Abstract
Nanopesticides are novel formulations that can be applied against a wide range of insect pests as a sustainable alternative to less effective chemical pesticides. Here, acute toxicity of nano (abamectin-PLA-NS (1%) and abamectin-PLA-NS (0.1%)) and commercial formulations of abamectin was evaluated against the South American tomato pinworm, Tuta absoluta, in laboratory and open-field conditions in northeastern Tunisia. Additionally, side effects of nano and commercial formulations of abamectin were also investigated towards the two predatory mirids Macrolophus pygmaeus and Nesidiocoris tenuis either under laboratory or open-field conditions. Laboratory results of acute toxicity revealed no differences between the tested abamectin formulations (against T. absoluta larvae. LC50 values were 0.28, 0.23, and 0.23 for abamectin EC; 0.30, 0.18, and 0.18 for abamectin-PLA-NS (1%) and 0.57, 0.28, and 0.25 for abamectin-PLA- NS (0.1%) corresponding to three time intervals (24, 72 and 120 h after treatment). Abamectin EC, abamectin-PLA-NS (1%) and abamectin-PLA-NS (0.1%) applied at higher doses (0.6 mL/L and 1.2 mL/L) showed higher efficacy percentages (> 90%) in controlling T. absoluta larvae, fourteen days after treatment in open-field tomatoes. Commercial abamectin formulation showed higher toxicity toward M. pygmaeus adults and N. tenuis nymphs compared to nano formulations applied at the two aforementioned doses. High mortality rates, reaching 100%, were reported for M. pygmaeus adults exposed to 1 and 3 day-old residues for commercial formulation at 0.6 mL/L and 1.2 mL/L in laboratory conditions. However, in open-field tomatoes, low acute toxicity was induced by abamectin-PLA-NS (0.1%), ranging from 25 to 41.17%, compared to abamectin EC, ranging from 58.33 to 94.11%, and abamectin-PLA-NS (1%), ranging from 58.33 to 76.47%, at 0.6 mL/L against N. tenuis nymphs at apical leaves. For middle leaves, only abamectin-PLA-NS (0.1%) applied at 0.3 mL/L did not show significant toxicity against N. tenuis nymphs with low mortality level up to 7%, fourteen days after treatment. The practical implications of these results for enhancing integrated pest management programs of T. absoluta in tomatoes are discussed herein.
Similar content being viewed by others
Availability of data and material
Not applicable.
References
Abbott WS (1925) A method of computing the effectiveness of an insecticide. J Econ Entomol 18:265–267
Arnó J, Gabarra R (2011) Side effects of selected insecticides on the Tuta absoluta (Lepidoptera: Gelechiidae) predators Macrolophus pygmaeus and Nesidiocoris tenuis (Hemiptera: Miridae). J Pest Sci 84:513–520. https://doi.org/10.1007/s10340-011-0384-z
Bawin T, Dujeu D, De Backer L, Francis F, Verheggen FJ (2016) Ability of Tuta absoluta (Lepidoptera: Gelechiidae) to develop on alternative host plant species. Can Entomol 148:434–442. https://doi.org/10.4039/tce.2015.59
Biondi A, Desneux N, Siscaro G, Zappala 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 87:803–812. https://doi.org/10.1016/j.chemosphere.2011.12.082
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. https://doi.org/10.1146/annurev-ento-031616-034933
Braham M, Glida-Gnidez H, Hajji L (2012) Management of the tomato borer, Tuta absoluta in Tunisia with novel insecticides and plant extracts. EPPO Bull 42:291–296. https://doi.org/10.1111/epp.2572
Campolo O, Cherif A, Ricupero M, Siscaro G, Grissa-Lebdi K, Russo A, Cucci LM, Di Pietro P, Satriano C, Desneux N, Biondi A, Zappalà L, Palmeri V (2017) Citrus peel essential oil nanoformulations to control the tomato borer, Tuta absoluta: chemical properties and biological activity. Sci Rep 7:13036. https://doi.org/10.1038/s41598-017-13413-0
Campolo O, Puglisi I, Nunzio Barbagallo R, Cherif A, Ricupero M, Biondi A, Palmeri V, Baglieri A, Zappalà L (2020) Side effects of two citrus essential oil formulations on a generalist insect predator, plant and soil enzymatic activities. Chemosphere 257:127–252. https://doi.org/10.1016/j.chemosphere.2020.127252
