Skip to main content
Log in

Combined Application of Entomopathogenic Nematodes and Insecticides in the Control of Leaf-Miner Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) on Tomato

  • Biological Control
  • Published:
Neotropical Entomology Aims and scope Submit manuscript

Abstract

The present research aimed to investigate the compatibility of entomopathogenic nematodes (EPNs) and registered insecticides for the control of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) in the tomato crop, as well as the susceptibility of pupae of T. absoluta to EPNs combined with different percentages below the recommended dose of compatible chemical insecticides in laboratory conditions and in the greenhouse. The species of EPN used was Heterorhabditis amazonensis JPM4. The insecticides used were Actara®, Premio®, and Warrant®. In the compatibility test between the EPNs and insecticides, the viability and infectivity of the nematodes after contact with the insecticides were evaluated. An assessment of the efficacy of the combined application of different doses of the insecticides and the EPNs on T. absoluta was carried out in the laboratory and greenhouse. The efficacy of the combined application of the insecticides and the EPNs on T. absoluta via soil was carried out at application intervals of 1 and 2 weeks. The EPNs were compatible with the three insecticides tested. In the laboratory, there was an additive effect of the combined application of insecticides and H. amazonensis as the dose of the products increased. In the greenhouse assay, the combined application of EPNs and insecticides induced mortality above 48%, and the combined application of EPNs and Warrant® 75% presented 60% of mortality. The weekly and fortnightly applications were effective in controlling T. absoluta, and there was no difference between the insecticides tested when applied together with the nematodes.

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.

Fig 1
Fig 2
Fig 3

Similar content being viewed by others

References

  • Adams BJ, Nguyen KB (2002) Taxonomy and systematics. In: Gaugler R (ed) Entomopathogenic nematology. CABI International, Wallingford, pp 1–33

    Google Scholar 

  • Apablaza J (1992) La polilla del tomate y su manejo. Tattersal 79:12–13

    Google Scholar 

  • Barrientos ZR, Apasblaza HJ, Norero SA, Estay PP (1998) Temperatura base y constante térmica de desarrollo de la polilla del tomate, Tuta absoluta (Lepidoptera: Gelechiidae). Cienc Invest Agraria 25:133–137

    Article  Google Scholar 

  • Batalla-Carrera L, Morton A, García-del-Pino F (2010) Efficacy of entomopathogenic nematodes against the tomato leafminer Tuta absoluta in laboratory and greenhouse conditions. BioControl 55:523–530

    Article  Google Scholar 

  • Cabanillas HE, Raulston JR (1995) Impact of Steinernema riobravis (Rhabditida: Steinernematidae) on the control of Helicoverpa zea (Lepidoptera: Noctuidae) in corn. J Econ Entomol 88(1):58–64. https://doi.org/10.1093/jee/88.1.58

  • Campos MR, Rodrigues ARS, Silva WM, Silva TBM, Silva VRF, Guedes RNC, Siqueira HAA (2014) Spinosad and the tomato borer Tuta absoluta: a bioinsecticide, an invasive pest threat, and high insecticide resistance. PLoS One 9:e103235. https://doi.org/10.1371/journal.pone.0103235

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • De Cock A, De Clerq P, Tirry L, Degheele D (1996) Toxicity of diafenthiuron and imidacloprid to the predatory bug Podisus maculiventris (Heteroptera: Pentatomidae). Environ Entomol 25(2):476–480. https://doi.org/10.1093/ee/25.2.476

    Article  Google Scholar 

  • Dubovskiy IM, Kryukov VY, Benkovskaya GV, Yaroslavtseva ON, Surina EV, Glupov VV (2010) Activity of detoxificative enzymes system and encapsulation rate in Colorado potato beetle Leptinotarsa decemlineata larvae under organophosphorus insecticide treatment and entomopathogenic fungus Metharizium anisopliae infection. Euroasian Entomol J 9:577–582

    Google Scholar 

  • Dubovskiy IM, Whitten MMA, Yaroslavtseva ON, Greig C, Kryukov VY, Grizanova EV, Mukherjee K, Vilcinskas A, Glupov VV, Butt TM (2013) Can insects develop resistance to insect pathogenic fungi? PLoS One 8:e60248. https://doi.org/10.1371/journal.pone.0060248

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dutky SR, Thompson LV, Cantwe GE (1964) A technique for the mass propagation of the DD-136 nematode. J Insect Pathol 6:417–422

