez-Vasquez, C. A., 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. Journal of Pest Science, 83(3), 197–215. https://doi.org/10.1007/s10340-010-0321-6
   Web of Science ®Google Scholar
• El-Arnaouty, S. A., Pizzol, J., Galal, H. H., Kortam, M. N., Afifi, A. I., Beyssat, V., Desneux, N., Biondi, A., & Heikal, I. H. (2014). Assessment of two Trichogramma species for the control of Tuta absoluta in North African tomato greenhouses. African Entomology, 22(4), 801–809. https://doi.org/10.4001/003.022.0410
   Web of Science ®Google Scholar
• Ettaib, R., Aoun, F., Assadi, B., Ben Belgacem, A., Chouikhi, S., & BelKadhi, M. S. (2019). Comparison of strains of Nesidiocoris tenuis against Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) under geothermal greenhouses in southern Tunisia. Journal of Oasis Agriculture and Sustainable Development, 1(1), 23–26. https://doi.org/10.56027/JOASD.042019
   Google Scholar
• Ferracini, C., Bueno, V. H. P., Dindo, M. L., Ingegno, B. L., Luna, M. G., Gervassio, N. G. S., Sanchez, N. E., Siscaro, G., van Lenteren, J. C., Zappalà, L., & Tavella, L. (2019). Natural enemies of Tuta absoluta in the Mediterranean basin. Europe and South America. Biocontrol Science and Technology, 29, 578–609. https://doi.org/10.1080/09583157.2019.1572711
   Google Scholar
• Gomez, K. A., & Gomez, A. A. (1984). Statistical procedures for agricultural research (2nd ed.). Wiley.
   Google Scholar
• Guedes, R. N. C., & Picanco, M. C. (2012). The tomato borer Tuta absoluta in South America: Pest status, management and insecticide resistance. EPPO Bulletin, 42(2), 211–216. https://doi.org/10.1111/epp.2557
   Google Scholar
• Guedes, R. N. C., Roditakis, E., Campos, M. R., Haddi, K., Bielza, P., Siqueira, H. A. A., Tsagkarakou, A., Vontas, J., & Nauen, R. (2019). Insecticide resistance in the tomato pinworm Tuta absoluta: Patterns, spread, mechanisms, management and outlook. Journal of Pest Science, 92(4), 1329–1342. https://doi.org/10.1007/s10340-019-01086-9
   Web of Science ®Google Scholar
• Haddi, K., Berger, M., Bielza, P., Rapisarda, C., Williamson, M. S., Moores, G., & Bass, C. (2017). Mutation in the ace-1 gene of the tomato leaf miner (Tuta absoluta) associated with organophosphates resistance. Journal of Applied Entomology, 141(8), 612–619. https://doi.org/10.1111/jen.12386
   Web of Science ®Google Scholar
• Han, P., Bayram, Y., Shaltiel-Harpaz, L., Sohrabi, F., Saji, A., Tair Esenali, U., Jalilov, A., Ali, A., Shashank, P. R., Ismoilov, K., Lu, Z. Z., Wang, S., Zhang, G. F., Wan, F. H., Biondi, A., & Desneux, N. (2019). Tuta absoluta continues to disperse in Asia: Damage, ongoing management and future challenges. Journal of Pest Science, 92(4), 1317–1327. https://doi.org/10.1007/s10340-018-1062-1
   Web of Science ®Google Scholar
• Huang, J., Hua, H.-Q., Zhang, F., & Li, Y.-X. (2018). Suitability assessment of three Trichogramma species in the control of Mythimna separate (Lepidoptera: Noctuidae). Journal of Applied Entomology, 142(1-2), 131–140. https://doi.org/10.1111/jen.12414
   Web of Science ®Google Scholar
• Ingegno, B. L., Messelink, G. J., Bodino, N., Iliadou, A., Driss, L., Woelke, J. B., Leman, A., & Tavella, L. (2019). Functional response of the mirid predators Dicyphus bolivari and Dicyphus errans and their efficacy as biological control agents of Tuta absoluta on tomato. Journal of Pest Science, 92(4), 1457–1466. https://doi.org/10.1007/s10340-019-01079-8
   Web of Science ®Google Scholar
• Khanh, H. D. T., Chailleux, A., Tiradon, M., Desneux, N., Colombel, E., & Tabone, E. (2012). Using new egg parasitoids (trichogramma spp.) to improve integrated management against Tuta absoluta. EPPO Bulletin, 42(2), 249–254. https://doi.org/10.1111/epp.2562
   Google Scholar
• Kortam, M. N., El-Arnaouty, S. A., Afifi, A. I., & Heikal, I. H. (2014). Efficacy of different biological methods for controlling the tomato leaf miner, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) on tomato in greenhouse in Egypt. Egyptian Journal of Biological Pest Control, 24, 523–528.