Campos MR, Biondi A, Adiga A, Guedes RNC, Desneux N (2017) From the Western Palaearctic region to beyond: Tuta absoluta ten years after invading Europe. J Pest Sci 90:787–796. https://doi.org/10.1007/s10340-017-0867-7
Caparros-Megido R, Haubruge E, Verheggen FJ (2013) Pheromone-based management strategies to control the tomato leafminer, Tuta absoluta (Lepidoptera: Gelechiidae). A review. Biotechnol Agron Soc Environ 17:475–482. https://popups.uliege.be/1780-4507/index.php?id=10229
Cherif A, Attia-Barhoumi S, Mansour R, Zappala L, Grissa-Lebdi K (2019a) Elucidating key biological parameters of Tuta absoluta on different host plants and under various temperature and relative humidity regimes. Entomol Gen 39:1–7. https://doi.org/10.1127/entomologia/2019/0685
Cherif A, Harbaoui K, Zappalà L, Grissa-Lebdi K (2018) Efficacy of mass trapping and insecticides to control Tuta absoluta in Tunisia. J Plant Dis Prot 125:51–61. https://doi.org/10.1007/s41348-017-0140-6
Cherif A, Mansour R, Barhoumi-Attia S, Zappalà L, Grissa-Lebdi K (2019b) 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 Sci Techn 29:149–161. https://doi.org/10.1080/09583157.2018.1542485
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. Environ Exp Biol 11:179–184
Cocco A, Deliperi S, Delrio G (2013) Control of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) in greenhouse tomato crops using the mating disruption technique. J Appl Entomol 137:16–28. https://doi.org/10.1111/j.1439-0418.2012.01735.x
Desneux N, Han P, Mansour R, Arnó J, Brévault T, Campos MR et al (2021) Integrated Pest Management of Tuta absoluta: practical implementations across different regions around the world. J Pest Sci 95:17–39. https://doi.org/10.1007/s10340-021-01442-8
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. https://doi.org/10.1007/s10340-011-0398-6
Desneux N, Wajnberg E, Wyckhuys KAG, Burgio G, Arpaia S, Narváez-Vasquez CA, González-Cabrera J, Catalán 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. https://doi.org/10.1007/s10340-010-0321-6
Ferracini C, Bueno VHP, Dindo ML, Ingegno BL, Luna MG, Gervassio NGS, Sanchez NE, Siscaro G, Van Lenteren JC, Zappalà L, Tavella L (2019) Natural enemies of Tuta absoluta in the Mediterranean basin, Europe and South America. Biocontrol Sci Techn 29:578–609. https://doi.org/10.1080/09583157.2019.1572711
Finney DJ (1971) Probit analysis, 3rd edn. Cambridge University Press, Cambridge, UK
Guedes RNC, Roditakis E, Campos MR, Haddi K, Bielza P, Siqueira HAA, Tsagkarakou A, Vontas J, Nauen R (2019) Insecticide resistance in the tomato pinworm Tuta absoluta: patterns, spread, mechanisms, management and outlook. J Pest Sci 92:1329–1342. https://doi.org/10.1007/s10340-019-01086-9
Haddi K, Berger M, Bielza P, Rapisarda C, Williamson MS, Moores G, Bass C (2017) Mutation in the ace-1 gene of the tomato leaf miner (Tuta absoluta) associated with organophosphates resistance. J Appl Entomol 141:612–619. https://doi.org/10.1111/jen.12386
Han P, Bayram Y, Shaltiel-Harpaz L, Sohrabi F, Saji A, Tair Esenali U, Jalilov A, Ali A, Shashank PR, Ismoilov K, Lu ZZ, Wang S, Zhang GF, Wan FH, Biondi A, Desneux N (2019) Tuta absoluta continues to disperse in Asia: Damage, ongoing management and future challenges. J Pest Sci 92:1317–1327. https://doi.org/10.1007/s10340-018-1062-1
Illakwahhi DT, Srivastava BBL (2019) Improving the Efficacy of Abamectin Using Neem Oil in Controlling Tomato Leaf miners, Tuta absoluta (Meyrick). Advanced J Chem Sect A 2:216–224. https://doi.org/10.33945/SAMI/AJCA.2019.2.216224
Kah M, Beulke S, Tiede K, Hofmann T (2013) Nanopesticides: State of knowledge, environmental fate, and exposure modeling. Crit Rev Environ Sci Technol 43:1823–1867. https://doi.org/10.1080/10643389.2012.671750
Kah M, Hofmann T (2014) Nanopesticide research: Current trends and future priorities. Environ Int 63:224–235. https://doi.org/10.1016/j.envint.2013.11.015