    Google Scholar 

  • European and Mediterranean Plant Prot Organization (EPPO) (2010) Archives of the EPPO Reporting Service. http://archives.eppo.org/EPPO/Reporting/Reporting_Archives.htm. Accessed 10 April 2017

  • Garcia-del-Pino F, Alabern X, Morton A (2013) Efficacy of soil treatments of entomopathogenic nematodes against the larvae, pupae and adults of Tuta absoluta and their interaction with the insecticides used against this insect. BioControl 58:723–731

    Article  CAS  Google Scholar 

  • Girling RD, Ennis D, Dillon AB, Griffin CT (2010) The lethal and sub-lethal consequences of entomopathogenic nematode infestation and exposure for adult pine weevils, Hylobius abietis (Coleoptera: Curculionidae). J Invertebr Pathol 104(3):195–202. https://doi.org/10.1016/j.jip.2010.04.003

    Article  CAS  PubMed  Google Scholar 

  • Gözel Ç, Kasap İ (2015) Efficacy of entomopathogenic nematodes against the tomato leafminer, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) in tomato field. Turk J Entomol 39(3):229–237. https://doi.org/10.16970/ted.84972

  • Imms AD, Richards OW, Davies RG (1977) Imms’ general textbook of entomology. Springer Netherlands, London, p 432

    Google Scholar 

  • Kaakeh N, Kaakeh W, Bennett GW (1996) Topical toxicity of imidacloprid, ftpronil, and seven conventional insecticides to the adult convergent lady beetle (Coleoptera: Coccinellidae). Entomol Sci 31:315–322

    Article  CAS  Google Scholar 

  • Kaya HK, Hara AH (1981) Susceptibility of various species of lepidopterous pupae to the entomogenous nematode Neoaplectona carpocapsae. J Nematol 13:291–294

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kaya HK, Stock SP (1997) Techniques in insect nematology. In: Lacey LA (ed) Manual of techniques in insect pathology. Academic Press, California, pp 281–324

    Chapter  Google Scholar 

  • Koppenhöfer AM, Fuzy EM (2008) Effect of the anthranilic diamide insecticide, chlorantraniliprole, on Heterorhabditis bacteriophora (Rhabditida: Heterorhabditidae) efficacy against white grubs (Coleoptera: Scarabaeidae). BioControl 45:93–102

    Google Scholar 

  • Koppenhöfer AK, Kaya HK (1998) Synergism of imidacloprid and an entomopathogenic nematode: a novel approach to white grub control in turfgrass. J Econ Entomol 91(3):618–623. https://doi.org/10.1093/jee/91.3.618

    Article  Google Scholar 

  • Koppenhöfer AM, Grewal PS, Kaya HK (2000) Synergism of entomopathogenic nematodes and imidacloprid against white grubs: the mechanism. Entomol Exp Appl 94:283–293

    Article  Google Scholar 

  • Koppenhöfer AM, Cowles RC, Cowles EA, Fuzy EM, Baumgartner L (2002) Comparison of neonicotinoid insecticides as synergists for entomopathogenic nematodes. BioControl 24:90–97

    Google Scholar 

  • Li XY, Cowles RS, Cowles EA, Gaugler R, Cox-Foster DL (2007) Relationship between the successful infection by entomopathogenic nematodes and the host immune response. Int J Parasitol 37:365–374. https://doi.org/10.1016/j.ijpara.2006.08.009

    Article  CAS  PubMed  Google Scholar 

  • Negrisoli AS, Garcia MS, Barbosa-Negrisoli CRC (2010) Compatibility of entomopathogenic nematodes (Nematoda: Rhabditida) with registered insecticides for Spodoptera frugiperda (Smith, 1797) (Lepidoptera: Noctuidae) under laboratory conditions. Crop Prot 29:545–549. https://doi.org/10.1016/j.cropro.2009.12.012

    Article  Google Scholar 

  • Nishimatsu T, Jackson J (1998) Interaction of insecticides, entomopathogenic nematodes, and larvae of the western corn rootworm (Coleoptera: Chrysomelidae). J Econ Entomol 9(2): 410–418

  • Parra JRP (1998) Criação de insetos para estudos com patógenos. In: Alves SB (ed) Controle microbiano de insetos. Piracicaba, FEALQ, pp 1015–1038

    Google Scholar 

  • Peters A, Poullot D (2004) Side effects of surfactants and pesticides on entomopathogenic nematodes assessed using advanced IOBC guidelines. IOBC/WPRS Bulletin 27:67–72