   Web of Science ®Google Scholar
• Leite, G. L. D., Picanço, M., Azevedo, A. A., & Gonring, A. H. R. (1999). Efeito de tricomas, aleloquímicos e nutrients na resistência de Lycopersicon hirsutumà traça-do-tomateiro. Pesquisa Agropecuaria Brasileira, 34(11), 2059–2064. https://doi.org/10.1590/S0100-204X1999001100012
   Google Scholar
• Mansour, R., & Biondi, A. (2021). Releasing natural enemies and applying microbial and botanical pesticides for managing Tuta absoluta in the MENA region. Phytoparasitica, 49(2), 179–194. https://doi.org/10.1007/s12600-020-00849-w
   Web of Science ®Google Scholar
• Mansour, R., Brevault, T., Chailleux, A., Cherif, A., Grissa-Lebdi, K., Haddi, K., Mohamed, S. A., Nofemela, R. S., Oke, A., Sylla, S., Tonnang, H. E. Z., Zappala, L., Kenis, M., Desneux, N., & Biondi, A. (2018). Occurrence, biology, natural enemies and management of Tuta absoluta in Africa. Entomologia Generalis, 38(2), 83–112. https://doi.org/10.1127/entomologia/2018/0749
   Web of Science ®Google Scholar
• Mansour, R., Cherif, A., Attia-Barhoumi, S., Zappala, L., & Grissa-Lebdi, K. (2019). Tuta absoluta in Tunisia: Ten years of invasion and pest management. Phytoparasitica, 47(4), 461–474. https://doi.org/10.1007/s12600-019-00748-9
   Web of Science ®Google Scholar
• Mirhosseini, M. A., Fathipour, Y., Soufbaf, M., & Reddy, G. V. P. (2019). Implications of using two natural enemies of Tuta absoluta (Lepidoptera: Gelechiidae) toward tomato yield enhancement. Bulletin of Entomological Research, 109(5), 617–625. https://doi.org/10.1017/S0007485318000998
   PubMed Web of Science ®Google Scholar
• Mollá, O., Montón, H., Vanaclocha, P., Beitia, F., & Urbaneja, A. (2009). Predation by the mirids Nesidiocoris tenuis and Macrolophus pygmaeus on the tomato borer Tuta absoluta. IOBC/WPRS Bulletin, 49, 209–214.
   Google Scholar
• Nannini, M., Atzori, F., Murgia, G., Pisci, R., & Sanna, F. (2012). Use of predatory mirids for control of the tomato borer Tuta absoluta (Meyrick) in Sardinian greenhouse tomatoes. EPPO Bulletin, 42(2), 255–259. https://doi.org/10.1111/epp.2563
   Google Scholar
• Oliveira, L., Durao, A. C., Fontes, J., Roja, I. S., & Tavares, J. (2017). Potential of Trichogramma achaeae (Hymenoptera: Trichogrammatidae) in biological control of Tuta absoluta (Lepidoptera: Gelechiidae) in Azorean greenhouse tomato crop. Journal of Economic Entomology, 110(5), 2010–2015. https://doi.org/10.1093/jee/tox197
   PubMed Web of Science ®Google Scholar
• Roditakis, E., Vasakis, E., Garcia-Vidal, L., Martinez-Aguirre Rison, M. D. R. J. L., Jean Luc, R., Odile Haxaire-Lutun, M., Nauen, R., Tsagkarakou, A., & Bielza, P. (2018). A four-year survey on insecticide resistance and likelihood of chemical control failure for tomato leaf miner Tuta absoluta in the European/Asian region. Journal of Pest Science, 91(1), 421–435. https://doi.org/10.1007/s10340-017-0900-x
   Web of Science ®Google Scholar
• Sarhan, A. A., Osman, M. A. M., Mandour, N. S., & Abd El-Hady, M. A. (2015). Parasitization capability of four Trichogrammatidae species against the tomato leaf miner, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) under different releasing regimes. Egyptian Journal of Biological Pest Control, 25, 107–112.
   Web of Science ®Google Scholar
• Soares, M. A., Campos, M. R., Passos, L. C., Carvalho, G. A., Haro, M. M., Lavoir, A. V., Biondi, A., Zappala, L., & Desneux, N. (2019). Botanical insecticide and natural enemies: A potential combination for pest management against Tuta absoluta. Journal of Pest Science, 92(4), 1433–1443. https://doi.org/10.1007/s10340-018-01074-5
   Web of Science ®Google Scholar
• SPSS. (2012). SPSS 21.0 brief guide. SPSS Incorporation.
   Google Scholar
• Urbaneja, A., Gonzalez-Cabrera, J., Arno, J., & Gabarra, R. (2012). Prospects for the biological control of Tuta absoluta in tomatoes of the Mediterranean basin. Pest Management Science, 68(9), 1215–1222. https://doi.org/10.1002/ps.3344
   PubMed Web of Science ®Google Scholar
• Zhang, F., Babendreier, D., Wang, Z.-Y., Il, K. S., Zheng, L., Pyon, Y. C., Bai, S. X., Song, K., Ri, J. O., Grossrieder, M., & Kuhlmann, U. (2010). Mass releases of Trichogramma ostriniae increase maize production in DPR Korea. Journal of Applied Entomology, 134(5), 481–490. https://doi.org/10.1111/j.1439-0418.2010.01512.x
   Web of Science ®Google Scholar
• Zouba, A., Chermiti, B., Chraiet, R., & Mahjoubi, K. (2013). Effect of two indigenous Trichogramma species on the infestation level by tomato miner Tuta absoluta in tomato greenhouses in the South-West of Tunisia. Tunisian Journal of Plant Protection, 8, 87–106.
   Google Scholar
• Zouba, A., & Mahjoubi, K. (2010). Biological control of Tuta absoluta (Lepidoptera: Gelechiidae) with release of Trichogramma cacoeciae (Hymenoptera: Trichogrammatidae) in tomato greenhouses in Tunisia. The African Journal of Plant Science and Biotechnology, 4, 85–87.
   Google Scholar