Khoshabi J, Sabahi Q, Sharifian I (2016) Lethal and sublethal effects of abamectin, acetamiprid and indoxacarb on predatory bug, Nesidiocorus tenuis feeding on tomato leafminer, Tuta absoluta. Iranian J Plant Prot Sci 47:71–81. https://doi.org/10.22059/ijpps.2016.59291
Kookana RS, Boxall ABA, Reeves PT, Ashauer R, Beulke S, Chaudhry Q, Cornelis G, Fernandes TF, Gan J, Kah M, Lynch I, Ranville J, Sinclair C, Spurgeon D, Tiede K, Van den Brink PJ (2014) Nanopesticides: guiding, principles for regulatory evaluation of environmental risks. J Agric Food Chem 62:4227–4240. https://doi.org/10.1021/jf500232f
Lade BD, Gogle DP (2019) Nano-biopesticides: Synthesis and applications in plant safety. In: Abd- Elsalam KA, Prasad R (eds) Nanobiotechnology applications in plant protection. Springer International Publishing, Switzerland, pp 169–189
Lee BK, Yun Y, Park K (2016) PLA micro- and nano-particles. Adv Drug Deliver Rev 107:176–191. https://doi.org/10.1016/j.addr.2016.05.020
Lietti MMM, Botto E, Alzogara R (2005) Insecticide Resistance in Argentine Populations of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). Neotrop Entomol 34:113–119. https://doi.org/10.1590/S1519-566X2005000100016
Machekano H, Mutamiswa R, Nyamukondiwa C (2018) Evidence of rapid spread and establishment of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) in semiarid Botswana. Agric Food Secur 7:48. https://doi.org/10.1186/s40066-018-0201-5
Mansour R, Biondi A (2021) Releasing natural enemies and applying microbial and botanical pesticides for managing Tuta absoluta in the MENA region. Phytoparasitica 49:179–194. https://doi.org/10.1007/s12600-020-00849-w
Mansour R, Brevault T, Chailleux A, Cherif A, Grissa-Lebdi K, Haddi K, Mohamed SA, Nofemela RS, Oke A, Sylla S, Tonnang HEZ, Zappalà L, Kenis M, Desneux N, Biondi A (2018) Occurrence, biology, natural enemies and management of Tuta absoluta in Africa. Entomol Gen 38:83–112. https://doi.org/10.1127/entomologia/2018/0749
Mansour R, Cherif A, Attia-Barhoumi S, Zappalà L, Grissa-Lebdi K (2019) Tuta absoluta in Tunisia: ten years of invasion and pest management. Phytoparasitica 47:461–474. https://doi.org/10.1007/s12600-019-00748-9
Martinou AF, Seraphides N, Stavrinides MC (2014) Lethal and behavioral effects of pesticides on the insect predator Macrolophus pygmaeus. Chemosphere 96:167–173. https://doi.org/10.1016/j.chemosphere.2013.10.024
Moscardini VF, Da Costa GP, Carvalho GA, De Oliveira RL, Maia JB, Fonseca e Silva F (2013) Toxicity and sublethal effects of seven insecticides to eggs of the flower bug Orius insidiosus (Say) (Hemiptera: Anthocoridae). Chemosphere 92:490–496. https://doi.org/10.1016/j.chemosphere.2013.01.111
Pradhan S, Mailapalli DR (2020) Nanopesticides for Pest Control. In: Lichtfouse E (ed) Sustainable Agriculture Reviews 40. Springer Nature, Switzerland AG, pp 43–74
Passos LC, Soares MA, Collares LJ, Malagoli I, Desneux N, Carvalho GA (2018) Lethal, sublethal and transgenerational effects of insecticides on Macrolophus basicornis, predator of Tuta absoluta. Entomol Gen 38:127–143. https://doi.org/10.1127/entomologia/2018/0744
Perdikis D, Psaroudaki S, Papadoulis G (2020) Compatibility of Nesidiocoris tenuis and Iphiseius degenerans with insecticides, miticides and fungicides used in tomato crops. Bull Insectol 73:181–192
Pereira RR, Picanço MC, Santana Jr PA, Moreira SS, Guedes RNC, Corrêa AS (2014) Insecticide toxicity and walking response of three pirate bug predators of the tomato leaf miner Tuta absoluta. Agric For Entomol 16:293–301. https://doi.org/10.1111/afe.12059
Pérez-Aguilar DA, Soares MA, Passos LC, Martínez AM, Pineda S, Carvalho GA (2018) Lethal and sublethal effects of insecticides on Engytatus varians (Heteroptera: Miridae), a predator of Tuta absoluta (Lepidoptera: Gelechiidae). Ecotoxicology 27:719–728. https://doi.org/10.1007/s10646-018-1954-0
Roditakis E, Vasakis E, Garcia-Vidal L, del Rosario M-A, Rison JL, Haxaire-Lutun MO, 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. J Pest Sci 91:421–435. https://doi.org/10.1007/s10340-017-0900-x