    Google Scholar 

  • Pye AE, Burman M (1978) Neoaplectana carpocapsae: infection and reproduction in large pine weevil larvae, Hylobius abietis. Exp Parasitol 46:1–11

    Article  CAS  PubMed  Google Scholar 

  • R CORE TEAM (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Reyes M, Rocha K, Alarc L, Siegwart M, Sauphanor B (2012) Metabolic mechanisms involved in the resistance of field populations of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) to spinosad. Pestic Biochem Physiol 102(1):45–50. https://doi.org/10.1016/j.pestbp.2011.10.008

    Article  CAS  Google Scholar 

  • Robertson JL, Preslier HK (1992) Pesticide Bioassays with Arthropods. Boca Raton, Florida, p 125.

  • Rovesti L, Deseo KV (1990) Compatibility of chemical pesticides with the entomopathogenic nematodes, Steinernema carpocapsae Weiser and S. feltiae Filipjev (Nematoda: Steinernematidae). Nematologica 36:237–245

    Article  Google Scholar 

  • Sabino PHS, Sales FS, Guevara EJ, Moino A Jr, Filgueiras CC (2014) Compatibility of entomopathogenic nematodes (Nematoda: Rhabditida) with insecticides used in the tomato crop. Nematoda 1:e03014. https://doi.org/10.4322/nematoda.03014

    Article  Google Scholar 

  • Shapiro-Ilan DI, Gouge DH, Piggott SJ, Fife JP (2006) Application technology and environmental considerations for use of entomopathogenic nematodes in biological control. Biol Control 38(1):124–133. https://doi.org/10.1016/j.biocontrol.2005.09.005

    Article  Google Scholar 

  • Silva GA, Picanço MC, Bacci L, Crespo ALB, Rosado JF, Guedes RNC (2011) Control failure likelihood and spatial dependence of insecticide resistance in the tomato pinworm, Tuta absoluta. Pest Manag Sci 67(8):913–920. https://doi.org/10.1002/ps.2131

    Article  CAS  PubMed  Google Scholar 

  • Siqueira HAA, Guedes RNC, Picanço MC (2000) Insecticide resistance in populations of Tula absoluta (Lepidoptera: Gelechiidae). Agric For Entomol 2:147–153. https://doi.org/10.1046/j.1461-9563.2000.00062.x

    Article  Google Scholar 

  • Türköz S, Kaşkavalcı G (2016) Determination of the efficacy of some entomopathogenic nematodes against Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) under laboratory conditions. Türk Entomol Dergisi 40(2):175–183. https://doi.org/10.16970/ted.92606

    Article  Google Scholar 

  • Urbaneja A, Vercher R, Navarro V, Porcuna JL, García María F (2007) La polilla del tomate, Tuta absoluta. Phytoma 194:16–23

    Google Scholar 

  • Van Damme VM, Beck BK, Berckmoes E, Moerkens R, Wittemans L, Vis R, Nuyttens D, Casteels HF, Maes M, Tirry L, Clercq P (2016) Efficacy of entomopathogenic nematodes against larvae of Tuta absoluta in the laboratory. Pest Manag Sci 72(9):1702–1709. https://doi.org/10.1002/ps.4195

    Article  CAS  PubMed  Google Scholar 

  • Zappala L, Siscaro G, Biondi A, Molla O, González-Cabrera J, Urbaneja A (2011) Efficacy of sulphur on Tuta absoluta and its side effects on the predator Nesidiocoris tenuis. J Appl Entomol 136: 401–409. https://doi.org/10.1111/j.1439-0418.2011.01662.x

Download references

Acknowledgments

The authors are grateful for financial support from CAPES – the Coordination for Improving Higher Education Personnel.

Author information

Authors and Affiliations

Authors

Contributions

PHSS, ASN, AMJR and FSS planed, designed, and executed experimental work; PHSS and ASN conducted data analyses; PHSS, ASN, VA, AMJR, and CCF wrote the manuscript.

Corresponding author

Correspondence to P H S Sabino.

Additional information

Edited by Geraldo A Carvalho – UFL

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sabino, P.H.S., Negrisoli, A.S., Andaló, V. et al. Combined Application of Entomopathogenic Nematodes and Insecticides in the Control of Leaf-Miner Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) on Tomato. Neotrop Entomol 48, 314–322 (2019). https://doi.org/10.1007/s13744-018-0643-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13744-018-0643-2

Keywords

Navigation