Sawadogo MW, Somda I, Nacro S, Legreve A, Verheggen FJ (2020) Insecticide susceptibility level and control failure likelihood estimation of Sub-Saharan African populations of tomato leafminer: Evidence from Burkina Faso. Physiol Entomol 45:147–153. https://doi.org/10.1111/phen.12332
Shahzad K, Manzoor F (2019) Nanoformulations and their mode of action in insects: a review of biological interactions. Drug Chem Toxicol 44:1–11. https://doi.org/10.1080/01480545.2018.1525393
Silva JE, Ribeiro LMDS, Vinasco N, Guedes RNC, Siqueira HAA (2019) Field-evolved resistance to chlorantraniliprole in the tomato pinworm Tuta absoluta: inheritance, cross-resistance profile, and metabolism. J Pest Sci 92:1421–1431. https://doi.org/10.1007/s10340-018-1064-z
Siqueira HAA, Guedes RNC, Fragoso DB, Magalhães LC (2001) Abamectin resistance and synergismin brazilian populations of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). Int J Pest Manag 47:247–251. https://doi.org/10.1080/09670870110044634
Soares MA, Campos MR, Passos LC, Carvalho GA, Haro MM, Lavoir AV, Biondi A, Zappalà L, Desneux N (2019) Botanical insecticide and natural enemies: a potential combination for pest management against Tuta absoluta. J Pest Sci 92:1433–1443. https://doi.org/10.1007/s10340-018-01074-5
SPSS (2012) SPSS 21.0 brief guide. SPSS Incorporation, Chicago
Sun C, Zeng Z, Cui H, Verheggen F (2020a) Polymer-based nanoinsecticides: current developments, environmental risks and future challenges: A review. Biotechnol Agron Soc Environ 24:59–69. https://doi.org/10.25518/1780-4507.18497
Sun C, Yu M, Zeng Z, Francis F, Cui H, Verheggen F (2020b) Biocidal activity of polylactic acid-based nano-formulated abamectin on Acyrthosiphon pisum (Hemiptera: Aphididae) and the aphid predator Adalia bipunctata (Coleoptera: Coccinellidae). PLoS ONE 15:e0228817. https://doi.org/10.1371/journal.pone.0228817
Urbaneja A, Montón H, Mollá O (2009) Suitability of the tomato borer Tuta absoluta as prey for Macrolophus pygmaeus and Nesidiocoris tenuis. J Appl Entomol 133:292–296. https://doi.org/10.1111/j.1439-0418.2008.01319.x
Wanumen AC, Carvalho GA, Medina P, Vinuela E, Adan A (2016) Residual acute toxicity of some modern insecticides toward two mirid predators of tomato pests. J Econ Entomol 109:1079–1085. https://doi.org/10.1093/jee/tow059
Zibaee I, Esmaeily M (2017) Effect of sublethal doses of abamectin on demographic traits of tomato leafminer Tuta absoluta (Meyrick 1917) (Lepidoptera: Gelechiidae). J Plant Prot Res 57:256–267. https://doi.org/10.1515/jppr-2017-0036
Acknowledgements
The authors thank the farmers for their valuable contribution to this work.
Funding
Not applicable.
Author information
Authors and Affiliations
Contributions
Asma Cherif: Conceptualization, methodology, technical and material supports, Resources, performing experiments, formal analysis, investigation, validation, writing the original draft. Ramzi Mansour: Conceptualization, Resources, formal analysis, investigation, supervision, validation, writing, review, editing. Changjiao Sun: Technical and material supports, Resources, validation. Kaouthar Grissa-Lebdi: Conceptualization, methodology, technical and material supports, Resources, supervision, validation.
Corresponding author
Ethics declarations
Ethics approval
The ethics are approved.
Consent to participate
The authors approved their participation to this paper.
Consent for publication
The authors approved the publication of the paper.
Conflicts of interest/Competing interests
The authors declare that there is 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
About this article
Cite this article
Cherif, A., Mansour, R., Sun, C. et al. Lethal effects of nano and commercial formulations of abamectin on Tuta absoluta (Meyrick) and its mirid predators Macrolophus pygmaeus and Nesidiocoris tenuis. Int J Trop Insect Sci 42, 2183–2193 (2022). https://doi.org/10.1007/s42690-022-00739-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s42690-022-00739-0